Skip to main content

Advertisement

Log in

Composition-driven Surface Domain Structuring Mediated by Sphingolipids and Membrane-active Proteins

Above the Nano- but under the Micro-scale: Mesoscopic Biochemical/Structural Cross-talk in Biomembranes

  • Review Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

Biomembranes contain a wide variety of lipids and proteins within an essentially two-dimensional structure. The coexistence of such a large number of molecular species causes local tensions that frequently relax into a phase or compositional immiscibility along the lateral and transverse planes of the interface. As a consequence, a substantial microheterogeneity of the surface topography develops and that depends not only on the lipid–protein composition, but also on the lateral and transverse tensions generated as a consequence of molecular interactions. The presence of proteins, and immiscibility among lipids, constitute major perturbing factors for the membrane sculpturing both in terms of its surface topography and dynamics. In this work, we will summarize some recent evidences for the involvement of membrane-associated, both extrinsic and amphitropic, proteins as well as membrane-active phosphohydrolytic enzymes and sphingolipids in driving lateral segregation of phase domains thus determining long-range surface topography.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

GSLs:

Glycosphingolipids

Cer:

N-acylsphingosine (ceramide)

GalCer:

Galβ1-1′Cer

Suphatide:

HSO3-3Galβ1-1′Cer

GluCer:

Glcβ1-1′Cer

Gg4Cer (asialo-GM1):

Galβ1-3GalNAcβ1-4Galβ1-4Glcβ1-1′Cer

GM1 (II3NeuAc-CgOse4Cer):

Galβ1-3GalNAcβ1-4Gal(3-2αNeuAc)β1-4Glcβ1-1′Cer

PC:

Phosphatidylcholine

dpPC:

Dipalmitoylphosphatidylcholine

doPC:

Dioleoylphosphatidylcholine

dsPC:

Distearoylphosphatidylcholine

dmPC:

Dimyristoylphosphatidylcholine

dlPC:

Dilauroylphosphatidylcholine

doPG:

Dioleoylphosphatidylglycerol

dpPE:

Dipalmitoylphosphatidylethanolamine

PIP2 :

Phosphatidylinositol bisphosphate

Ch:

Cholesterol

SM:

Sphingomyelin

NBD-PE:

1,2-Dioleoyl-sn-glycero-3-phosphoethanolamine-N-(7-nitro-2-1,3-bensoxadiazol-4-yl)

Rh-PE:

1,2-Dipalmitoyl-sn-phosphoethanolamine-N-[lyssamine rhodamine B sulfonyl]

DI:

1,1′-Didodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate

HI :

Hexagonal I (micellar) phase

HII :

Hexagonal II (inverse micellar) phase

PLA2 :

Phospholipase A2

PLC:

Phospholipase C

SMase:

Sphingomyelinase

MBP:

Myelin basic protein

PLP:

Folch’s proteolipid

MARCKS:

Myristoylated alanine-rich C-kinase substrate

T m :

Transition temperature

IR:

Infrared spectroscopy

EPR:

Electron paramagnetic resonance

BAM:

Brewster angle microscopy.

References

  1. Roberts, G. (1990). Langmuir-Blodgett films. NY: Plenum Press.

    Google Scholar 

  2. Gorter, E., & Grendel F. (1925). On bimolecular layers of lipoids on the chromocytes of the blood. Journal of Experimental Medicine, 41, 439–443.

    CAS  PubMed  Google Scholar 

  3. Cevc, G., & Marsh D. (1987). Phospholipid bilayers. New York: Wiley-Interscience Publication.

    Google Scholar 

  4. Israelachvili, J. N., Marcelja, S., & Horn, R. G. (1980). Physical principles of membrane organization. Quarterly Reviews of Biophysics, 13, 121–200.

    PubMed  CAS  Google Scholar 

  5. Phillips, M. C. (1972). The physical state of phospholipid and cholesterol in monolayers, bilayers, membranes. In J. F. Danielli, M. D. Rosenberg, & D. A. Cadenhead (Eds.), Progress in surface and membrane science (pp. 139–221). New York: Academic Press.

    Google Scholar 

  6. Maggio, B., Cumar, F. A., & Caputto, R. (1981). Molecular behaviour of glycosphingolipids in interfaces. Possible participation in some properties of nerve membranes. Biochimica et Biophysica Acta, 650, 69–87.

    PubMed  CAS  Google Scholar 

  7. Maggio, B. (1994). The surface behavior of glycosphingolipids in biomembranes: A new frontier of molecular ecology. Progress in Biophysics and Molecular Biology, 62, 55–117.

    PubMed  CAS  Google Scholar 

  8. Maggio, B., Carrer, D. C., Fanani, M. L., Oliveira, R. G., & Rosetti, C. M. (2004). Interfacial behavior of glycosphingolipids and related sphingolipids. Current Opinion in Colloid & Interface Science, 8, 448–458.

    CAS  Google Scholar 

  9. Maggio, B., Fanani, M. L., Rosetti, C. M., & Wilke, N. (2006). Biophysics of sphingolipids II. Glycosphingolipids: An assortment of multiple structural information transducers at the membrane surface. Biochimica et Biophysica Acta, 1758, 1922–1944.

    PubMed  CAS  Google Scholar 

  10. Rilfors, L., & Lindblom, G. (2002). Regulation of lipid composition in biological membranes-biophysical studies of lipids and lipid synthesizing enzymes. Colloids and Surfaces B, Biointerfaces, 26, 112–124.

    CAS  Google Scholar 

  11. Esch, S. W., Williams, T. D., Biswas, S., Chakrabarty, A., & Levine, S. M. (2003). Sphingolipid profile in the CNS of the twitcher (globoid cell leukodystrophy) mouse: A lipidomics approach. Cellular and Molecular Biology (Noisy-le-Grand), 49, 779–787.

    CAS  Google Scholar 

  12. Han, X., & Gross, R. W. (2003). Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: A bridge to lipidomics. Journal of Lipid Research, 44, 1071–1079.

    PubMed  CAS  Google Scholar 

  13. Lee, S. H., Williams, M. V., DuBois, R. N., & Blair, I. A. (2003). Targeted lipidomics using electron capture atmospheric pressure chemical ionization mass spectrometry. Rapid Communications in Mass Spectrometry, 17, 2168–2176.

    PubMed  CAS  Google Scholar 

  14. Lagarde, M., Geloen, A., Record, M., Vance, D., & Spener, F. (2003). Lipidomics is emerging. Biochimica et Biophysica Acta, 1634, 61.

    PubMed  CAS  Google Scholar 

  15. Phillips, M. C., Graham, D. E., & Hauser, H. (1975). Lateral compressibility and penetration into phospholipid monolayers and bilayer membranes. Nature, 254, 154–156.

    PubMed  CAS  Google Scholar 

  16. Thuren, T., Virtanen, J. A., & Kinnunen, P. K. (1986). Estimation of the equilibrium lateral pressure in 1-palmitoyl-2-[6(pyren-1-yl)]hexanoyl-glycerophospholipid liposomes. Chemistry and Physics of Lipids, 41, 329–334.

    PubMed  CAS  Google Scholar 

  17. Dahim, M., Mizuno, N. K., Li, X., Momsen, W. E., Momsen, M. M., & Brockman, H. L. (2002). Physical and photophysical characterization of a BODIPY phosphatidylcholine as a membrane probe. Biophysical Journal, 83, 1511–1524.

    PubMed  CAS  Google Scholar 

  18. Feng, S. (1999). Interpretation of mechanochemical properties of lipid bilayer vesicles from equation of state or pressure-area measurement of the monolayer at the air–water interface or oil–water interface. Langmuir, 15, 998–1010.

    CAS  Google Scholar 

  19. Marsh, D. (1996). Lateral pressure in membranes. Biochimica et Biophysica Acta, 1286, 183–223.

    PubMed  CAS  Google Scholar 

  20. Sackmann, E. (1995). Physical basis of self-organization and function of membranes: Physics of vesicles. In R. Lipowsky & E. Sackmann (Eds.), Structure and dynamics of membranes: From cells to vesicles (pp. 213–298). North-Holland: Elsevier.

    Google Scholar 

  21. Fanani, M. L., & Maggio, B. (2000). Kinetic steps for the hydrolysis of sphingomyelin by Bacillus cereus sphingomyelinase in lipid monolayers. Journal of Lipid Research, 41, 1832–1840.

    PubMed  CAS  Google Scholar 

  22. Bloom, M., Evans, E., & Mouritsen, O. G. (1991). Physical properties of the fluid lipid-bilayer component of cell membranes: A perspective. Quarterly Reviews of Biophysics, 24, 293–397.

    PubMed  CAS  Google Scholar 

  23. McMullen, T. P. W., Lewis, R. N., & McElhaney, R. N. (2004). Cholesterol–phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes. Current Opinion in Colloid & Interface Science, 8, 459–468.

    CAS  Google Scholar 

  24. Lichtenberg, D., Goni, F. M., & Heerklotz, H. (2005). Detergent-resistant membranes should not be identified with membrane rafts. Trends in Biochemical Sciences, 30, 430–436.

    PubMed  CAS  Google Scholar 

  25. Munro, S. (2003). Lipid rafts: Elusive or illusive? Cell, 115, 377–388.

    PubMed  CAS  Google Scholar 

  26. Leidy, C., Gousset, K., Ricker, J., Wolkers, W. F., Tsvetkova, N. M., Tablin, F., & Crowe, J. H. (2004). Lipid phase behavior and stabilization of domains in membranes of platelets. Cell Biochemistry and Biophysics, 40, 123–148.

    PubMed  CAS  Google Scholar 

  27. Ledeen, R. W., Hakomori, S. I., Yates, A. J., Schneider, J. S., & Yu, R. K. (1998). Sphingolipids as signaling modulators in the nervous system. Annals of the New York Academy of Sciences, 845, 1–401.

    Google Scholar 

  28. Hakomori, S. (1990). Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. Journal of Biological Chemistry, 265, 18713–18716.

    PubMed  CAS  Google Scholar 

  29. Maggio, B., & Cumar, F. A. (1975). Experimental allergic encephalomyelitis: Dissociation of neurological symptoms from lipid alterations in brain. Nature, 253, 364–365.

    PubMed  CAS  Google Scholar 

  30. Cumar, F. A., Brady, R. O., Kolodny, E. H., McFarland, V. W., & Mora, P. T. (1970). Enzymatic block in the synthesis of gangliosides in DNA virus-transformed tumorigenic mouse cell lines. Proceedings of the National Academy of Sciences of the USA, 67, 757–764.

    PubMed  CAS  Google Scholar 

  31. Sonnino, S., Prinetti, A., Mauri, L., Chigorno, V., & Tettamanti, G. (2006). Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chemical Reviews, 106, 2111–2125.

    PubMed  CAS  Google Scholar 

  32. Goni, F. M., & Alonso, A. (2006). Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochimica et Biophysica Acta, 1758, 1902–1921.

    PubMed  CAS  Google Scholar 

  33. Maccioni, H. J., Giraudo, C. G., & Daniotti, J. L. (2002). Understanding the stepwise synthesis of glycolipids. Neurochemical Research, 27, 629–636.

    PubMed  CAS  Google Scholar 

  34. Yu, R. K., Bieberich, E., Xia, T., & Zeng, G. (2004). Regulation of ganglioside biosynthesis in the nervous system. Journal of Lipid Research, 45, 783–793.

    PubMed  CAS  Google Scholar 

  35. Fidelio, G. D., Ariga, T., & Maggio, B. (1991). Molecular parameters of gangliosides in monolayers: Comparative evaluation of suitable purification procedures. Journal of Biochemistry (Tokyo), 110, 12–16.

    CAS  Google Scholar 

  36. Orthaber, D., & Glatter, O. (1998). Time and temperature dependent aggregation behaviour of the ganglioside GM1 in aqueous solution. Chemistry and Physics of Lipids, 92, 53–62.

    PubMed  CAS  Google Scholar 

  37. Sot, J., Goni, F. M., & Alonso, A. (2005). Molecular associations and surface-active properties of short- and long-N-acyl chain ceramides. Biochimica et Biophysica Acta, 1711, 12–19.

    PubMed  CAS  Google Scholar 

  38. Sot, J., Aranda, F. J., Collado, M. I., Goni, F. M., & Alonso, A. (2005). Different effects of long- and short-chain ceramides on the gel–fluid and lamellar-hexagonal transitions of phospholipids: A calorimetric, NMR, and X-ray diffraction study. Biophysical Journal, 88, 3368–3380.

    PubMed  CAS  Google Scholar 

  39. Maggio, B. (1992). The molecular electrostatics of glycosphingolipids in oriented interfaces. In M. J. Allen, S. F. Cleary, A. E. Sowers, & D. D. Shillady (Eds.), Charge and field effects in biosystems-III (pp. 69–80). Boston: Birkhauser.

    Google Scholar 

  40. Perillo, M. A., Polo, A., Guidotti, A., Costa E., & Maggio, B. (1993). Molecular parameters of semisynthetic derivatives of gangliosides and sphingosine in monolayers at the air–water interface. Chemistry and Physics of Lipids, 65, 225–238.

    PubMed  CAS  Google Scholar 

  41. Maggio, B., Ariga, T., & Yu, R. K. (1985). Molecular parameters and conformation of globoside and asialo-GM1. Archives of Biochemistry and Biophysics, 241, 14–21.

    PubMed  CAS  Google Scholar 

  42. Ando, S., Yu, R. K., Scarsdale, J. N., Kusunoki, S., & Prestegard, J. H. (1989). High resolution proton NMR studies of gangliosides. Structure of two types of GD3 lactones and their reactivity with monoclonal antibody R24. Journal of Biological Chemistry, 264, 3478–3483.

    PubMed  CAS  Google Scholar 

  43. Riboni, L., Sonnino, S., Acquotti, D., Malesci, A., Ghidoni, R., Egge, H., Mingrino, S., & Tettamanti, G. (1986). Natural occurrence of ganglioside lactones. Isolation and characterization of GD1b inner ester from adult human brain. Journal of Biological Chemistry, 261, 8514–8519.

    PubMed  CAS  Google Scholar 

  44. Maggio, B., Ariga, T., Calderón, R. O., & Yu, R. K. (1997). Ganglioside GD3 and GD3-lactone mediated regulation of the intermolecular organization in mixed monolayers with dipalmitoylphosphatidylcholine. Chemistry and Physics of Lipids, 90, 1–10.

    PubMed  CAS  Google Scholar 

  45. Maggio, B., Ariga, T., & Yu, R. K. (1990). Ganglioside GD3 lactones: Polar head group mediated control of the intermolecular organization. Biochemistry, 29, 8729–8734.

    PubMed  CAS  Google Scholar 

  46. Maggio, B., Cumar, F. A., & Caputto, R. (1978). Surface behaviour of gangliosides and related glycosphingolipids. Biochemical Journal, 171, 559–565.

    PubMed  CAS  Google Scholar 

  47. McDaniel, R. V., Sharp, K., Brooks, D., McLaughlin, A. C., Winiski, A. P., Cafiso, D., & McLaughlin, S. (1986). Electrokinetic and electrostatic properties of bilayers containing gangliosides GM1, GD1a, or GT1. Comparison with a nonlinear theory. Biophysical Journal, 49, 741–752.

    PubMed  CAS  Google Scholar 

  48. Majewski, J., Kuhl, T. L., Kjaer, K., & Smith, G. S. (2001). Packing of ganglioside-phospholipid monolayers: An X-ray diffraction and reflectivity study. Biophysical Journal, 81, 2707–2715.

    PubMed  CAS  Google Scholar 

  49. Diociaiuti, M., Ruspantini, I., Giordani, C., Bordi, F., & Chistolini, P. (2004). Distribution of GD3 in DPPC monolayers: A thermodynamic and atomic force microscopy combined study. Biophysical Journal, 86, 321–328.

    PubMed  CAS  Google Scholar 

  50. Miller, C. E., Majewski, J., Faller, R., Satija, S., & Kuhl, T. L. (2004). Cholera toxin assault on lipid monolayers containing ganglioside GM1. Biophysical Journal, 86, 3700–3708.

    PubMed  CAS  Google Scholar 

  51. Roy, D., & Mukhopadhyay, C. (2001). GD1a in phospholipid bilayer: A molecular dynamics simulation. Journal of Biomolecular Structure & Dynamics, 18, 639–646.

    CAS  Google Scholar 

  52. Singh, D., Jarrell, H. C., Barber, K. R., & Grant, C. W. (1992). Glycosphingolipids: 2H NMR study of the influence of ceramide fatty acid characteristics on the carbohydrate headgroup in phospholipid bilayers. Biochemistry, 31, 2662–2669.

    PubMed  CAS  Google Scholar 

  53. Saxena, K., Duclos, R. I., Zimmermann, P., Schmidt, R. R., & Shipley, G. G. (1999). Structure and properties of totally synthetic galacto- and gluco-cerebrosides. Journal of Lipid Research, 40, 839–849.

    PubMed  CAS  Google Scholar 

  54. Boggs, J. M., Koshy, K. M., & Rangaraj, G. (1984). Effect of fatty acid chain length, fatty acid hydroxylation and various cations on phase behavior of synthetic cerebroside sulfate. Chemistry and Physics of Lipids, 36, 65–89.

    CAS  Google Scholar 

  55. Boggs, J. M. (1987). Lipid intermolecular hydrogen bonding: Influence on structural organization and membrane function. Biochimica et Biophysica Acta, 906, 353–404.

    PubMed  CAS  Google Scholar 

  56. Albon, N., & Baret, J. F. (1983). Comparison and correlation between the properties of lipid molecules in crystals, bilayer dispersions in water and monolayers on a water surface. Journal of Colloid and Interface Science, 92, 545–560.

    CAS  Google Scholar 

  57. Fidelio, G. D., Maggio, B., & Cumar, F. A. (1986). Molecular parameters and physical state of neutral glycosphingolipids and gangliosides in monolayers at different temperatures. Biochimica et Biophysica Acta, 854, 231–239.

    PubMed  CAS  Google Scholar 

  58. Seddon, J. M. (1990). Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochimica et Biophysica Acta, 1031, 1–69.

    PubMed  CAS  Google Scholar 

  59. Shipley, G. G., Avecilla, L. S., & Small, D. M. (1974). Phase behavior and structure of aqueous dispersions of sphingomyelin. Journal of Lipid Research, 15, 124–131.

    PubMed  CAS  Google Scholar 

  60. Sripada, P. K., Maulik, P. R., Hamilton, J. A., & Shipley, G. G. (1987). Partial synthesis and properties of a series of N-acyl sphingomyelins. Journal of Lipid Research, 28, 710–718.

    PubMed  CAS  Google Scholar 

  61. Cullis, P. R., & Hope, M. J. (1980). The bilayer stabilizing role of sphingomyelin in the presence of cholesterol: A 31P NMR study. Biochimica et Biophysica Acta, 597, 533–542.

    PubMed  CAS  Google Scholar 

  62. Siminovitch, D. J., & Jeffrey, K. R. (1981). Orientational order in the choline headgroup of sphingomyelin: A 14N-NMR study. Biochimica et Biophysica Acta, 645, 270–278.

    PubMed  CAS  Google Scholar 

  63. Saez-Cirion, A., Basañez, G., Fidelio, G., Goñi, F. M., Maggio, B., & Alonso, A. (2000). Sphingolipids (galactosylceramide and sulfatide) in lamellar-hexagonal phospholipid phase transitions and in membrane fusion. Langmuir, 16, 8958–8963.

    CAS  Google Scholar 

  64. Sonnino, S., Cantu, L., Corti, M., Acquotti, D., & Venerando, B. (1994). Aggregative properties of gangliosides in solution. Chemistry and Physics of Lipids, 71, 21–45.

    PubMed  CAS  Google Scholar 

  65. Maggio, B. (1985). Geometric and thermodynamic restrictions for the self-assembly of glycosphingolipid-phospholipid systems. Biochimica et Biophysica Acta, 815, 245–258.

    PubMed  CAS  Google Scholar 

  66. Maggio, B., Albert, J., & Yu, R. K. (1988). Thermodynamic-geometric correlations for the morphology of self-assembled structures of glycosphingolipids and their mixtures with dipalmitoylphosphatidylcholine. Biochimica et Biophysica Acta, 945, 145–160.

    PubMed  CAS  Google Scholar 

  67. Basanez, G., Fidelio, G. D., Goni, F. M., Maggio, B., & Alonso, A. (1996). Dual inhibitory effect of gangliosides on phospholipase C-promoted fusion of lipidic vesicles. Biochemistry, 35, 7506–7513.

    PubMed  CAS  Google Scholar 

  68. Maggio, B., Cumar, F. A., & Caputto, R. (1978). Induction of membrane fusion by polysialogangliosides. FEBS Letters, 90, 149–152.

    PubMed  CAS  Google Scholar 

  69. Monferran, C. G., Maggio, B., Roth, G. A., Cumar, F. A., & Caputto, R. (1979). Membrane instability induced by purified myelin components. Its possible relevance to experimental allergic encephalomyelitis. Biochimica et Biophysica Acta, 553, 417–423.

    PubMed  CAS  Google Scholar 

  70. Cumar, F. A., Maggio, B., & Caputto, R. (1980). Neurotransmitter movements in nerve endings. Influence of substances that modify the interfacial potential. Biochimica et Biophysica Acta, 597, 174–182.

    PubMed  CAS  Google Scholar 

  71. Maggio, B., & Yu, R. K. (1989). Interaction and fusion of unilamellar vesicles containing cerebrosides and sulfatides induced by myelin basic protein. Chemistry and Physics of Lipids, 51, 127–136.

