Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1986 Nov;50(5):779–788. doi: 10.1016/S0006-3495(86)83518-4

Morphological responses to calcium-induced interaction of phosphatidylserine-containing vesicles.

B Kachar, N Fuller, R P Rand
PMCID: PMC1329802  PMID: 3790685

Abstract

Structural changes in phospholipid vesicles made of dioleylphosphatidylethanolamine (DOPE)/bovine phosphatidylserine (PS) (1/1, 3/1, 10/1) or of egg phosphatidylcholine (PC)/PS (3/1) and exposed to calcium chloride for various times have been observed by means of video-enhanced light microscopy and freeze-fracture electron microscopy. Calcium induces the formation of large, smooth double-bilayer diaphragms as the spherical vesicles adhere to and deform each other. No subsequent changes are seen with PC/PS vesicles. DOPE/PS vesicles respond to the resultant stress, with about equal probability, by either fusing, through diaphragm rupture, or deflating, by way of volume loss through intact bilayers, even when they contain up to 400 mM sucrose. The diaphragm areas only rarely show the structural destabilization necessary for fusion. The final state is lipid segregated into DOPE hexagonal and Ca-PS lamellar bulk phases with the exclusion of most of the vesicle contents. Results with these and pure PS vesicles studied earlier indicate that the early response of vesicles to calcium chloride is determined by the competing rates at which mechanical stress (bilayer tension and intravesicular pressure) builds up as the vesicles adhere and flatten against each other, and is relieved by vesicle fusion or by volume loss. We attribute the qualitatively different responses of these three lipid systems to their measured differences in adhesion energies and consequent rate of build-up of mechanical stress. Yield to that stress for any one of these lipid systems is not a unique sequence of morphological changes, and so it remains obscure how such a stochastic process could be used in the controlled process of cellular fusion.

Full text

PDF
779

Images in this article

783FIGURE 3
on p.783
781FIGURE 1
on p.781
782FIGURE 2
on p.782
784FIGURE 4
on p.784
785FIGURE 5
on p.785

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akabas M. H., Cohen F. S., Finkelstein A. Separation of the osmotically driven fusion event from vesicle-planar membrane attachment in a model system for exocytosis. J Cell Biol. 1984 Mar;98(3):1063–1071. doi: 10.1083/jcb.98.3.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen R. D., Allen N. S. Video-enhanced microscopy with a computer frame memory. J Microsc. 1983 Jan;129(Pt 1):3–17. doi: 10.1111/j.1365-2818.1983.tb04157.x. [DOI] [PubMed] [Google Scholar]
  3. Bearer E. L., Düzgünes N., Friend D. S., Papahadjopoulos D. Fusion of phospholipid vesicles arrested by quick-freezing. The question of lipidic particles as intermediates in membrane fusion. Biochim Biophys Acta. 1982 Dec 8;693(1):93–98. doi: 10.1016/0005-2736(82)90474-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cohen F. S., Akabas M. H., Zimmerberg J., Finkelstein A. Parameters affecting the fusion of unilamellar phospholipid vesicles with planar bilayer membranes. J Cell Biol. 1984 Mar;98(3):1054–1062. doi: 10.1083/jcb.98.3.1054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Das S., Rand R. P. Diacylglycerol causes major structural transitions in phospholipid bilayer membranes. Biochem Biophys Res Commun. 1984 Oct 30;124(2):491–496. doi: 10.1016/0006-291x(84)91580-8. [DOI] [PubMed] [Google Scholar]
  6. Düzgüneş N., Wilschut J., Fraley R., Papahadjopoulos D. Studies on the mechanism of membrane fusion. Role of head-group composition in calcium- and magnesium-induced fusion of mixed phospholipid vesicles. Biochim Biophys Acta. 1981 Mar 20;642(1):182–195. doi: 10.1016/0005-2736(81)90148-6. [DOI] [PubMed] [Google Scholar]
  7. Evans E. A., Parsegian V. A. Energetics of membrane deformation and adhesion in cell and vesicle aggregation. Ann N Y Acad Sci. 1983;416:13–33. doi: 10.1111/j.1749-6632.1983.tb35176.x. [DOI] [PubMed] [Google Scholar]
  8. Evans E., Kwok R. Mechanical calorimetry of large dimyristoylphosphatidylcholine vesicles in the phase transition region. Biochemistry. 1982 Sep 28;21(20):4874–4879. doi: 10.1021/bi00263a007. [DOI] [PubMed] [Google Scholar]
  9. Lis L. J., McAlister M., Fuller N., Rand R. P., Parsegian V. A. Interactions between neutral phospholipid bilayer membranes. Biophys J. 1982 Mar;37(3):657–665. [PMC free article] [PubMed] [Google Scholar]
  10. Parsegian V. A., Rand R. P. Membrane interaction and deformation. Ann N Y Acad Sci. 1983;416:1–12. doi: 10.1111/j.1749-6632.1983.tb35175.x. [DOI] [PubMed] [Google Scholar]
  11. Rand R. P. Interacting phospholipid bilayers: measured forces and induced structural changes. Annu Rev Biophys Bioeng. 1981;10:277–314. doi: 10.1146/annurev.bb.10.060181.001425. [DOI] [PubMed] [Google Scholar]
  12. Rand R. P., Kachar B., Reese T. S. Dynamic morphology of calcium-induced interactions between phosphatidylserine vesicles. Biophys J. 1985 Apr;47(4):483–489. doi: 10.1016/S0006-3495(85)83941-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Rand R. P., Parsegian V. A. Mimicry and mechanism in phospholipid models of membrane fusion. Annu Rev Physiol. 1986;48:201–212. doi: 10.1146/annurev.ph.48.030186.001221. [DOI] [PubMed] [Google Scholar]
  14. Rand R. P., Parsegian V. A. Physical force considerations in model and biological membranes. Can J Biochem Cell Biol. 1984 Aug;62(8):752–759. doi: 10.1139/o84-097. [DOI] [PubMed] [Google Scholar]
  15. Siegel D. P. Inverted micellar structures in bilayer membranes. Formation rates and half-lives. Biophys J. 1984 Feb;45(2):399–420. doi: 10.1016/S0006-3495(84)84164-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Szoka F., Jr, Papahadjopoulos D. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4194–4198. doi: 10.1073/pnas.75.9.4194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Verkleij A. J., Momvers C., Leunissen-Bijvelt J., Ververgaert P. H. Lipidic intramembranous particles. Nature. 1979 May 10;279(5709):162–163. doi: 10.1038/279162a0. [DOI] [PubMed] [Google Scholar]
  18. Wilschut J., Düzgüneş N., Fraley R., Papahadjopoulos D. Studies on the mechanism of membrane fusion: kinetics of calcium ion induced fusion of phosphatidylserine vesicles followed by a new assay for mixing of aqueous vesicle contents. Biochemistry. 1980 Dec 23;19(26):6011–6021. doi: 10.1021/bi00567a011. [DOI] [PubMed] [Google Scholar]
  19. Zimmerberg J., Cohen F. S., Finkelstein A. Fusion of phospholipid vesicles with planar phospholipid bilayer membranes. I. Discharge of vesicular contents across the planar membrane. J Gen Physiol. 1980 Mar;75(3):241–250. doi: 10.1085/jgp.75.3.241. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES