The Siv Tilted Peptide Induces Cylindrical Reverse Micelles In Supported Lipid Bilayers

[en] Elucidation of the molecular mechanism leading to biomembrane fusion is a challenging issue in current biomedical research in view of its involvement in controlling cellular functions and in mediating various important diseases. According to the generally admitted stalk mechanism described for membrane fusion, negatively curved lipids may play a central role during the early steps of the process. In this study, we used atomic force microscopy (AFM) to address the crucial question of whether negatively curved lipids influence the interaction of the simian immunodeficiency virus (SIV) fusion peptide with model membranes. To this end, dioleoylphosphatidylcholine/dipalmitoylphosphatidylcholine (DOPC/DPPC) bilayers containing 0.5 mol % dioleoylphosphatidic acid (DOPA) were incubated with the SIV peptide and imaged in real time using AFM. After a short incubation time, we observed a 1.9 nm reduction in the thickness of the DPPC domains, reflecting either interdigitation or fluidization of lipids. After longer incubation times, these depressed DPPC domains evolved into elevated domains, composed of nanorod structures protruding several nanometers above the bilayer surface and attributed to cylindrical reverse micelles. Such DOPC/DPPC/DOPA bilayer modifications were never observed with nontilted peptides. Accordingly, this is the first time that AFM reveals the formation of cylindrical reverse micelles in lipid bilayers promoted by fusogenic peptides.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

El Kirat, K.

Dufrene, Yf.

Lins, Laurence ; Université de Liège - ULiège > Gembloux Agro-Bio Tech

Brasseur, Robert ; Université de Liège - ULiège > Gembloux Agro-Bio Tech

Language :

English

Title :

The Siv Tilted Peptide Induces Cylindrical Reverse Micelles In Supported Lipid Bilayers

Publication date :

2006

Journal title :

Biochemistry

ISSN :

0006-2960

eISSN :

1520-4995

Publisher :

American Chemical Society, Washington, United States - District of Columbia

Volume :

Issue :

Pages :