    PubMed  CAS  Google Scholar 

  72. Mannock, D. A., Lewis, R. N., Sen, A., & McElhaney, R. N. (1988). The physical properties of glycosyldiacylglycerols. Calorimetric studies of a homologous series of 1,2-di-O-acyl-3-O-(beta-D-glucopyranosyl)-sn-glycerols. Biochemistry, 27, 6852–6859.

    PubMed  CAS  Google Scholar 

  73. Wieslander, A., Ulmius, J., Lindblom, G., & Fontell, K. (1978). Water binding and phase structures for different Acholeplasma laidlawii membrane lipids studied by deuteron nuclear magnetic resonance and X-ray diffraction. Biochimica et Biophysica Acta, 512, 241–253.

    PubMed  CAS  Google Scholar 

  74. McElhaney, R. N. (1984). The structure and function of the Acholeplasma laidlawii plasma membrane. Biochimica et Biophysica Acta, 779, 1–42.

    PubMed  CAS  Google Scholar 

  75. Shipley, G. G., Green, J. P., & Nichols, B. W. (1973). The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochimica et Biophysica Acta, 311, 531–544.

    PubMed  CAS  Google Scholar 

  76. Brentel, I., Selstam, E., & Lindbom, G. (1985). Phase equilibria of mixtures of plant galactolipids: The formation of a bicontinuous cubic phase. Biochimica et Biophysica Acta, 812, 816–826.

    CAS  Google Scholar 

  77. Gruner, S. M. (1985). Intrinsic curvature hypothesis for biomembrane lipid composition: A role for nonbilayer lipids. Proceedings of the National Academy of Sciences of the USA, 82, 3665–3669.

    PubMed  CAS  Google Scholar 

  78. Kulkarni, K., Snyder, D. S., & McIntosh, T. J. (1999). Adhesion between cerebroside bilayers. Biochemistry, 38, 15264–15271.

    PubMed  CAS  Google Scholar 

  79. Boggs, J. M., Menikh, A., & Rangaraj, G. (2000). Trans interactions between galactosylceramide and cerebroside sulfate across apposed bilayers. Biophysical Journal, 78, 874–885.

    Article  PubMed  CAS  Google Scholar 

  80. Bach, D., Sela, B., & Miller, I. R. (1982). Compositional aspects of lipid hydration. Chemistry and Physics of Lipids, 31, 381–394.

    PubMed  CAS  Google Scholar 

  81. Bianco, I. D., Fidelio, G. D., & Maggio, B. (1988). Effect of glycerol on the molecular properties of cerebrosides, sulphatides and gangliosides in monolayers. Biochemical Journal, 251, 613–616.

    PubMed  CAS  Google Scholar 

  82. Arnulphi, C., Levstein, P. R., Ramia, M. E., Martin, C. A., & Fidelio, G. D. (1997). Ganglioside hydration study by 2H-NMR: Dependence on temperature and water/lipid ratio. Journal of Lipid Research, 38, 1412–1420.

    PubMed  CAS  Google Scholar 

  83. Arnulphi, C., Martin, C. A., & Fidelio, G. D. (2003). Mixed lipid aggregates containing gangliosides impose different 2H-NMR dynamical parameters on water environment depending on their lipid composition. Molecular Membrane Biology, 20, 319–327.

    PubMed  CAS  Google Scholar 

  84. Hinz, H. J., Kuttenreich, H., Meyer, R., Renner, M., Frund, R., Koynova, R., Boyanov, A. I., & Tenchov, B. G. (1991). Stereochemistry and size of sugar head groups determine structure and phase behavior of glycolipid membranes: Densitometric, calorimetric, and X-ray studies. Biochemistry, 30, 5125–5138.

    PubMed  CAS  Google Scholar 

  85. Johnston, D. S., Coppard, E., Parera, G. V., & Chapman, D. (1984). Langmuir film balance study of the interactions between carbohydrates and phospholipid monolayers. Biochemistry, 23, 6912–6919.

    CAS  Google Scholar 

  86. Maggio, B., Montich, G. G., & Cumar, F. A. (1988). Surface topography of sulfatide and gangliosides in unilamellar vesicles of dipalmitoylphosphatidylcholine. Chemistry and Physics of Lipids, 46, 137–146.

    PubMed  CAS  Google Scholar 

  87. Montich, G. G., Bustos, M., Maggio, B., & Cumar, F. A. (1985). Micropolarity of interfaces containing anionic and neutral glycosphingolipids as sensed by Merocyanine 540. Chemistry and Physics of Lipids, 38, 319–326.

    CAS  Google Scholar 

  88. Bagatolli, L. A., Maggio, B., Aguilar, F., Sotomayor, C. P., & Fidelio, G. D. (1997). Laurdan properties in glycosphingolipid–phospholipid mixtures: A comparative fluorescence and calorimetric study. Biochimica et Biophysica Acta, 1325, 80–90.

    PubMed  CAS  Google Scholar 

  89. Maggio, B. (2004). Favorable and unfavorable lateral interactions of ceramide, neutral glycosphingolipids and gangliosides in mixed monolayers. Chemistry and Physics of Lipids, 132, 209–224.

    PubMed  CAS  Google Scholar 

  90. Carrer, D. C., & Maggio, B. (2001). Transduction to self-assembly of molecular geometry and local interactions in mixtures of ceramides and ganglioside GM1. Biochimica et Biophysica Acta, 1514, 87–99.

    PubMed  CAS  Google Scholar 

  91. Rosetti, C. M., Oliveira, R. G., & Maggio, B. (2003). Reflectance and topography of glycosphingolipid monolayers at the air–water interface. Langmuir, 19, 377–384.

    CAS  Google Scholar 

  92. Dietrich, C., Bagatolli, L. A., Volovyk, Z. N., Thompson, N. L., Levi, M., Jacobson, K., & Gratton, E. (2001). Lipid rafts reconstituted in model membranes. Biophysical Journal, 80, 1417–1428.

    PubMed  CAS  Google Scholar 

  93. Mohwald, H. (1995). Phospholipids monolayers. In R. Lipowsky & E. Sackmann (Eds.), Structure and dynamics of membranes (pp. 161–211). Amsterdam: Elsevier.

    Google Scholar 

  94. McConnell, H. M. (1991). Structures and transitions in lipid monolayers at the air–water interface. Annual Review of Physical Chemistry, 42, 171–195.

    CAS  Google Scholar 

  95. Oliveira, R. G., & Maggio, B. (2000). Epifluorescence microscopy of surface domain microheterogeneity in myelin monolayers at the air–water interface. Neurochemical Research, 25, 77–86.

    PubMed  CAS  Google Scholar 

  96. Oliveira, R. G., & Maggio, B. (2002). Compositional domain immiscibility in whole myelin monolayers at the air–water interface and Langmuir-Blodgett films. Biochimica et Biophysica Acta, 1561, 238–250.

    PubMed  CAS  Google Scholar 

  97. Rosetti, C. M., Oliveira, R. G., & Maggio, B. (2005). The Folch-Lees proteolipid induces phase coexistence and transverse reorganization of lateral domains in myelin monolayers. Biochimica et Biophysica Acta, 1668, 75–86.

    PubMed  CAS  Google Scholar 

  98. Fanani, M. L., Hartel, S., Oliveira, R. G., & Maggio, B. (2002). Bidirectional control of sphingomyelinase activity and surface topography in lipid monolayers. Biophysical Journal, 83, 3416–3424.

    Article  PubMed  CAS  Google Scholar 

  99. Jost, P. C., & Griffith, O. H. (1980). The lipid–protein interface in biological membranes. Annals of the New York Academy of Sciences, 348, 391–407.

    PubMed  CAS  Google Scholar 

  100. Lee, A. G., Birdsall, N. J., Metcalfe, J. C., Toon, P. A., & Warren, G. B. (1974). Clusters in lipid bilayers and the interpretation of thermal effects in biological membranes. Biochemistry, 13, 3699–3705.

    PubMed  CAS  Google Scholar 

  101. Heerklotz, H. (2002). Triton promotes domain formation in lipid raft mixtures. Biophysical Journal, 83, 2693–2701.

    PubMed  CAS  Google Scholar 

  102. Heerklotz, H., Szadkowska, H., Anderson, T., & Seelig, J. (2003). The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton. Journal of Molecular Biology, 329, 793–799.

    PubMed  CAS  Google Scholar 

  103. Sot, J., Collado, M. I., Arrondo, J. L., Alonso, A., & Goñi, F. M. (2002). Triton X-100-resistant bilayers: Effect of lipid composition and relevance to the raft phenomenon. Langmuir, 18, 2828–2835.

    CAS  Google Scholar 

  104. Kiyokawa, E., Baba, T., Otsuka, N., Makino, A., Ohno, S., & Kobayashi, T. (2005). Spatial and functional heterogeneity of sphingolipid-rich membrane domains. Journal of Biological Chemistry, 280, 24072–24084.

    PubMed  CAS  Google Scholar 

  105. Wilson, B. S., Steinberg, S. L., Liederman, K., Pfeiffer, J. R., Surviladze, Z., Zhang, J., Samelson, L. E., Yang, L. H., Kotula, P. G., & Oliver, J. M. (2004). Markers for detergent-resistant lipid rafts occupy distinct and dynamic domains in native membranes. Molecular Biology of the Cell, 15, 2580–2592.

    PubMed  CAS  Google Scholar 

  106. Heffer-Lauc, M., Lauc, G., Nimrichter, L., Fromholt, S. E., & Schnaar, R. L. (2005). Membrane redistribution of gangliosides and glycosylphosphatidylinositol-anchored proteins in brain tissue sections under conditions of lipid raft isolation. Biochimica et Biophysica Acta, 1686(3), 200–208.

    PubMed  CAS  Google Scholar 

  107. Ramstedt, B., & Slotte, J. P. (2006). Sphingolipids and the formation of sterol-enriched ordered membrane domains. Biochimica et Biophysica Acta, 1758, 1945–1956.

    PubMed  CAS  Google Scholar 

  108. Veatch, S. L., & Keller, S. L. (2005). Seeing spots: Complex phase behavior in simple membranes. Biochimica et Biophysica Acta, 1746, 172–185.

    PubMed  CAS  Google Scholar 

  109. Kahya, N., Scherfeld, D., Bacia, K., Poolman, B., & Schwille, P. (2003). Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. Journal of Biological Chemistry, 278, 28109–28115.

    PubMed  CAS  Google Scholar 

  110. de Almeida, R. F., Fedorov, A., & Prieto, M. (2003). Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: Boundaries and composition of lipid rafts. Biophysical Journal, 85, 2406–2416.

    PubMed  Google Scholar 

  111. Hsueh, Y. W., Giles, R., Kitson, N., & Thewalt, J. (2002). The effect of ceramide on phosphatidylcholine membranes: A deuterium NMR study. Biophysical Journal, 82, 3089–3095.

