Mechanics of membrane fusion
Tóm tắt
Từ khóa
Tài liệu tham khảo
Duelli, D. & Lazebnik, Y. Cell-to-cell fusion as a link between viruses and cancer. Nat. Rev. Cancer 7, 968–976 (2007).
Sapir, A., Avinoam, O., Podbilewicz, B. & Chernomordik, L.V. Viral and developmental cell fusion mechanisms: conservation and divergence. Dev. Cell 14, 11–21 (2008).
Kielian, M. & Rey, F.A. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4, 67–76 (2006).
Earp, L.J., Delos, S.E., Park, H.E. & White, J.M. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285, 25–66 (2005).
Jahn, R. & Scheller, R.H. SNAREs–engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631–643 (2006).
Hoppins, S., Lackner, L. & Nunnari, J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751–780 (2007).
McNeil, P.L. & Steinhardt, R.A. Plasma membrane disruption: repair, prevention, adaptation. Annu. Rev. Cell Dev. Biol. 19, 697–731 (2003).
Martens, S. & McMahon, H.T. Disparate and common players in cellular membrane fusion events. Nat. Rev. Mol. Cell Biol. advance online publication, doi:10.1038/nrm2417 (21 May 2008).
Chernomordik, L.V. & Kozlov, M.M. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175–207 (2003).
Lentz, B.R., Malinin, V., Haque, M.E. & Evans, K. Protein machines and lipid assemblies: current views of cell membrane fusion. Curr. Opin. Struct. Biol. 10, 607–615 (2000).
Jackson, M.B. & Chapman, E.R. The fusion pores of Ca2+-triggered exocytosis. Nat. Struct. Mol. Biol. 15, 684–689 (2008).
Chernomordik, L.V., Melikyan, G.B. & Chizmadzhev, Y.A. Biomembrane fusion: a new concept derived from model studies using two interacting planar lipid bilayers. Biochim. Biophys. Acta 906, 309–352 (1987).
Chanturiya, A., Chernomordik, L.V. & Zimmerberg, J. Flickering fusion pores comparable with initial exocytotic pores occur in protein-free phospholipid bilayers. Proc. Natl. Acad. Sci. USA 94, 14423–14428 (1997).
Yang, L. & Huang, H.W. A rhombohedral phase of lipid containing a membrane fusion intermediate structure. Biophys. J. 84, 1808–1817 (2003).
Malinin, V.S., Frederik, P. & Lentz, B.R. Osmotic and curvature stress affect PEG-induced fusion of lipid vesicles but not mixing of their lipids. Biophys. J. 82, 2090–2100 (2002).
Cohen, F.S., Zimmerberg, J. & Finkelstein, A. Fusion of phospholipid vesicles with planar phospholipid bilayer membranes. II. Incorporation of a vesicular membrane marker into the planar membrane. J. Gen. Physiol. 75, 251–270 (1980).
Ohki, S. Surface tension, hydration energy and membrane fusion. in Molecular Mechanisms of Membrane Fusion (eds. Ohki, S., Doyle, D., Flanagan, T.D., Hui, S.W. & Mayhew, E.) 123–139 (Plenum, New York, 1988).
Kozlov, M.M., Leikin, S.L., Chernomordik, L.V., Markin, V.S. & Chizmadzhev, Y.A. Stalk mechanism of vesicle fusion. Intermixing of aqueous contents. Eur. Biophys. J. 17, 121–129 (1989).
Kozlov, M.M. & Markin, V.S. Possible mechanism of membrane fusion. Biophysics 28, 255–261 (1983). The work was the first to propose the stalk intermediate of membrane fusion and presents calculations of the stalk energy as a function of the spontaneous curvature of the membrane monolayers.
Kozlovsky, Y., Chernomordik, L. & Kozlov, M.M. Lipid intermediates in membrane fusion: formation, structure, and decay of hemifusion diaphragm. Biophys. J. 83, 2634–2651 (2002).
Kozlovsky, Y., Efrat, A., Siegel, D.P. & Kozlov, M.M. Stalk phase formation: effects of dehydration and saddle splay modulus. Biophys. J. 87, 2508–2521 (2004).
Kozlovsky, Y. & Kozlov, M.M. Stalk model of membrane fusion: solution of energy crisis. Biophys. J. 82, 882–895 (2002). Energy of fusion stalk is computed using the tilt-splay model for membrane mechanics. The analysis predicts a biologically feasible energy barrier of stalk formation.
Kuzmin, P.I., Zimmerberg, J., Chizmadzhev, Y.A. & Cohen, F.S. A quantitative model for membrane fusion based on low-energy intermediates. Proc. Natl. Acad. Sci. USA 98, 7235–7240 (2001).
Siegel, D.P. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophys. J. 65, 2124–2140 (1993).
