Abstract
Glycosphingolipids, in particular gangliosides, play a crucial role in neuronal development and are known to change dramatically in total content and distribution in different brain areas during embryogenesis. In the present work we analyzed the activity of enzymes involved in the metabolism of gangliosides, at different periods of functional maturation in different regions of chick embryo brain. Our data demonstrate differences in the enzymatic activities in the examined areas; these differences might be correlated with the functional lateralization occurring in the brain during development. Significative differences were found in glycosphingolipid composition between controlateral cerebral hemispheres and optic lobes; these results together with previous data we found, contribute to reinforce our hypothesis on the occurrence of biochemical lateralization during early brain development.
Similar content being viewed by others
REFERENCES
IUPAC-IUB Joint Commissionon Biochemical Nomenclature (JCBN). 1998. Nomenclature of glycolipids. Recommendations 1997. Eur. J. Biochem. 257:293-298.
Hakomori, S. 1990. Bifunctional role of glycosphingolipids. J. Biol. Chem. 265:18713-18716.
Zeller, C. B. and Marchase, R. B. 1992. Gangliosides as modulators of cell function. Am. J. Physiol. 262:C1341-C1355.
Huwiler, A., Kolter, T., Pfeilschifter, J., and Sandhoff, K. 2000. Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta 1485:63-99.
Popko, B. 2000. Myelin galactolipids: mediators of axon-glial interactions? Glia 29:149-153.
Merril, A. H., Schmelz, E.-M., Dillehay, D. L., Spiegel, S., Shayman, J. A., Schroeder, J. J., Riley, R. T., Voss, K. A., and Wang, E. 1997. Spingolipids: the enigmatic lipid class: biochemistry, physiology and pathophysiology. Toxicol. Appl. Pharmacol. 142:208-225.
Merrill, A. H. 1991. Cell regulation by sphingosine and more complex sphingolipids. J. Bioenerg. Biomembr. 23:83-104.
Dyer, C. A. and Benjamins, J. A. 1990. GSL and transmembrane signaling: antibodies to galactocerebroside cause an influx of calcium in oligodendrocytes. J. Cell Biol. 111:625-633.
Nagai, Y. 1994. Functional roles of gangliosides in bio-signaling. Behav. Brain Res. 66:99-104.
Nagai, Y. and Iwamori, M. 1995. Cellular biology of gangliosides. Pages 197-241, in Rosenberg A. (ed.), Biology of the Sialic Acid, Plenum Press, New York.
Kopitz, J., von Reitzenstein, C., Burchert, M., Cants, M., and Gabius, H. J. 1998. Galectin-1 is a major receptor for ganglioside GM1, aproduct of the growth-controlling acitvity of a cell surface ganglioside sialidase, on human neuroblastoma cells In culture. J. Biol. Chem. 273:589-596.
Rahmann, H., Rosner, H., Kortje K.-H., Beitinger, H., and Seybold, V. 1994. Ca2+-ganglioside interaction in neuronal differentiation and developmen. Pages 127-145, in Svennerholm, L., Asbury, A. K., Reisfeld, R. A., Sandhoff, K., Suzuki, K., Tettamanti, G., and Toffano, G. (eds.), Progress in Brain Research Vol. 101, Elsevier Science BV.
Higashi, H., Omori, A., and Yamagata, T. 1992. Calmodulin, a ganglioside-binding protein. J. Biol. Chem. 267:9831-9838.
Kasahara, K., Watanabe, Y., Yamamoto, T., and Sanai, Y. 1997 Association of Src family tyrosine kinase Lyn with ganglioside GD3 In rat brain. J. Biol. Che. 272:29947-29953.
Masserini, M., Palestini, P., and Pitto, M. 1999. Glyclipid-enriched caveolae and caveolae-like domains in the nervous syste. J. Neurochem. 73:1-11.
Teixeira, A., Chaverot, N., Schroder, C., Strosberg, A. D., Couraud, P.-O., and Cazaubon, S. 1999. Requirement of caveolale microdomains In extracellular signal-regulated kinase and focal adhesion kinase activation Induced by endothelin-1 in primary astrocytes. J. Neurochem. 72:120-128.
Hakomori, S., Handa, K., Iwabuchi, K., Yamamura, S., and Prinetti, A. 1998. New insights in glycosphingolipid function: “glycosignaling domain,” a cell surface assembly of glycosphingolipids with signal transducer molecules, involved in cell adhesion coupled with signaling. Glycobiology 8:xi-xix.
Rampersaud, A. A., Oblinger, J. L., Ponnappan, R. K., Burry, R. W., and Yates, A. J. 1999. Gangliosides and growth factor receptor regulation. Biochem. Soc. Trans. 27:415-422.
Furukawa, K., Takamiya, K., Okada, M., Inoue, M., Fukumoto, S., and Furukawa, K. 2001. Novel functions of complex carbohydrates elucidated by the mutant mice of glycosyltransferase genes. Biochim. Biophys. Acta 1525:1-12.
Iwamoto, T., Fukumoto, S., Kanaoka, K., Sakai, E., Shibata, M., Fukumoto, E., Inokuchi, J., Takamiya, K., Furukawa, K., Furukawa, K., Kato, Y., and Mizuno, A. 2001. Lactosylceramide is essential for the osteoclastogenesis mediated by macrophagecolony-stimulating factor and receptor activator of nuclear factor-kappa B ligand. J. Biol. Chem. 276:406031-40638.
Takamiya, K., Yamamoto, A., Furukawa, K., Yamashiro, S., Shin, M., Okada, M., Fukumoto, S., Haraguchi, M., Takeda, N., Fujimura, K., Sakae, M., Kishikawa, M., Shiku, H., Furukawa, K., and Aizawa, S. 1996. Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system Proc. Natl. Acad. Sci. U.S.A. 93820:10662-10667.
Furukawa, K., Fukumoto, S., Mutoh, T., Ito, M., Ohishi, H., Furukawa, K., Mitsuda, T., Okajima, T., Honda, T., and Sugiura, Y. 1999. Roles of glycosphingolipids in the nervous system: studies by remodeling of carbohydrate moiety in cultured cells and in experimental animals. Glycoconj. J. 16:S57.
Sheikh, K. A., Sun, J., Liu, Y., Kawai, H., Crawford, T. O., Proia, R. L., Griffin, J. W., and Schnaar, R. L. 1999. Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc. Natl. Acad. Sci. U.S.A. 96(13): 7532-7537.
Hakomori, S., Yamamura, S., and Handa, A. K. 1998. Signal transduction through glyco(sphingo)lipids. Introduction and recent studies on glyco(sphingo)lipid-enriched microdomains. Ann. N. Y. Acad. Sci. 845:1-10.
Masserini, M. and Ravasi, D. 2001. Role of sphingolipids In the biogenesis of membrane domains. Biochim. Biophys. Acta 1532(3):149-161.
Dreyfus, H., Urban, P. F., Edel-Hart, S., and Mandel, P. 1975. Developmental patterns of gangliosides and phospholipids in chick retina and brain. J. Neurochem. 25:245-250.
Rosner, H. 1975. Changes in the contents of gangliosides and ganglioside pattern of chicken brain. J. Neurochem. 24:815-816.
Rosner, H. 1982. Ganglioside changes in the chick optic lobes as biochemical indicators of brain development and maturation. Brain Res. 236:49-61.
Seybold, V. and Rahmann, H. 1985. Brain gangliosides in birds with different types of postnatal development. Dev. Br. Res. 17:201-208.
Sonnino, S., Bassi, R., Chigorno, V., and Tettamanti G. 1990. Further studies on changes of chicken brain gangliosides during prenatal and postnatal life. J. Neurochem. 54:1653-1660.
Van Echten, G. and Sandhoff, K. 1993. Ganglioside metabolism. J. Biol. Chem. 268:5341-5344.
Kolter, T., Doering, T., Wilkening, G., Werth, N., and Sandhoff, K. 1999. Recent advances in the biochemistry of glycosphingolipid metabolism. Biochem. Soc. Trans. 27:409-415.
Basu, S. and Basu, M. 1982. Expression of glycosphingolipid glycosyltransferases in development and transformation, Pages 265-284, in Horowits, M. I. (ed.), The Glycoconjugates vol. III. Academic Press. New York.
Rizzo, A. M., Galli, C. F., Montorfano, G., and Berra, B. 1995. Phospholipid distribution and fatty acid composition in different brain regions during chick embryo development. J. Neurochem. 64:1728-1735.
Basu, S., Basu, M., and Basu, S. S. 1995. Biological specificity of sialyltransferases, Pages 69-94, in Rosenberg, A. (ed.), Biology of Sialic Acid. Plenum Press, New York.
Basu M., Basu S., Stoffyn, A., and Stoffyn, P. 1982. Biosynthesis in vitro of sialyl(a2-3))neolactosylceramide by a sialytransferase from embryonic chicken brain. J. Biol. Chem. 257: 12765-12769.
Peterson, G. M. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83:346-356.
Basu, M., Das, K. K., Kyle, J. W., Chon, H. C., Schaeper, R., and Basu, S. 1987. Complex carbohydrates, Pages 575-607, in (Ginsburg, V., (ed.), Methods in Enzymology, vol. 38, Academic Press., New York.
Tettamanti, G., Bonali, F., Marchesini, S., and Zambotti, V. 1973. A new procedure for the extraction and purification of brain gangliosides. Biochim. Biophys. Acta 296:160-170.
Vance, D. E. and Sweeley, C. C. 1967. Quantitative determination of the neutral glycosilceramides in human blood. J. Lipid Res. 8:621-630.
Svennerholm, L. and Fredman, P. 1980. A procedure for the quantitative isolation of brain gangliosides. Biochim. Biophys. Acta 617:97-109.
Smith, I. 1960. Chromatographic and Electrophoretic Technique. Vol 1, p 260, Intersciences, New York.
Panzetta, P., Maccione, H. J. F., and Caputto R. 1980. Synthesis of retinal gangliosides during chick embryonic development. J. Neurochem. 35:100-108.
Rahmann, H. 1995. Brain gangliosides and memory formation. Behav.Brain Res. 66:105-116.
Rogers, L. J. 1991. Development of lateralization, Pages 507-535, in Andrew, R. J. (ed.), Neural and Behavioural Plasticity, Oxford University Press.
Rogers, L. J., Robinson, T., and Ehrlich, D. 1986. Role of supraoptic decussation in development of asymmetry of brain function in the chicken. Dev. Brain Res. 28:33-39.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rizzo, A.M., Rossi, F. & Berra, B. Glycosyltransferases in Different Brain Regions During Chick Embryo Development. Neurochem Res 27, 815–821 (2002). https://doi.org/10.1023/A:1020213209078
Issue Date:
DOI: https://doi.org/10.1023/A:1020213209078