    PubMed  CAS  Google Scholar 

  112. Carrer, D. C., Schreier, S., Patrito, M., & Maggio, B. (2006). Effects of a short-chain ceramide on bilayer domain formation, thickness, and chain mobility: DMPC and asymmetric ceramide mixtures. Biophysical Journal, 90, 2394–2403.

    PubMed  CAS  Google Scholar 

  113. Wang, T. Y., & Silvius, J. R. (2003). Sphingolipid partitioning into ordered domains in cholesterol-free and cholesterol-containing lipid bilayers. Biophysical Journal, 84, 367–378.

    PubMed  CAS  Google Scholar 

  114. Slotte, J. P., & Bierman, E. L. (1988). Depletion of plasma-membrane sphingomyelin rapidly alters the distribution of cholesterol between plasma membranes and intracellular cholesterol pools in cultured fibroblasts. Biochemical Journal, 250, 653–658.

    PubMed  CAS  Google Scholar 

  115. Holopainen, J. M., Subramanian, M., & Kinnunen, P. K. (1998). Sphingomyelinase induces lipid microdomain formation in a fluid phosphatidylcholine/sphingomyelin membrane. Biochemistry, 37, 17562–17570.

    PubMed  CAS  Google Scholar 

  116. Kolesnick, R. N., Goni, F. M., & Alonso, A. (2000). Compartmentalization of ceramide signaling: Physical foundations and biological effects. Journal of Cellular Physiology, 184, 285–300.

    PubMed  CAS  Google Scholar 

  117. Holopainen, J. M., Brockman, H. L., Brown, R. E., & Kinnunen, P. K. (2001). Interfacial interactions of ceramide with dimyristoylphosphatidylcholine: Impact of the N-acyl chain. Biophysical Journal, 80, 765–775.

    PubMed  CAS  Google Scholar 

  118. Nybond, S., Bjorkqvist, Y. J., Ramstedt, B., & Slotte, J. P. (2005). Acyl chain length affects ceramide action on sterol/sphingomyelin-rich domains. Biochimica et Biophysica Acta, 1718, 61–66.

    PubMed  CAS  Google Scholar 

  119. Huang, H. W., Goldberg, E. M., & Zidovetzki, R. (1998). Ceramides perturb the structure of phosphatidylcholine bilayers and modulate the activity of phospholipase A2. European Biophysics Journal, 27, 361–366.

    PubMed  CAS  Google Scholar 

  120. Pincelli, M. M., Levstein P. R., Fidelio G. D., & Gennaro A. M. (2000). Cholesterol-induced alterations of the packing properties of gangliosides: An EPR study. Chemistry and Physics of Lipids, 104, 193–206.

    PubMed  CAS  Google Scholar 

  121. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C., & London, E. (2001). Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. Journal of Biological Chemistry, 276, 33540–33546.

    PubMed  CAS  Google Scholar 

  122. Masserini, M., & Ravasi, D. (2001). Role of sphingolipids in the biogenesis of membrane domains. Biochimica et Biophysica Acta, 1532, 149–161.

    PubMed  CAS  Google Scholar 

  123. Ruocco, M. J., & Shipley, G. G. (1984). Interaction of cholesterol with galactocerebroside and galactocerebroside-phosphatidylcholine bilayer membranes. Biophysical Journal, 46, 695–707.

    Article  PubMed  CAS  Google Scholar 

  124. Regen, S. L. (2002). Lipid–lipid recognition in fluid bilayers: Solving the cholesterol mystery. Current Opinion in Chemical Biology, 6, 729–735.

    PubMed  CAS  Google Scholar 

  125. Mattjus, P., Malewicz, B., Valiyaveettil, J. T., Baumann, W. J., Bittman, R., & Brown, R. E. (2002). Sphingomyelin modulates the transbilayer distribution of galactosylceramide in phospholipid membranes. Journal of Biological Chemistry, 277, 19476–19481.

    PubMed  CAS  Google Scholar 

  126. Malewicz, B., Valiyaveettil, J. T., Jacob, K., Byun, H. S., Mattjus, P., Baumann, W. J., Bittman, R., & Brown, R. E. (2005). The 3-hydroxy group and 4,5-trans double bond of sphingomyelin are essential for modulation of galactosylceramide transmembrane asymmetry. Biophysical Journal, 88, 2670–2680.

    PubMed  CAS  Google Scholar 

  127. Contreras, F. X., Villar, A. V., Alonso, A., Kolesnick, R. N., & Goni, F. M. (2003). Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. Journal of Biological Chemistry, 278, 37169–37174.

    PubMed  CAS  Google Scholar 

  128. Rogasevskaia, T., & Coorssen, J. R. (2006). Sphingomyelin-enriched microdomains define the efficiency of native Ca(2+)-triggered membrane fusion. Journal of Cell Science, 119, 2688–2694.

    PubMed  CAS  Google Scholar 

  129. Patra, S. K., Alonso, A., & Goni, F. M. (1998). Detergent solubilisation of phospholipid bilayers in the gel state: The role of polar and hydrophobic forces. Biochimica et Biophysica Acta, 1373, 112–118.

    PubMed  CAS  Google Scholar 

  130. Patra, S. K., Alonso, A., Arrondo, J. L., & Goñi, F. M. (1999). Liposomes containing sphingomyelin and cholesterol: Detergent solubilization and infrared spectroscopy studies. Journal of Liposome Research, 9, 247–260.

    CAS  Google Scholar 

  131. Veiga, M. P., Goni, F. M., Alonso, A., & Marsh, D. (2000). Mixed membranes of sphingolipids and glycerolipids as studied by spin-label ESR spectroscopy. A search for domain formation. Biochemistry, 39, 9876–9883.

    PubMed  CAS  Google Scholar 

  132. Veiga, M. P., Arrondo, J. L., Goni, F. M., Alonso, A., & Marsh, D. (2001). Interaction of cholesterol with sphingomyelin in mixed membranes containing phosphatidylcholine, studied by spin-label ESR and IR spectroscopies. A possible stabilization of gel-phase sphingolipid domains by cholesterol. Biochemistry, 40, 2614–2622.

    PubMed  CAS  Google Scholar 

  133. Hwang, J., Tamm, L. K., Bohm, C., Ramalingam, T. S., Betzig, E., & Edidin, M. (1995). Nanoscale complexity of phospholipid monolayers investigated by near-field scanning optical microscopy. Science, 270, 610–614.

    PubMed  CAS  Google Scholar 

  134. Hammond, A. T., Heberle, F. A., Baumgart, T., Holowka, D., Baird, B., & Feigenson, G. W. (2005). Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proceedings of the National Academy of Sciences of the USA, 102, 6320–6325.

    PubMed  CAS  Google Scholar 

  135. Peters, M. W., & Grant, C. W. (1984). Freeze-etch study of an unmodified lectin interacting with its receptors in model membranes. Biochimica et Biophysica Acta, 775, 273–282.

    PubMed  CAS  Google Scholar 

  136. Thompson, T. E., Allietta, M., Brown, R. E., Johnson, M. L., & Tillack, T. W. (1985). Organization of ganglioside GM1 in phosphatidylcholine bilayers. Biochimica et Biophysica Acta, 817, 229–237.

    PubMed  CAS  Google Scholar 

  137. Revesz, T., & Greaves, M. (1975). Ligand-induced redistribution of lymphocyte membrane ganglioside GM1. Nature, 257, 103–106.

    PubMed  CAS  Google Scholar 

  138. Goins, B., Masserini, M., Barisas, B. G., & Freire, E. (1986). Lateral diffusion of ganglioside GM1 in phospholipid bilayer membranes. Biophysical Journal, 49, 849–856.

    PubMed  CAS  Google Scholar 

  139. Kenworthy, A. K., Petranova, N., & Edidin, M. (2000). High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Molecular Biology of the Cell, 11, 1645–1655.

    PubMed  CAS  Google Scholar 

  140. Wang, T. Y., & Silvius, J. R. (2000). Different sphingolipids show differential partitioning into sphingolipid/cholesterol-rich domains in lipid bilayers. Biophysical Journal, 79, 1478–1489.

    PubMed  CAS  Google Scholar 

  141. Pagano, R. E., Watanabe, R., Wheatley, C., & Dominguez, M. (2000). Applications of BODIPY-sphingolipid analogs to study lipid traffic and metabolism in cells. Methods in Enzymology, 312, 523–534.

    PubMed  CAS  Google Scholar 

  142. Klausner, R. D., & Wolf, D. E. (1980). Selectivity of fluorescent lipid analogues for lipid domains. Biochemistry, 19, 6199–6203.

    PubMed  CAS  Google Scholar 

  143. Dahlen, B., & Pascher, I. (1979). Molecular arrangement in sphingolipids. Thermotropic phase behaviour of tetracosanoylphytosphingosine. Chemistry and Physics of Lipids, 24, 119–133.

    CAS  Google Scholar 

  144. O´Brien, J. S., & Rouser, G. (1964). The fatty acid composition of brain sphingolipids: Sphingomyelin, ceramide, cerebroside and cerebroside sulfate. Journal of Lipid Research, 5, 339–342.

    CAS  Google Scholar 

  145. DeVries, G. H., & Norton W. T. (1974). The fatty acid composition of sphingolipids from bovine CNS axons and myelin. Journal of Neurochemistry, 22, 251–257.

    PubMed  CAS  Google Scholar 

  146. Huang, C., & Mason, J. T. (1986). Structure and properties of mixed-chain phospholipid assemblies. Biochimica et Biophysica Acta, 864, 423–470.

    PubMed  CAS  Google Scholar 

  147. Mehlhorn, I. E., Florio, E., Barber, K. R., Lordo, C., & Grant, C. W. (1988). Evidence that trans-bilayer interdigitation of glycosphingolipid long chain fatty acids may be a general phenomenon. Biochimica et Biophysica Acta, 939, 151–159.

    PubMed  CAS  Google Scholar 

  148. Boggs, J. M., & Koshy, K. M. (1994). Do the long fatty acid chains of sphingolipids interdigitate across the center bilayer of shorter chain symmetric phospholipids? Biochimica et Biophysica Acta, 1189, 233–241.

    PubMed  CAS  Google Scholar 

  149. Nabet, A., Boggs, J. M., & Pezolet, M. (1996). Study by infrared spectroscopy of the interdigitation of C26:0 cerebroside sulfate into phosphatidylcholine bilayers. Biochemistry, 35, 6674–6683.

    PubMed  CAS  Google Scholar 

  150. Perillo, M. A., Scarsdale, N. J., Yu, R. K., & Maggio, B. (1994). Modulation by gangliosides of the lamellar-inverted micelle (hexagonal II) phase transition in mixtures containing phosphatidylethanolamine and dioleoylglycerol. Proceedings of the National Academy of Sciences of the USA, 91, 10019–10023.

    PubMed  CAS  Google Scholar 

  151. van Gorkom, L. C., Cheetham, J. J., & Epand, R. M. (1995). Ganglioside GD1a generates domains of high curvature in phosphatidylethanolamine liposomes as determined by solid state 31P-NMR spectroscopy. Chemistry and Physics of Lipids, 76, 103–108.

    PubMed  Google Scholar 

  152. Goni, F. M., Contreras, F. X., Montes, L. R., Sot, J., & Alonso, A. (2005). Biophysics (and sociology) of ceramides. Biochemical Society Symposium, 177–188.

  153. Siegel, D. P., & Epand, R. M. (1997). The mechanism of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: Implications for membrane fusion mechanisms. Biophysical Journal, 73, 3089–3111.

    PubMed  CAS  Google Scholar 

  154. Maggio, B., & Yu, R. K. (1992). Modulation by glycosphingolipids of membrane–membrane interactions induced by myelin basic protein and melittin. Biochimica et Biophysica Acta, 1112, 105–114.

    PubMed  CAS  Google Scholar 

  155. Goins, B., & Freire, E. (1985). Lipid phase separations induced by the association of cholera toxin to phospholipid membranes containing ganglioside GM1. Biochemistry, 24, 1791–1797.

    PubMed  CAS  Google Scholar 

  156. Goins, B., & Freire, E. (1988). Thermal stability and intersubunit interactions of cholera toxin in solution and in association with its cell-surface receptor ganglioside GM1. Biochemistry, 27, 2046–2052.

    PubMed  CAS  Google Scholar 

  157. Dalziel, A. W., Lipka, G., Chowdhry, B. Z., Sturtevant, J. M., & Schafer, D. E. (1984). Effects of ganglioside GM1 on the thermotropic behavior of cholera toxin B subunit. Molecular and Cellular Biochemistry, 63, 83–91.

    PubMed  CAS  Google Scholar 

  158. Cumar, F. A., Maggio, B., & Caputto, R. (1982). Ganglioside-cholera toxin interactions: A binding and lipid monolayer study. Molecular and Cellular Biochemistry, 46, 155–160.

    PubMed  CAS  Google Scholar 

  159. Schiavo, G., Demel, R., & Montecucco, C. (1991). On the role of polysialoglycosphingolipids as tetanus toxin receptors. A study with lipid monolayers. European Journal of Biochemistry, 199, 705–711.

    PubMed  CAS  Google Scholar 

  160. Fishman, P. H. (1982). Role of membrane gangliosides in the binding and action of bacterial toxins. Journal of Membrane Biology, 69, 85–97.

    PubMed  CAS  Google Scholar 

  161. Fidelio, G. D., Maggio, B., & Cumar, F. A. (1986). Stability and penetration of soluble and membrane proteins in interfaces. Anales de la Asociacion Química Argentina, 74, 801–813.

    Google Scholar 

  162. Epand, R. M., & Moscarello, M. A. (1982). The effects of bovine myelin basic protein on the phase transition properties of sphingomyelin. Biochimica et Biophysica Acta, 685, 230–232.

    PubMed  CAS  Google Scholar 

  163. Maggio, B., Ariga, T., Sturtevant, J. M., & Yu, R. K. (1985). Thermotropic behavior of glycosphingolipids in aqueous dispersions. Biochemistry, 24, 1084–1092.

    PubMed  CAS  Google Scholar 

  164. Maggio, B., Sturtevant, J. M., & Yu, R. K. (1987). Effect of myelin basic protein on the thermotropic behavior of aqueous dispersions of neutral and anionic glycosphingolipids and their mixtures with dipalmitoylphosphatidylcholine. Journal of Biological Chemistry, 262, 2652–2659.

    PubMed  CAS  Google Scholar 

  165. Fidelio, G. D., Maggio, B., & Cumar, F. A. (1982). Interaction of soluble and membrane proteins with monolayers of glycosphingolipids. Biochemical Journal 203, 717–725.

    PubMed  CAS  Google Scholar 

  166. Maggio, B., Fidelio, G. D., Cumar, F. A., & Yu, R. K. (1986). Molecular interactions and thermotropic behavior of glycosphingolipids in model membrane systems. Chemistry and Physics of Lipids, 42, 49–63.

    PubMed  CAS  Google Scholar 

  167. Papahadjopoulos, D., Moscarello, M., Eylar, E. H., & Isac, T. (1975). Effects of proteins on thermotropic phase transitions of phospholipid membranes. Biochimica et Biophysica Acta, 401, 317–335.

    PubMed  CAS  Google Scholar 

  168. Maggio, B., Rosetti, C. M., Borioli, G. A., Fanani, M. L., & Del Boca, M. (2005). Protein-mediated surface structuring in biomembranes. Brazilian Journal of Medical and Biological Research, 38, 1735–1748.

    PubMed  CAS  Google Scholar 

  169. Whitmarsh, A. J. (2006). Regulation of gene transcription by mitogen-activated protein kinase signaling pathways. Biochimica et Biophysica Acta, 1773, 1285–1298.

    PubMed  Google Scholar 

  170. Newman, J. R., & Keating, A. E. (2003). Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science, 300, 2097–2101.

    PubMed  CAS  Google Scholar 

  171. Vinson, C., Myakishev, M., Acharya, A., Mir, A. A., Moll, J. R., & Bonovich, M. (2002). Classification of human B-ZIP proteins based on dimerization properties. Molecular and Cellular Biology, 22, 6321–6335.

    PubMed  CAS  Google Scholar 

  172. Dyson, H. J., & Wright, P. E. (2005). Intrinsically unstructured proteins and their functions. Nature Reviews Molecular Cell Biology, 6, 197–208.

    PubMed  CAS  Google Scholar 

  173. Glover, J. N., & Harrison, S. C. (1995). Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature, 373, 257–261.

    PubMed  CAS  Google Scholar 

  174. Kohler, J. J., & Schepartz, A. (2001). Kinetic studies of Fos.Jun.DNA complex formation: DNA binding prior to dimerization. Biochemistry, 40, 130–142.

    PubMed  CAS  Google Scholar 

  175. Kim, Y. S., Kim, S. G., Park, J. E., Park, H. Y., Lim, M. H., Chua, N. H., & Park, C. M. (2006). A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell, 18, 3132–3144.

    PubMed  CAS  Google Scholar 

  176. Gil, G. A., Bussolino, D. F., Portal, M. M., Pecchio, A. A., Renner, M. L., Borioli, G. A., Guido, M. E., & Caputto, B. L. (2004). c-Fos activated phospholipid synthesis is required for neurite elongation in differentiating PC12 cells. Molecular Biology of the Cell, 15, 1881–1894.

    PubMed  CAS  Google Scholar 

  177. Borioli, G. A., Caputto, B. L., & Maggio, B. (2001). c-Fos is surface active and interacts differentially with phospholipid monolayers. Biochemical and Biophysical Research Communications 280, 9–13.

    PubMed  CAS  Google Scholar 

  178. Santagata, S., Boggon, T. J., Baird, C. L., Gomez, C. A., Zhao, J., Shan, W. S., Myszka, D. G., & Shapiro, L. (2001). G-protein signaling through tubby proteins. Science, 292, 2041–2050.

    PubMed  CAS  Google Scholar 

  179. Del Boca, M., Caputto, B. L., Maggio, B., & Borioli, G. A. (2005). c-Jun interacts with phospholipids and c-Fos at the interface. Journal of Colloid and Interface Science, 287, 80–84.

    PubMed  Google Scholar 

  180. Borioli, G. A., Caputto, B. L., & Maggio, B. (2004). Phospholipase activity is modulated by c-Fos through substrate expansion and hyperpolarization. FEBS Letters, 570, 82–86.

    PubMed  CAS  Google Scholar 

  181. Borioli, G. A., Caputto, B. L., & Maggio, B. (2005). c-Fos and phosphatidylinositol-4,5-bisphosphate reciprocally reorganize in mixed monolayers. Biochimica et Biophysica Acta, 1668, 41–52.

    PubMed  CAS  Google Scholar 

  182. Borioli, G. A., & Maggio, B. (2006). Surface thermodynamics reveals selective structural information storage capacity of c-Fos-phospholipid interactions. Langmuir, 22, 1775–1781.

    PubMed  CAS  Google Scholar 

  183. Glaser, M., Wanaski, S., Buser, C. A., Boguslavsky, V., Rashidzada, W., Morris, A., Rebecchi, M., Scarlata, S. F., Runnels, L. W., Prestwich, G. D., Chen, J., Aderem, A., Ahn, J., & McLaughlin, S. (1996). Myristoylated alanine-rich C kinase substrate (MARCKS) produces reversible inhibition of phospholipase C by sequestering phosphatidylinositol 4,5-bisphosphate in lateral domains. Journal of Biological Chemistry, 271, 26187–26193.

    PubMed  CAS  Google Scholar 

  184. Laux, T., Fukami, K., Thelen, M., Golub, T., Frey, D., & Caroni, P. (2000). GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. Journal of Cell Biology, 149, 1455–1472.

    PubMed  CAS  Google Scholar 

  185. Sundaram, M., Cook, H. W., & Byers, D. M. (2004). The MARCKS family of phospholipid binding proteins: Regulation of phospholipase D and other cellular components. Biochemistry and Cell Biology, 82, 191–200.

    PubMed  CAS  Google Scholar 

  186. Gatlin, J. C., Estrada-Bernal, A., Sanford, S. D., & Pfenninger, K. H. (2006). Myristoylated, alanine-rich C-kinase substrate phosphorylation regulates growth cone adhesion and pathfinding. Molecular Biology of the Cell, 17, 5115–5130.

    PubMed  CAS  Google Scholar 

  187. Gambhir, A., Hangyas-Mihalyne, G., Zaitseva, I., Cafiso, D. S., Wang, J., Murray, D., Pentyala, S. N., Smith, S. O., & McLaughlin, S. (2004). Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins. Biophysical Journal, 86, 2188–2207.

    PubMed  CAS  Google Scholar 

  188. Victor, K., Jacob, J., & Cafiso, D. S. (1999). Interactions controlling the membrane binding of basic protein domains: Phenylalanine and the attachment of the myristoylated alanine-rich C-kinase substrate protein to interfaces. Biochemistry, 38, 12527–12536.

    PubMed  CAS  Google Scholar 

  189. Cho, W., & Stahelin, R. V. (2005). Membrane–protein interactions in cell signaling and membrane trafficking. Annual Review of Biophysics and Biomolecular Structure, 34, 119–151.

    PubMed  CAS  Google Scholar 

  190. Elortza, F., Mohammed, S., Bunkenborg, J., Foster, L. J., Nuhse, T. S., Brodbeck, U., Peck, S. C., & Jensen, O. N. (2006). Modification-specific proteomics of plasma membrane proteins: Identification and characterization of glycosylphosphatidylinositol-anchored proteins released upon phospholipase D treatment. Journal of Proteome Research, 5, 935–943.

    PubMed  CAS  Google Scholar 

  191. Portal, M. M., Ferrero, G. O., & Caputto, B. L. (2006). N-terminal c-Fos tyrosine phosphorylation regulates c-Fos/ER association and c-Fos-dependent phospholipid synthesis activation. Oncogene, 26, 3551–3558.