May, S. Structure and energy of fusion stalks: The role of membrane edges. Biophys. J. 83, 2969–2980 (2002).
Katsov, K., Muller, M. & Schick, M. Field theoretic study of bilayer membrane fusion. I. Hemifusion mechanism. Biophys. J. 87, 3277–3290 (2004).
Katsov, K., Muller, M. & Schick, M. Field theoretic study of bilayer membrane fusion: II. Mechanism of a stalk-hole complex. Biophys. J. 90, 915–926 (2006).
Marrink, S.J. & Mark, A.E. The Mechanism of Vesicle Fusion as Revealed by Molecular Dynamics Simulations. J. Am. Chem. Soc. 125, 11144–11145 (2003).
Marrink, S.J. & Tieleman, D.P. Molecular dynamics simulation of spontaneous membrane fusion during a cubic-hexagonal phase transition. Biophys. J. 83, 2386–2392 (2002).
Knecht, V. & Marrink, S.J. Molecular dynamics simulations of lipid vesicle fusion in atomic detail. Biophys. J. 92, 4254–4261 (2007). The work presents the molecular dynamic simulation of membrane fusion in atomic detail, largely confirms the fusion pathway through a hemifusion diaphragm and provides a computational basis for more detailed investigation of the fusion intermediates.
Muller, M., Katsov, K. & Schick, M. A new mechanism of model membrane fusion determined from Monte Carlo simulation. Biophys. J. 85, 1611–1623 (2003).
Noguchi, H. & Takasu, M. Self-assembly of amphiphiles into vesicles: A Brownian dynamics simulation. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 64, 041913 (2001).
Noguchi, H. & Takasu, M. Fusion pathways of vesicles: a Brownian dynamics simulation. J. Chem. Phys. 115, 9547–9551 (2001).
Grafmuller, A., Shillcock, J. & Lipowsky, R. Pathway of membrane fusion with two tension-dependent energy barriers. Phys. Rev. Lett. 98, 218101 (2007).
Shillcock, J.C. & Lipowsky, R. Tension-induced fusion of bilayer membranes and vesicles. Nat. Mater. 4, 225–228 (2005).
Efrat, A., Chernomordik, L.V. & Kozlov, M.M. Point-like protrusion as a prestalk intermediate in membrane fusion pathway. Biophys. J. 92, L61–L63 (2007).
Hamm, M. & Kozlov, M.M. Tilt model of inverted amphiphilic mesophases. Eur. Phys. J. B 6, 519–528 (1998).
Hamm, M. & Kozlov, M.M. Elastic energy of tilt and bending of fluid membranes. Eur. Phys. J. E 3, 323–335 (2000).
May, S., Kozlovsky, Y., Ben-Shaul, A. & Kozlov, M.M. Tilt modulus of a lipid monolayer. Eur. Phys. J. E 14, 299–308 (2004).
Siegel, D.P. & Kozlov, M.M. The gaussian curvature elastic modulus of N-monomethylated dioleoylphosphatidylethanolamine: relevance to membrane fusion and lipid phase behavior. Biophys. J. 87, 366–374 (2004).
Lee, J.Y. & Schick, M. Dependence of the energies of fusion on the intermembrane separation: optimal and constrained. J. Chem. Phys. 127, 075102 (2007).
Lee, J.Y. & Schick, M. Field theoretic study of bilayer membrane fusion III: membranes with leaves of different composition. Biophys. J. 92, 3938–3948 (2007).
Lee, J.Y. & Schick, M. Calculation of free energy barriers to the fusion of small vesicles. Biophys. J. 94, 1699–1706 (2008).
Marrink, S.J., de Vries, A.H. & Mark, A.E. Coarse grained model for semiquantitative lipid simulations. J. Phys. Chem. B 108, 750–760 (2004).
Lindahl, E. & Edholm, O. Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. Biophys. J. 79, 426–433 (2000).
Yang, L. & Huang, H.W. Observation of a membrane fusion intermediate structure. Science 297, 1877–1879 (2002).
Cornell, B.A., Fletcher, G.C., Middlehurst, J. & Separovic, F. The lower limit to the size of small sonicated phospholipid vesicles. Biochim. Biophys. Acta 690, 15–19 (1982).
Kasson, P.M. & Pande, V.S. Control of membrane fusion mechanism by lipid composition: predictions from ensemble molecular dynamics. PLoS Comput. Biol. 3, e220 (2007).
Chernomordik, L.V., Melikyan, G.B., Abidor, I.G., Markin, V.S. & Chizmadzhev, Y.A. The shape of lipid molecules and monolayer membrane fusion. Biochim. Biophys. Acta 812, 643–655 (1985).
Kozlov, M.M. & Chernomordik, L.V. A mechanism of protein-mediated fusion: coupling between refolding of the influenza hemagglutinin and lipid rearrangements. Biophys. J. 75, 1384–1396 (1998).