9336-9341
9336-41

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 23 June 2010

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Bibliography

Peuvot, J., Schanck, A., Lins, L., and Brasseur, R. (1999) Are the fusion processes involved in birth, life and death of the cell depending on tilted insertion of peptides into membranes? J. Theor. Biol. 198, 173-181.
Jena, B. P. (2004) Discovery of the Porosome: Revealing the molecular mechanism of secretion and membrane fusion in cells, J. Cell. Mol. Med. 8, 1-21.
Malinin, V. S., and Lentz, B. R. (2004) Energetics of vesicle fusion intermediates: Comparison of calculations with observed effects of osmotic and curvature stresses, Biophys. J. 86, 2951-2964.
Chernomordik, L. (1996) Non-bilayer lipids and biological fusion intermediates, Chem. Phys. Lipids 81, 203-213.
Epand, R. M., and Epand, R. F. (2000) Modulation of membrane curvature by peptides, Biopolymers 55, 358-363.
Haque, M. E., and Lentz, B. R. (2004) Roles of curvature and hydrophobic interstice energy in fusion: Studies of lipid perturbant effects, Biochemistry 43, 3507-3517.
Stieglitz, K. A., Seaton, B. A., and Roberts, M. F. (2001) Binding of proteolytically processed phospholipase D from Streptomyces chromofuscus to phosphatidylcholine membranes facilitates vesicle aggregation and fusion, Biochemistry 40, 13954-13963.
Blackwood, R. A., Smolen, J. E., Transue, A., Hessler, R. J., Harsh, D. M., Brower, R. C., and French, S. (1997) Phospholipase D activity facilitates Ca2+-induced aggregation and fusion of complex liposomes, Am. J. Physiol. 272, C1279-C1285.
Hughson, F. M. (1997) Enveloped viruses: A common mode of membrane fusion? Curr. Biol. 7, R565-R569.
Brasseur, R. (2000) Tilted peptides: A motif for membrane destabilization (hypothesis), Mol. Membr. Biol. 17, 31-40.
El Kirat, K., Lins, L., Brasseur, R., and Dufrene, Y. F. (2005) Nanoscale Modification of Supported Lipid Membranes: Synergetic Effect of Phospholipase D and Viral Fusion Peptides, J. Biomed. Nanotechnol. 1, 39-46.
Engel, A., and Muller, D. J. (2000) Observing single biomolecules at work with the atomic force microscope, Nat. Struct. Biol. 7, 715-718.
Giocondi, M. C., Vie, V., Lesniewska, E., Milhiet, P. E., Zinke-Allmang, M., and Le Grimellec, C. (2001) Phase Topology and Growth of Single Domains in Lipid Bilayers, Langmuir 17, 1653-1659.
Reviakine, I., Bergsma-Schutter, W., Morozov, A. N., and Brisson, A. (2001) Two-Dimensional Crystallization of Annexin A5 on Phospholipid Bilayers and Monolayers: A Solid-Solid-Phase Transition between Crystal Forms, Langmuir 17, 1680-1686.
Mou, J., Yang, J., Huang, C., and Shao, Z. (1994) Alcohol induces interdigitated domains in unilamellar phosphatidylcholine bilayers, Biochemistry 33, 9981-9985.
Rinia, H. A., Boots, J. W., Rijkers, D. T., Kik, R. A., Snel, M. M., Demel, R. A., Killian, J. A., van der Eerden, J. P., and de Kruijff, B. (2002) Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: Specific effects of flanking residues, Biochemistry 41, 2814-2824.
Milhiet, P. E., Giocondi, M. C., Baghdadi, O., Ronzon, F., Roux, B., and Le Grimellec, C. (2002) Spontaneous insertion and partitioning of alkaline phosphatase into model lipid rafts, EMBO Rep. 3, 485-490.
Berquand, A., Mingeot-Leclercq, M. P., and Dufrene, Y. F. (2004) Real-time imaging of drug-membrane interactions by atomic force microscopy, Biochim. Biophys. Acta 1664, 198-205.
Epand, R. F., Yip, C. M., Chernomordik, L. V., LeDuc, D. L., Shin, Y. K., and Epand, R. M. (2001) Self-assembly of influenza hemagglutinin: Studies of ectodomain aggregation by in situ atomic force microscopy, Biochim. Biophys. Acta 1513, 167-175.
Green, J. D., Kreplak, L., Goldsbury, C., Li, B. X., Stolz, M., Cooper, G. S., Seelig, A., Kistler, J., and Aebi, U. (2004) Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide, J. Mol. Biol. 342, 877-887.
Martin, I., Dubois, M. C., Defrise-Quertain, P., Saermark, T., Burny, A., Brasseur, R., and Ruysschaert, J. M. (1994) Correlation between fusogenicity of synthetic modified peptides corresponding to the NH2-terminal extremity of simian immunodeficiency virus gp32 and their mode of insertion into the lipid bilayer: An infrared spectroscopy study, J. Virol. 68, 1139-1148.
Voneche, V., Portetelle, D., Kettmann, R., Willems, L., Limbach, K., Paoletti, E., Ruysschaert, J. M., Burny, A., and Brasseur, R. (1992) Fusogenic segments of bovine leukemia virus and simian immunodeficiency virus are interchangeable and mediate fusion by means of oblique insertion in the lipid bilayer of their target cells, Proc. Natl. Acad. Sci. U.S.A. 89, 3810-3814.
Epand, R. F., Martin, I., Ruysschaert, J. M., and Epand, R. M. (1994) Membrane orientation of the SIV fusion peptide determines its effect on bilayer stability and ability to promote membrane fusion, Biochem. Biophys. Res. Commun. 205, 1938-1943.
Bradshaw, J. P., Darkes, M. J., Harroun, T. A., Katsaras, J., and Epand, R. M. (2000) Oblique membrane insertion of viral fusion peptide probed by neutron diffraction, Biochemistry 39, 6581-6585.
Lins, L., Charloteaux, B., Thomas, A., and Brasseur, R. (2001) Computational study of lipid-destabilizing protein fragments: Towards a comprehensive view of tilted peptides, Proteins 44, 435-447.
Reviakine, I., and Brisson, A. (2000) Formation of Supported Phospholipid Bilayers from Unilamellar Vesicles Investigated by Atomic Force Microscopy, Langmuir 16, 1806-1815.
Dufrene, Y. F., Barger, W. R., Green, J. B. D., and Lee, G. U. (1997) Nanometer-Scale Surface Properties of Mixed Phospholipid Monolayers and Bilayers, Langmuir 13, 4779-4784.
El Kirat, K., Lins, L., Brasseur, R., and Dufrene, Y. F. (2005) Fusogenic tilted peptides induce nanoscale holes in supported phosphatidylcholine bilayers, Langmuir 21, 3116-3121.
Rinia, H. A., Kik, R. A., Demel, R. A., Snel, M. M., Killian, J. A., Der Eerden, J. P., and de Kruijff, B. (2000) Visualization of highly ordered striated domains induced by transmembrane peptides in supported phosphatidylcholine bilayers, Biochemistry 39, 5852-5858.
Mou, J., Czajkowsky, D. M., and Shao, Z. (1996) Gramicidin A aggregation in supported gel state phosphatidylcholine bilayers, Biochemistry 35, 3222-3226.
Plenat, T., Boichot, S., Dosset, P., Milhiet, P. E., and Le Grimellec, C. (2005) Coexistence of a two-states organization for a cell-penetrating peptide in lipid bilayer, Biophys. J. 89, 4300-4309.
Nelson, M., Cain, N., Taylor, C. E., Ocko, B. M., Gin, D. L., Hammond, S. R., and Schwartz, D. K. (2005) Periodic Arrays of Interfacial Cylindrical Reverse Micelles, Langmuir 21, 9799-9802.
Kowalewski, T., and Holtzman, D. M. (1999) In situ atomic force microscopy study of Alzheimer's β-amyloid peptide on different substrates: New insights into mechanism of β-sheet formation, Proc. Natl. Acad. Sci. U.S.A. 96, 3688-3693.
Michaelson, D. M., Horwitz, A. F., and Klein, M. P. (1974) Head group modulation of membrane fluidity in sonicated phospholipid dispersions, Biochemistry 13, 2605-2612.