    PubMed  Google Scholar 

  192. Antonny, B., Beraud-Dufour, S., Chardin, P., & Chabre, M. (1997). N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange. Biochemistry, 36, 4675–4684.

    PubMed  CAS  Google Scholar 

  193. Cornell, R. B., & Northwood, I. C. (2000). Regulation of CTP:phosphocholine cytidylyltransferase by amphitropism and relocalization. Trends in Biochemical Sciences, 25, 441–447.

    PubMed  CAS  Google Scholar 

  194. Escriba, P. V., Ozaita, A., Ribas, C., Miralles, A., Fodor, E., Farkas, T., & Garcia-Sevilla, J. A. (1997). Role of lipid polymorphism in G protein–membrane interactions: Nonlamellar-prone phospholipids and peripheral protein binding to membranes. Proceedings of the National Academy of Sciences of the USA, 94, 11375–11380.

    PubMed  CAS  Google Scholar 

  195. Attard, G. S., Templer, R. H., Smith, W. S., Hunt, A. N., & Jackowski, S. (2000). Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress. Proceedings of the National Academy of Sciences of the USA, 97, 9032–9036.

    PubMed  CAS  Google Scholar 

  196. Borioli, G. A., Fanani, M. L., Caputto, B. L., & Maggio, B. (2002). c-Fos is a surface pressure-dependent diverter of phospholipase activity. Biochemical and Biophysical Research Communications, 295, 964–969.

    PubMed  CAS  Google Scholar 

  197. Bussolino, D. F., Guido, M. E., Gil, G. A., Borioli, G. A., Renner, M. L., Grabois, V. R., Conde, C. B., & Caputto, B. L. (2001). c-Fos associates with the endoplasmic reticulum and activates phospholipid metabolism. FASEB Journal, 15, 556–558.

    PubMed  CAS  Google Scholar 

  198. Ivorra, C., Kubicek, M., Gonzalez, J. M., Sanz-Gonzalez, S. M., Alvarez-Barrientos, A., O’Connor, J. E., Burke, B., & Andres, V. (2006). A mechanism of AP-1 suppression through interaction of c-Fos with lamin A/C. Genes & Development, 20, 307–320.

    CAS  Google Scholar 

  199. Seelig, J., Macdonald, P. M., & Scherer, P. G. (1987). Phospholipid head groups as sensors of electric charge in membranes. Biochemistry, 26, 7535–7541.

    PubMed  CAS  Google Scholar 

  200. Benvegnu, D. J., & McConnell, H. M. (1993). Surface dipole densities in lipid monolayers. Journal of Physical Chemistry, 97, 6686–6691.

    CAS  Google Scholar 

  201. Lee, K. Y., Klingler, J. F., & McConnell, H. M. (1994). Electric field-induced concentration gradients in lipid monolayers. Science, 263, 655–658.

    PubMed  CAS  Google Scholar 

  202. Groves, J. T., Boxer, S. G., & McConnell, H. M. (1998). Electric field-induced critical demixing in lipid bilayer membranes. Proceedings of the National Academy of Sciences of the USA, 95, 935–938.

    PubMed  CAS  Google Scholar 

  203. Nassoy, P., Birch, W. R., Andelman, D., & Rondelez, F. (1996). Hydrodynamic mapping of two-dimensional electric fields in monolayers. Physical Review Letters, 76, 455–458.

    PubMed  CAS  Google Scholar 

  204. Neumann, E., Sowers, A. E., & Jordan, C. A. (1989). Electroporation and electrofusion in cell biology. New York: Plenum Press.

  205. Abidor, I. G., & Sowers, A. E. (1992). The coaxial-pore mechanism of cell membrane electrofusion: Theory and experiment. In M. J. Allen, S. F. Cleary, A. E. Sowers, & D. D. Shillady (Eds.), Charge and field effects in biosystems-3 (pp. 375–410). Boston: Birkhauser Press.

    Google Scholar 

  206. Despa, S. I. (1992). A model for membrane potential changes during mitogenic simulation of lymphocytes. In M. J. Allen, S. F. Cleary, & A. E. Sowers (Eds.), Charge and field effects in biosystems-4 (pp. 22–38). Virginia: World Scientific.

    Google Scholar 

  207. Markov, M. S., Ryoby, J. T., Kauffman, J. J., & Pilla, A. A. (1992). Extremely weak AC and DC magnetic fields significantly affect myosin phosphorylation. In M. J. Allen, S. F. Cleary, A. E. Sowers, & D. D. Shillady (Eds.), Charge and field effects in biosystems-3 (pp. 225–230). Boston: Birkhauser.

    Google Scholar 

  208. Stulen, G. (1981). Electric field effects on lipid membrane structure. Biochimica et Biophysica Acta, 640, 621–627.

    PubMed  CAS  Google Scholar 

  209. Teissie, J., & Tsong, T. Y. (1981). Electric field induced transient pores in phospholipid bilayer vesicles. Biochemistry, 20, 1548–1554.

    PubMed  CAS  Google Scholar 

  210. Lopez, A., Rols, M. P., & Teissie, J. (1988). 31P NMR analysis of membrane phospholipid organization in viable, reversibly electropermeabilized Chinese hamster ovary cells. Biochemistry, 27, 1222–1228.

    PubMed  CAS  Google Scholar 

  211. Kwee, S., & Roskmark, P. (1994). Changes in cell proliferation due to environment electromagnetic fields. In M. J. Allen, S. F. Cleary, & A. E. Sowers (Eds.), Charge and field effects in biosystems-4 (pp. 255–259). Singapore: World Scientific Pub. Co.

  212. Tsong, T. Y., & Astumian, R. D. (1988). Electroconformational coupling: How membrane-bound ATPase transduces energy from dynamic electric fields. Annual Review of Physiology, 50, 273–290.

    PubMed  CAS  Google Scholar 

  213. Thuren, T., Tulkki, A. P., Virtanen, J. A., & Kinnunen, P. K. (1987). Triggering of the activity of phospholipase A2 by an electric field. Biochemistry, 26, 4907–4910.

    PubMed  CAS  Google Scholar 

  214. Maggio, B. (1999). Modulation of phospholipase A2 by electrostatic fields and dipole potential of glycosphingolipids in monolayers. Journal of Lipid Research, 40, 930–939.

    PubMed  CAS  Google Scholar 

  215. Liu, D. S., Astumian, R. D., & Tsong, T. Y. (1990). Activation of Na+ and K+ pumping modes of (Na,K)-ATPase by an oscillating electric field. Journal of Biological Chemistry, 265, 7260–7267.

    PubMed  CAS  Google Scholar 

  216. Graziana, A., Ranjeva, R., & Teissie, J. (1990). External electric fields stimulate the electrogenic calcium/sodium exchange in plant protoplasts. Biochemistry, 29, 8313–8318.

    PubMed  CAS  Google Scholar 

  217. Lin, Y., Nielsen, R., Murray, D., Hubbell, W. L., Mailer, C., Robinson, B. H., & Gelb, M. (1998). Docking phospholipase A2 on membranes using electrostatic potential-modulated spin relaxation magnetic resonance. Science, 279, 1925–1929.

    PubMed  CAS  Google Scholar 

  218. Muderhwa, J. M., & Brockman, H. L. (1992). Lateral lipid distribution is a major regulator of lipase activity. Implications for lipid-mediated signal transduction. Journal of Biological Chemistry, 267, 24184–24192.

    PubMed  CAS  Google Scholar 

  219. Wang, M. M., Olsher, M., Sugar, I. P., & Chong, P. L. (2004). Cholesterol superlattice modulates the activity of cholesterol oxidase in lipid membranes. Biochemistry, 43, 2159–2166.

    PubMed  CAS  Google Scholar 

  220. Klinger J. F., & McConnell, H. M. (1993). Field-gradient electrophoresis of lipid domains. Journal of Physical Chemistry, 97, 2962–2966.

    Google Scholar 

  221. Heckl W. M., Miller, A., & Möhwald, H. (1988). Electric-field-induced domain movement in phospholipid monolayers. Thin Solid Films, 159, 125–132.

    CAS  Google Scholar 

  222. Szabo, I., Adams, C., & Gulbins, E. (2004). Ion channels and membrane rafts in apoptosis. Pflugers Archiv, 448, 304–312.

    PubMed  CAS  Google Scholar 

  223. Moczydlowski, E., Alvarez, O., Vergara, C., & Latorre, R. (1985). Effect of phospholipid surface charge on the conductance and gating of a Ca2+-activated K+ channel in planar lipid bilayers. Journal of Membrane Biology, 83, 273–282.

    PubMed  CAS  Google Scholar 

  224. Park, J. B., Kim, H. J., Ryu, P. D., & Moczydlowski, E. (2003). Effect of phosphatidylserine on unitary conductance and Ba2+ block of the BK Ca2+-activated K+ channel: Re-examination of the surface charge hypothesis. Journal of General Physiology, 121, 375–397.

    PubMed  CAS  Google Scholar 

  225. Miller, A., Helm, C., & Mohwald, H. (1987). The colloid nature of phospholipid monolayer. Journal de Physique , 48, 693–701.

    CAS  Google Scholar 

  226. Wilke, N., Dassie, S. A., Leiva, E. P., & Maggio, B. (2006). Externally applied electric fields on immiscible lipid monolayers: Repulsion between condensed domains precludes domain migration. Langmuir, 22, 9664–9670.

    PubMed  CAS  Google Scholar 

  227. Hughes, D., Pailthorpe, B., & White, L. (1981). The translational and rotational drag on a cylinder moving in a membrane. Journal of Fluid Mechanics, 110, 349–372.

    CAS  Google Scholar 

  228. Mi, L., & Sui, S. (1996). Effects of an externally applied electric field on the static redistribution of monolayer domains. Langmuir, 12, 3743–3746.

    CAS  Google Scholar 

  229. Andelman D., Brochard, F., & Joanny, J. F. (1987). Phase transition in langmuir monolayers of polar molecules. Journal of Chemical Physics, 86, 3673–3681.

    CAS  Google Scholar 

  230. Wilke, N., & Maggio, B. (2006). Effect of externally applied electrostatic fields on the surface topography of ceramide-enriched domains in mixed monolayers with sphingomyelin. Biophysical Chemistry, 122, 36–42.

    PubMed  CAS  Google Scholar 

  231. Perillo, M. A., Guidotti, A., Costa, E., Yu, R. K., & Maggio, B. (1994). Modulation of phospholipases A2 and C activities against dilauroylphosphorylcholine in mixed monolayers with semisynthetic derivatives of ganglioside and sphingosine. Molecular Membrane Biology, 11, 119–126.

    PubMed  CAS  Google Scholar 

  232. Scott, D. L., White, S. P., Otwinowski, Z., Yuan, W., Gelb, M. H., & Sigler, P. B. (1990). Interfacial catalysis: The mechanism of phospholipase A2. Science, 250, 1541–1546.