Martens, S., Kozlov, M.M. & McMahon, H.T. How synaptotagmin promotes membrane fusion. Science 316, 1205–1208 (2007). The work demonstrates the ability of synaptotagmin C 2 to bend membranes into 17-nm-diameter tubes with fusogenic end caps and suggests a new model of protein mediated membrane fusion based on calcium-dependent insertion of the synaptotagmin C 2 domain into the membrane matrix.
Hed, G. & Safran, S.A. Initiation and dynamics of hemifusion in lipid bilayers. Biophys. J. 85, 381–389 (2003).
Chernomordik, L. Non-bilayer lipids and biological fusion intermediates. Chem. Phys. Lipids 81, 203–213 (1996).
Blood, P.D. & Voth, G.A. Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proc. Natl. Acad. Sci. USA 103, 15068–15072 (2006).
Ayton, G.S., Blood, P.D. & Voth, G.A. Membrane remodeling from N-BAR domain interactions: insights from multi-scale simulation. Biophys. J. 92, 3595–3602 (2007).
Campelo, F., McMahon, H.T. & Kozlov, M.M. The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. (in the press) (2008).
Chernomordik, L.V., Zimmerberg, J. & Kozlov, M.M. Membranes of the world unite! J. Cell Biol. 175, 201–207 (2006).
Chernomordik, L.V., Frolov, V.A., Leikina, E., Bronk, P. & Zimmerberg, J. The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. J. Cell Biol. 140, 1369–1382 (1998). The first work (i) describing hemifusion mediated by wild-type protein fusogen, (ii) identifying restricted hemifusion intermediates and (iii) reporting the dependence of fusion pore formation on the lipid composition of the distal membrane leaflets.
Zimmerberg, J., Blumenthal, R., Sarkar, D.P., Curran, M. & Morris, S.J. Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. J. Cell Biol. 127, 1885–1894 (1994).
Leikina, E. & Chernomordik, L.V. Reversible merger of membranes at the early stage of influenza hemagglutinin-mediated fusion. Mol. Biol. Cell 11, 2359–2371 (2000).
Markosyan, R.M., Bates, P., Cohen, F.S. & Melikyan, G.B. A study of low pH-induced refolding of Env of avian sarcoma and leukosis virus into a six-helix bundle. Biophys. J. 87, 3291–3298 (2004).
Zaitseva, E., Mittal, A., Griffin, D.E. & Chernomordik, L.V. Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J. Cell Biol. 169, 167–177 (2005).
Yoon, T.Y., Okumus, B., Zhang, F., Shin, Y.K. & Ha, T. Multiple intermediates in SNARE-induced membrane fusion. Proc. Natl. Acad. Sci. USA 103, 19731–19736 (2006). By imaging real-time dynamics of single fusion events between the SNARE-carrying liposomes, this work identifies fusion intermediates with distinct extents of lipid mixing and characterizes the dwell times of docked and hemifused states and the lifetime of early fusion pores.
Melikyan, G.B., Niles, W.D. & Cohen, F.S. Influenza virus hemagglutinin-induced cell-planar bilayer fusion: quantitative dissection of fusion pore kinetics into stages. J. Gen. Physiol. 102, 1151–1170 (1993).
Mittal, A., Leikina, E., Chernomordik, L.V. & Bentz, J. Kinetically differentiating influenza hemagglutinin fusion and hemifusion machines. Biophys. J. 85, 1713–1724 (2003).
Giraudo, C.G. et al. SNAREs can promote complete fusion and hemifusion as alternative outcomes. J. Cell Biol. 170, 249–260 (2005).
Zimmerberg, J. & Chernomordik, L.V. Neuroscience. Synaptic membranes bend to the will of a neurotoxin. Science 310, 1626–1627 (2005).
Zampighi, G.A. et al. Conical electron tomography of a chemical synapse: vesicles docked to the active zone are hemi-fused. Biophys. J. 91, 2910–2918 (2006).
Wong, J.L., Koppel, D.E., Cowan, A.E. & Wessel, G.M. Membrane hemifusion is a stable intermediate of exocytosis. Dev. Cell 12, 653–659 (2007).
Schaub, J.R., Lu, X., Doneske, B., Shin, Y.K. & McNew, J.A. Hemifusion arrest by complexin is relieved by Ca2+-synaptotagmin I. Nat. Struct. Mol. Biol. 13, 748–750 (2006).
Razinkov, V.I., Melikyan, G.B., Epand, R.M., Epand, R.F. & Cohen, F.S. Effects of spontaneous bilayer curvature on influenza virus-mediated fusion pores. J. Gen. Physiol. 112, 409–422 (1998).
