Skip to main content

Advertisement

Log in

Onsager’s irreversible thermodynamics of the dynamics of transient pores in spherical lipid vesicles

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

Onsager’s irreversible thermodynamics is used to perform a systematic deduction of the kinetic equations governing the opening and collapse of transient pores in spherical vesicles. We show that the edge tension has to be determined from the initial stage of the pore relaxation and that in the final state the vesicle membrane is not completely relaxed, since the surface tension and the pressure difference are about 25 % of its initial value. We also show that the pore life-time is controlled by the solution viscosity and its opening is driven by the solution leak-out and the surface tension drop. The final collapse is due to a non-linear interplay between the edge and the surface tensions together with the pressure difference. We also discuss the connection with previous models.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Brochard-Wyart F, de Gennes PG, Sandre O (2000) Transient pores in stretched vesicles: role of leak-out. Physica A 278:32–51

    Article  CAS  Google Scholar 

  • Cooper RA, Shattil SJ (1971) Mechanisms of hemolysis-the minimal red-cell defect. N Engl J Med 285(27):1514–1520

    Article  CAS  PubMed  Google Scholar 

  • Debrégeas G, Martin P, Brochard-Wyart F (1995) Viscous bursting of suspended films. Phys Rev Lett 75:3886–3889

    Article  PubMed  Google Scholar 

  • Diederich A, Bähr G, Winterhalter M (1998) Influence of polylysine on the rupture of negatively charged membranes. Langmuir 14:4597–4605

    Article  CAS  Google Scholar 

  • Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902

    Article  CAS  PubMed  Google Scholar 

  • Helfrich W (1973) Elastic properties of lipid bilayers-theory and possible experiments. Z Naturforsch C C28:693–703

    Google Scholar 

  • Hernández-Zapata E, Matínez-Balbuena L, Santamaría-Holek I (2009) Thermodynamics and dynamics of the formation of spherical lipid vesicles. J Biol Phys 35:297–308

    Article  PubMed Central  PubMed  Google Scholar 

  • Isambert H (1998) Understanding the electroporation of cells and artificial bilayer membranes. Phys Rev Lett 80:3404–3407

    Article  CAS  Google Scholar 

  • Karatekin E, Sandre O, Guitouni H, Borghi N, Puech P-H, Brochard-Wyart Françoise (2003) Cascades of transient pores in giant vesicles: line tension and transport. Biophys J 84:1734–1749

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kondepudi D, Prigogine I (2007) Modern thermodynamics. Wiley, England

    Google Scholar 

  • Koslov MM, Markin VS (1984) A theory of osmotic lysis of lipid vesicles. J Theor Biol 109:17–39

    Article  CAS  PubMed  Google Scholar 

  • Le TD, Olsson U, Mortensen K (2000) Topological transformation of a surfactant bilayer. Physica B 276–278:379–380

    Article  Google Scholar 

  • Levin Y, Idiart MA (2004) Pore dynamics of osmotically stressed vesicles. Physica A 331:571–578

    Article  CAS  Google Scholar 

  • Lipowsky R (1995) Generic interactions of flexible membranes. In: Lipowski BR, Sackmann E (eds) Structure and dynamics of membranes: generic and specific interactions. Handbook of biological physics, V. 1. Elsevier Science, B.V. Amsterdam, The Netherlands. pp 521–602

  • Liu T, Singh P, Jenkins JT, Jagota A, Bykhovskaia M, Hui C-Y (2015) A continuum model of docking of synaptic vesicle to plasma membrane. J R Soc Interf 12:20141119

    Article  Google Scholar 

  • Majd S, Yusko EC, Billeh YN, Macrae MX, Yang J, Mayer M (2010) Applications of biological pores in nanomedicine, sensing, and nanoelectronics. Curr Opin Biotechnol 21:439–476

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matsuzaki K (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim Biophys Acta 1462:1–10