    PubMed  CAS  Google Scholar 

  233. Wilke, N., Baruzzi, A. M., & Maggio, B. (2001). Sphingolipid monolayers in the air–water interface and electrochemical behavior of the films transferred onto glassy carbon electrodes. Langmuir, 17, 3980–3986.

    CAS  Google Scholar 

  234. Wilke, N., Baruzzi, A. M., Maggio, B., Perez, M. A., & Teijelo, M. L. (2005). Properties of galactocerebroside layers transferred to glassy carbon electrodes: Effect of an applied electric field. Colloids and Surfaces B, Biointerfaces, 41, 223–231.

    PubMed  CAS  Google Scholar 

  235. Jain, M. K., & Berg, O. G. (1989). The kinetics of interfacial catalysis by phospholipase A2 and regulation of interfacial activation: Hopping versus scooting. Biochimica et Biophysica Acta, 1002, 127–156.

    PubMed  CAS  Google Scholar 

  236. Arni, R. K., & Ward, R. J. (1996). Phospholipase A2—a structural review. Toxicon, 34, 827–841.

    PubMed  CAS  Google Scholar 

  237. Aloulou, A., Rodriguez, J. A., Fernandez, S., van Oosterhout, D., Puccinelli, D., & Carriere, F. (2006). Exploring the specific features of interfacial enzymology based on lipase studies. Biochimica et Biophysica Acta, 1761, 995–1013.

    PubMed  CAS  Google Scholar 

  238. Janmey, P. A., & Kinnunen, P. K. (2006). Biophysical properties of lipids and dynamic membranes. Trends in Cell Biology, 16, 538–546.

    PubMed  CAS  Google Scholar 

  239. Maggio, B., Fanani, M. L., & Oliveira, R. G. (2002). Biochemical and structural information transduction at the mesoscopic level in biointerfaces containing sphingolipids. Neurochemical Research, 27, 547–557.

    PubMed  CAS  Google Scholar 

  240. Fanani, M. L., Topham, M. K., Walsh, J. P., & Epand, R. M. (2004). Lipid modulation of the activity of diacylglycerol kinase alpha- and zeta-isoforms: Activation by phosphatidylethanolamine and cholesterol. Biochemistry, 43, 14767–14777.

    PubMed  CAS  Google Scholar 

  241. Ahyayauch, H., Villar, A. V., Alonso, A., & Goni, F. M. (2005). Modulation of PI-specific phospholipase C by membrane curvature and molecular order. Biochemistry, 44, 11592–11600.

    PubMed  CAS  Google Scholar 

  242. Boguslavsky, V., Rebecchi, M., Morris, A. J., Jhon, D. Y., Rhee, S. G., & McLaughlin, S. (1994). Effect of monolayer surface pressure on the activities of phosphoinositide-specific phospholipase C-beta 1, -gamma 1, and -delta 1. Biochemistry, 33, 3032–3037.

    PubMed  CAS  Google Scholar 

  243. Fanani, M. L., & Maggio, B. (1997). Mutual modulation of sphingomyelinase and phospholipase A2 activities against mixed lipid monolayers by their lipid intermediates and glycosphingolipids. Molecular Membrane Biology, 14, 25–29.

    Article  PubMed  CAS  Google Scholar 

  244. Kinnunen, P. K., Koiv, A., Lehtonen, J. Y. A., Rytomaa, M., & Mustonen, P. (1994). Lipid dynamic and peripheral interactions of proteins with membranes surfaces. Chemistry and Physics of Lipids, 73, 181–207.

    PubMed  CAS  Google Scholar 

  245. Maggio, B. (1996). Control by ganglioside GD1a of phospholipase A2 activity through modulation of the lamellar-hexagonal (HII) phase transition. Molecular Membrane Biology, 13, 109–112.

    Article  PubMed  CAS  Google Scholar 

  246. Ruiz-Arguello, M. B., Veiga, M. P., Arrondo, J. L., Goni, F. M., & Alonso, A. (2002). Sphingomyelinase cleavage of sphingomyelin in pure and mixed lipid membranes. Influence of the physical state of the sphingolipid. Chemistry and Physics of Lipids, 114, 11–20.

    PubMed  CAS  Google Scholar 

  247. Volwerk, J. J., Filthuth, E., Griffith, O. H., & Jain, M. K. (1994). Phosphatidylinositol-specific phospholipase C from Bacillus cereus at the lipid–water interface: Interfacial binding, catalysis, and activation. Biochemistry, 33, 3464–3474.

    PubMed  CAS  Google Scholar 

  248. Myers, M., Wortman, C., & Freire, E. (1984). Modulation of neuraminidase activity by the physical state of phospholipid bilayers containing gangliosides Gd1a and Gt1b. Biochemistry, 23, 1442–1448.

    PubMed  CAS  Google Scholar 

  249. Masserini, M., Palestini, P., Venerando, B., Fiorilli, A., Acquotti, D., & Tettamanti, G. (1988). Interactions of proteins with ganglioside-enriched microdomains on the membrane: The lateral phase separation of molecular species of GD1a ganglioside, having homogeneous long-chain base composition, is recognized by Vibrio cholerae sialidase. Biochemistry, 27, 7973–7978.

    PubMed  CAS  Google Scholar 

  250. Perillo, M. A., Yu, R. K., & Maggio, B. (1994). Modulation of the activity of Clostridium perfringens neuraminidase by the molecular organization of gangliosides in monolayers. Biochimica et Biophysica Acta, 1193, 155–164.

    PubMed  CAS  Google Scholar 

  251. Dennis, E. A., Rhee, S. G., Billah, M. M., & Hannun, Y. A. (1991). Role of phospholipase in generating lipid second messengers in signal transduction. FASEB Journal, 5, 2068–2077.

    PubMed  CAS  Google Scholar 

  252. Hannun, Y. A., & Luberto, C. (2000). Ceramide in the eukaryotic stress response. Trends in Cell Biology, 10, 73–80.

    PubMed  CAS  Google Scholar 

  253. Goni, F. M., & Alonso, A. (2002). Sphingomyelinases: Enzymology and membrane activity. FEBS Letters, 531, 38–46.

    PubMed  CAS  Google Scholar 

  254. Clarke, C. J., & Hannun, Y. A. (2006). Neutral sphingomyelinases and nSMase2: Bridging the gaps. Biochimica et Biophysica Acta, 1758, 1893–1901.

    PubMed  CAS  Google Scholar 

  255. Cremesti, A. E., Goni, F. M., & Kolesnick, R. (2002). Role of sphingomyelinase and ceramide in modulating rafts: Do biophysical properties determine biologic outcome? FEBS Letters, 531, 47–53.

    PubMed  CAS  Google Scholar 

  256. Carrer, D. C., Hartel, S., Monaco, H. L., & Maggio, B. (2003). Ceramide modulates the lipid membrane organization at molecular and supramolecular levels. Chemistry and Physics of Lipids, 122, 147–152.

    PubMed  CAS  Google Scholar 

  257. Holopainen, J. M., Medina, O. P., Metso, A. J., & Kinnunen, P. K. (2000). Sphingomyelinase activity associated with human plasma low density lipoprotein. Journal of Biological Chemistry, 275, 16484–16489.

    PubMed  CAS  Google Scholar 

  258. Montes, L. R., Ruiz-Arguello, M. B., Goni, F. M., & Alonso, A. (2002). Membrane restructuring via ceramide results in enhanced solute efflux. Journal of Biological Chemistry, 277, 11788–11794.

    PubMed  CAS  Google Scholar 

  259. Ruiz-Arguello, M. B., Basanez, G., Goni, F. M., & Alonso, A. (1996). Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage. Journal of Biological Chemistry, 271, 26616–26621.

    PubMed  CAS  Google Scholar 

  260. Taniguchi, Y., Ohba, T., Miyata, H., & Ohki, K. (2006). Rapid phase change of lipid microdomains in giant vesicles induced by conversion of sphingomyelin to ceramide. Biochimica et Biophysica Acta, 1758, 145–153.

    PubMed  CAS  Google Scholar 

  261. Morita, S. Y., Nakano, M., Sakurai, A., Deharu, Y., Vertut-Doi, A., & Handa, T. (2005). Formation of ceramide-enriched domains in lipid particles enhances the binding of apolipoprotein E. FEBS Letters, 579, 1759–1764.

    PubMed  CAS  Google Scholar 

  262. Jungner, M., Ohvo, H., & Slotte, J. P. (1997). Interfacial regulation of bacterial sphingomyelinase activity. Biochimica et Biophysica Acta, 1344, 230–240.

    PubMed  CAS  Google Scholar 

  263. Yu, B. Z., Zakim, D., & Jain, M. K. (2002). Processive interfacial catalytic turnover by Bacillus cereus sphingomyelinase on sphingomyelin vesicles. Biochimica et Biophysica Acta, 1583, 122–132.

    PubMed  CAS  Google Scholar 

  264. Hartel, S., Fanani, M. L., & Maggio, B. (2005). Shape transitions and lattice structuring of ceramide-enriched domains generated by sphingomyelinase in lipid monolayers. Biophysical Journal, 88, 287–304.

    PubMed  Google Scholar 

  265. Fanani, M. L., & Maggio, B. (1998). Surface pressure-dependent cross-modulation of sphingomyelinase and phospholipase A2 in monolayers. Lipids, 33, 1079–1087.

    PubMed  CAS  Google Scholar 

  266. De Tullio, L., Maggio, B., Hartel, S., Jara, J., & Fanani, M. L. (2007). The initial surface composition and topography modulate sphingomyelinase-driven sphingomyelin to ceramide conversion in lipid monolayers. Cell Biochemistry and Biophysics, 47, 169–177.

    PubMed  Google Scholar 

  267. Apitz-Castro, R., Jain, M. K., & De Haas, G. H. (1982). Origin of the latency phase during the action of phospholipase A2 on unmodified phosphatidylcholine vesicles. Biochimica et Biophysica Acta, 688, 349–356.

    PubMed  CAS  Google Scholar 

  268. Burack, W. R., & Biltonen, R. L. (1994). Lipid bilayer heterogeneities and modulation of phospholipase A2 activity. Chemistry and Physics of Lipids, 73, 209–222.

    PubMed  CAS  Google Scholar 

  269. Grainger, D. W., Reichert, A., Ringsdorf, H., & Salesse, C. (1989). An enzyme caught in action: Direct imaging of hydrolytic function and domain formation of phospholipase A2 in phosphatidulcholine monolayers. FEBS Letters, 252, 73–82.

    CAS  Google Scholar 

  270. Basanez, G., Nieva, J. L., Goni, F. M., & Alonso, A. (1996). Origin of the lag period in the phospholipase C cleavage of phospholipids in membranes. Concomitant vesicle aggregation and enzyme activation. Biochemistry, 35, 15183–15187.