    Article  CAS  PubMed  Google Scholar 

  • McNeil PL, Steinhardt RA (2003) Plasma membrane disruption: repair, prevention, adaptation. Annu Rev Cell Dev Biol 19:697–731

    Article  CAS  PubMed  Google Scholar 

  • Monck JR, Fernandez JM (1994) The exocytotic fusion pore and neurotransmitter release. Neuron 12:707–716

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759–803

    CAS  PubMed  Google Scholar 

  • Onsager L (1931) Reciprocal relations in irreversible processes I. Phys Rev 37:405–426

    Article  CAS  Google Scholar 

  • Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189:347–358

    Article  CAS  PubMed  Google Scholar 

  • Papo N, Shai Y (2003) Exploring peptide membrane interaction using surface plasmon resonance: differentiation between pore formation versus membrane disruption by lytic peptides. Biochemistry 42:458–466

    Article  CAS  PubMed  Google Scholar 

  • Pavlin M, Kotnik T, Miklavcic D, Kramar P, Lebar AM (2008) Electroporation of planar lipid bilayers and membranes. Adv Planar Lipid Bilayers Liposomes 6:165–226

    Article  CAS  Google Scholar 

  • Picco A, Mund M, Ries J, Nédélec F, Kaksonen M (2015) Visualizing the functional architecture of the endocytotic machinery. eLife. doi:10.7554/eLife. 04535

  • Portet T, Dimova R (2010) A new method for measuring edge tensions and stability of lipid bilayers: effect of membrane composition. Biophys J 99:3264–3273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prigogine I (1968) Introduction to thermodynamics of irreversible processes. Wiley, New York

    Google Scholar 

  • Rawicz W, Olbrich KC, McIntosh T, Needham D, Evans E (2000) Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys J 79:328–339

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riske KA, Dimova R (2005) Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys J 88:1143–1155

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez N, Cribier S, Pincet F (2006) Transformation from long- to short-lived transient pores in giant vesicles in an aqueous medium. Phys Rev E 74:061902–061912

    Article  Google Scholar 

  • Ryham R, Berezovik I, Cohen FS (2011) Aqueous viscosity is the primary source of friction in lipidic pore dynamics. Biophys J 101:2929–2938

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ryham R, Cohen FS, Eisenberg R (2012) A dynamic model of open vesicles in fluids. Commun Math Sci 10(4):1273–1285

    Article  Google Scholar 

  • Sakuma Y, Imai M (2015) From vesicles to protocells: the roles of amphiphilic molecules. Life 5:651–675. doi:10.3390/life5010651

    Article  PubMed Central  PubMed  Google Scholar 

  • Sandre O, Moreaux L, Brochard-Wyart F (1999) Dynamics of transient pores in stretched vesicles. Proc Natl Acad Sci USA 96:10591–10596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Siegel DP, Kozlov MM (2004) The Gaussian curvature elastic modulus of N-monomethylated dioleoylphosphatidylethanolamine: relevance to membrane fusion and lipid phase behavior. Biophys J 87:366–374

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vardjan N, Jorgacevski J, Zorec R (2013) Fusion pores, SNAREs, and exocytosis. Neuroscientist 19:160–174

    Article  CAS  PubMed  Google Scholar 

  • Weaver JC (2000) Electroporation of cells and tissues. IEEE Trans Plasma Sci 28:24–33

    Article  CAS  Google Scholar 

  • Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank A. Ledesma-Durán and A. Arteaga-Jiménez for their useful discussions. This work was supported by UNAM DGAPA Grant No. IN113415 and CONACYT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Martínez-Balbuena.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martínez-Balbuena, L., Hernández-Zapata, E. & Santamaría-Holek, I. Onsager’s irreversible thermodynamics of the dynamics of transient pores in spherical lipid vesicles. Eur Biophys J 44, 473–481 (2015). https://doi.org/10.1007/s00249-015-1051-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-015-1051-8

Keywords

Navigation