    PubMed  CAS  Google Scholar 

  271. Barenholz, Y., & Thompson, T. E. (1999). Sphingomyelin: Biophysical aspects. Chemistry and Physics of Lipids, 102, 29–34.

    PubMed  CAS  Google Scholar 

  272. Contreras, F. X., Sot, J., Ruiz-Arguello, M. B., Alonso, A., & Goni, F. M. (2004). Cholesterol modulation of sphingomyelinase activity at physiological temperatures. Chemistry and Physics of Lipids, 130, 127–134.

    PubMed  CAS  Google Scholar 

  273. de Almeida, R. F., Loura, L. M., Fedorov, A., & Prieto, M. (2002). Nonequilibrium phenomena in the phase separation of a two-component lipid bilayer. Biophysical Journal, 82, 823–834.

    PubMed  Google Scholar 

  274. Fanani, M. L., Hartel, S., Jara, J., & Maggio, B. (2006). Sphingomyelinase-induced non-equilibrium phenomena in biointerfaces. Madrid: Procedures of VI Ibero-American Congress of Biophysics.

  275. de Lima Santos, H., Lopes, M. L., Maggio, B., & Ciancaglini, P. (2005). Na,K-ATPase reconstituted in liposomes: Effects of lipid composition on hydrolytic activity and enzyme orientation. Colloids and Surfaces B, Biointerfaces, 41, 239–248.

    PubMed  Google Scholar 

  276. Huang, H. W., Goldberg, E. M., & Zidovetzki, R. (1999). Ceramides modulate protein kinase C activity and perturb the structure of phosphatidylcholine/phosphatidylserine bilayers. Biophysical Journal, 77, 1489–1497.

    PubMed  CAS  Google Scholar 

  277. Sanchez, J. M., Ciklic, I., & Perillo, M. A. (2005). Effect of partitioning equilibria on the activity of beta-galactosidase in heterogeneous media. Biophysical Chemistry, 118, 69–77.

    PubMed  CAS  Google Scholar 

  278. Caseli, L., Oliveira, R. G., Masui, D. C., Furriel, R. P., Leone, F. A., Maggio, B., & Zaniquelli, M. E. (2005). Effect of molecular surface packing on the enzymatic activity modulation of an anchored protein on phospholipid Langmuir monolayers. Langmuir, 21, 4090–4095.

    PubMed  CAS  Google Scholar 

  279. Verger, R., & Pattus, F. (1976). Spreading of membranes at the air/water interface. Chemistry and Physics of Lipids, 16, 285–291.

    PubMed  CAS  Google Scholar 

  280. Schurholz, T., & Schindler, H. (1991). Lipid–protein surface films generated from membrane vesicles: Selfassembly, composition, and film structure. European Biophysics Journal, 20, 71–78.

    PubMed  CAS  Google Scholar 

  281. Calderon, R. O., Maggio, B., Neuberger, T. J., & De Vries, G. H. (1993). Surface behavior of axolemma monolayers: Physico-chemical characterization and use as supported planar membranes for cultured Schwann cells. Journal of Neuroscience Research, 34, 206–218.

    PubMed  CAS  Google Scholar 

  282. Calderon, R. O., Maggio, B., Neuberger, T. J., & DeVries, G. H. (1995). Modulation of Schwann cell Po glycoprotein and galactocerebroside by the surface organization of axolemma. Journal of Neuroscience Research, 40, 349–358.

    PubMed  CAS  Google Scholar 

  283. Kirschner, D. A., Ganser, A. L. & Caspar, D. L. (1984). Diffraction studies of molecular organization and membrane interactions in myelin. In Myelin (pp. 51–95) Anonymous. New York: Plenum Press.

  284. Gonzalez-Sastre, F. (1970). The protein composition of isolated myelin. Journal of Neurochemistry 17, 1049–1056.

    PubMed  CAS  Google Scholar 

  285. Norton, W. T., & Cammer, W. (1984). Isolation and characterization of myelin. In P. Morell (Ed.), Myelin (pp. 147–195). New York: Plenum Press.

  286. Oliveira, R. G., Calderon, R. O., & Maggio, B. (1998). Surface behavior of myelin monolayers. Biochimica et Biophysica Acta, 1370, 127–137.

    PubMed  CAS  Google Scholar 

  287. Trurnit, H. J. (1960). A theory and method for spreading of protein monolayers. Journal of Colloid Science, 15, 1–13.

    CAS  Google Scholar 

  288. Ginsberg, L., & Gershfeld, N. L. (1991). Membrane bilayer instability and the pathogenesis of disorders of myelin. Neuroscience Letters, 130, 133–136.

    PubMed  CAS  Google Scholar 

  289. Oliveira, R. G., & Maggio, B. (2003). Surface behavior, microheterogeneity and adsorption equilibrium of myelin at the air–water interface. Chemistry and Physics of Lipids, 122, 171–176.

    PubMed  CAS  Google Scholar 

  290. von Tscharner, V., & McConnell, H. M. (1981). An alternative view of phospholipid phase behavior at the air–water interface. Microscope and film balance studies. Biophysical Journal, 36, 409–419.

    Google Scholar 

  291. Hénon, S., & Meunier, J. (1991). Microscope at the Brewster angle: Direct observation of first-order phase transitions in mmonolayers. Review of Scientific Instruments, 62, 936–939.

    Google Scholar 

  292. Hönig, D., & Möbius, D. (1991). Direct visualization of monolayers at the air–water interface by Brewster angle microscopy. Journal of Physical Chemistry, 95, 4590–4592.

    Google Scholar 

  293. Hönig, D., & Möbius, D. (1992). Reflectometry at the Brewster angle and Brewster angle microscopy at the air–water interface. Thin solid films, 210/211, 64–68.

    Google Scholar 

  294. Oliveira, R. G., Tanaka, M., & Maggio, B. (2005). Many length scales surface fractality in monomolecular films of whole myelin lipids and proteins. Journal of Structural Biology, 149, 158–169.

    PubMed  CAS  Google Scholar 

  295. Keller, S. L., Pitcher, W. H. III, Huestis, W. H., & McConnell, H. M. (1998). Red blood cell lipids form immiscible liquids. Physical Review Letters, 81, 5019–5022.

    CAS  Google Scholar 

  296. Mouritsen, O. G., & Jorgensen, K. (1994). Dynamical order and disorder in lipid bilayers. Chemistry and Physics of Lipids, 73, 3–25.

    PubMed  CAS  Google Scholar 

  297. Demel, R. A., Paltauf, F., & Hauser, H. (1987). Monolayer characteristics and thermal behavior of natural and synthetic phosphatidylserines. Biochemistry, 26, 8659–8665.

    PubMed  CAS  Google Scholar 

  298. Leveiller, F., Böhm, C., Jacquemain, D., Möhwald, H., Leiserowitz, L., Kjaer, K., & Als-Nielsen, J. (1994). Two-dimensional crystal structure of cadmium arachidate studied by synchrotron X-ray diffraction and reflectivity. Langmuir, 10, 819–829.

    CAS  Google Scholar 

  299. Subramaniam, S., & McConnell, H. M. (1987). Critical mixing in monolayer mixtures of phospholipid and cholesterol. Journal of Physical Chemistry, 91, 1715–1718.

    CAS  Google Scholar 

  300. McConnell, H. M., & Radhakrishnan, A. (2003). Condensed complexes of cholesterol and phospholipids. Biochimica et Biophysica Acta, 1610, 159–173.

    PubMed  CAS  Google Scholar 

  301. Dewey, T.G. (1997). Fractals in molecular biophysics. Oxford: Oxford University Press.

  302. Miller, A., Knoll, W., & Mohwald, H. (1986). Fractal growth of crystalline phospholipid domains in monomolecular layers. Physical Review Letters, 56, 2633–2636.

    PubMed  CAS  Google Scholar 

  303. Rosetti, C. M., & Maggio, B. (2007). Protein-induced surface structuring in myelin membrane monolayers. Biophysical Journal. doi: 10.1529/biophysj.107.112441.

  304. Fidelio, G. D., Maggio, B., & Cumar, F. A. (1984). Interaction of myelin basic protein, melittin and bovine serum albumin with gangliosides, sulphatide and neutral glycosphingolipids in mixed monolayers. Chemistry and Physics of Lipids, 35, 231–245.

    PubMed  CAS  Google Scholar 

  305. Maggio, B. (1997). Molecular interactions of the major myelin glycosphingolipids and myelin basic protein in model membranes. Neurochemical Research, 22, 475–481.

    PubMed  CAS  Google Scholar 

  306. Braun, P. E. (1984). Molecular organization of myelin. In P. Morell (Ed.), Myelin (pp. 97–116). New York: Plenum Press.

  307. Franks, N. P., Melchior, V., Kirshner, D. A., & Caspar, D. L. (1982). Structure of myelin lipid bilayers. Changes during maturation. Journal of Molecular Biology, 155, 133–153.

    PubMed  CAS  Google Scholar 

  308. Gershfeld, N. L. (1989). The critical unilamellar lipid state: A perspective for membrane bilayer assembly. Biochimica et Biophysica Acta, 988, 335–350.

    PubMed  CAS  Google Scholar 

  309. Taylor, C. M., Coetzee, T., & Pfeiffer, S. E. (2002). Detergent-insoluble glycosphingolipid/cholesterol microdomains of the myelin membrane. Journal of Neurochemistry, 81, 993–1004.

    PubMed  CAS  Google Scholar 

  310. Arvanitis, D. N., Yang, W., & Boggs, J. M. (2002). Myelin proteolipid protein, basic protein, the small isoform of myelin-associated glycoprotein, and p42MAPK are associated in the Triton X-100 extract of central nervous system myelin. Journal of Neuroscience Research, 70, 8–23.

    PubMed  CAS  Google Scholar 

  311. Debruin, L. S., & Harauz, G. (2007). White matter rafting—membrane microdomains in myelin. Neurochemical Research, 32, 213–228.

    PubMed  CAS  Google Scholar 

  312. Gielen, E., Baron, W., Vandeven, M., Steels, P., Hoekstra, D., & Ameloot, M. (2006). Rafts in oligodendrocytes: Evidence and structure–function relationship. Glia, 54, 499–512.

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by: SECyT-UNC, CONICET and FONCyT (Argentina); B.M., G.A.B, M.L.F., R.G.O. and N.W. are Career Investigators of CONICET; M.D.B. and C.M.R. are Doctoral Fellows of CONICET; and L.D. is a Doctoral Fellow of FONCYT. R. G. O. thanks The Alexander von Humboldt Foundation for a Research Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bruno Maggio.

Additional information

All the authors contributed equally to this work and are listed in alphabetical order.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maggio, B., Borioli, G.A., Del Boca, M. et al. Composition-driven Surface Domain Structuring Mediated by Sphingolipids and Membrane-active Proteins. Cell Biochem Biophys 50, 79–109 (2008). https://doi.org/10.1007/s12013-007-9004-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-007-9004-1

Keywords