Chernomordik, L.V., Leikina, E., Frolov, V., Bronk, P. & Zimmerberg, J. An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol. 136, 81–94 (1997).
Chernomordik, L.V. et al. Lysolipids reversibly inhibit Ca2+-, GTP- and pH-dependent fusion of biological membranes. FEBS Lett. 318, 71–76 (1993). This paper demonstrates that lipids known to inhibit hemifusion stage of fusion between protein-free bilayers also inhibit disparate biological fusion reactions, suggesting that these reactions proceed through a common hemifusion intermediate.
Melikyan, G.B., Barnard, R.J., Abrahamyan, L.G., Mothes, W. & Young, J.A. Imaging individual retroviral fusion events: from hemifusion to pore formation and growth. Proc. Natl. Acad. Sci. USA 102, 8728–8733 (2005). Different stages of virus–cell fusion mediated by avian sarcoma and leukosis virus envelope glycoproteins were dissected by imaging single virions. The findings suggest that fusion involves a direct transition from hemifusion into a small and then growing pore within a small virus-2013 cell contact zone.
Markosyan, R.M., Cohen, F.S. & Melikyan, G.B. Time-resolved imaging of HIV-1 Env-mediated lipid and content mixing between a single virion and cell membrane. Mol. Biol. Cell 16, 5502–5513 (2005).
Liu, T., Wang, T., Chapman, E.R. & Weisshaar, J.C. Productive hemifusion intermediates in fast vesicle fusion driven by neuronal SNAREs. Biophys. J. 94, 1303–1314 (2008).
Frolov, V.A., Dunina-Barkovskaya, A.Y., Samsonov, A.V. & Zimmerberg, J. Membrane permeability changes at early stages of influenza hemagglutinin-mediated fusion. Biophys. J. 85, 1725–1733 (2003).
Lindau, M. & Almers, W. Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Curr. Opin. Cell Biol. 7, 509–517 (1995).
Jackson, M.B. & Chapman, E.R. Fusion pores and fusion machines in Ca2+-triggered exocytosis. Annu. Rev. Biophys. Biomol. Struct. 35, 135–160 (2006).
Kemble, G.W., Danieli, T. & White, J.M. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76, 383–391 (1994). Replacing transmembrane domain of influenza hemagglutinin with a lipid anchor yielded the first direct demonstration that protein fusogens can induce hemifusion and emphasized the functional importance of transmembrane domain of the fusogen.
Cleverley, D.Z. & Lenard, J. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 95, 3425–3430 (1998).
Grote, E., Baba, M., Ohsumi, Y. & Novick, P.J. Geranylgeranylated SNAREs are dominant inhibitors of membrane fusion. J. Cell Biol. 151, 453–466 (2000).
Xu, Y., Zhang, F., Su, Z., McNew, J.A. & Shin, Y.K. Hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12, 417–422 (2005). This study on fusion between SNARE-proteoliposomes was the first direct demonstration that intracellular fusogens can mediate hemifusion.
Langosch, D., Hofmann, M. & Ungermann, C. The role of transmembrane domains in membrane fusion. Cell. Mol. Life Sci. 64, 850–864 (2007).
Melikyan, G.B., Lin, S., Roth, M.G. & Cohen, F.S. Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell 10, 1821–1836 (1999).
Frolov, V., Cho, M.-S., Bronk, P., Reese, T. & Zimmerberg, J. Multiple local contact sites are induced by GPI-linked influenza hemagglutinin during hemifusion and flickering pore formation. Traffic 1, 622–630 (2000).
Markosyan, R.M., Cohen, F.S. & Melikyan, G.B. The lipid-anchored ectodomain of influenza virus hemagglutinin (GPI-HA) is capable of inducing nonenlarging fusion pores. Mol. Biol. Cell 11, 1143–1152 (2000).
McNew, J.A. et al. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150, 105–117 (2000).
Jun, Y., Xu, H., Thorngren, N. & Wickner, W. Sec18p and Vam7p remodel trans-SNARE complexes to permit a lipid-anchored R-SNARE to support yeast vacuole fusion. EMBO J. 26, 4935–4945 (2007).
Jun, Y. & Wickner, W. Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc. Natl. Acad. Sci. USA 104, 13010–13015 (2007).
Vogel, S.S., Leikina, E.A. & Chernomordik, L.V. Lysophosphatidylcholine reversibly arrests exocytosis and viral fusion at a stage between triggering and membrane merger. J. Biol. Chem. 268, 25764–25768 (1993).
Reese, C., Heise, F. & Mayer, A. Trans-SNARE pairing can precede a hemifusion intermediate in intracellular membrane fusion. Nature 436, 410–414 (2005).
Amatore, C. et al. Regulation of exocytosis in chromaffin cells by trans-insertion of lysophosphatidylcholine and arachidonic acid into the outer leaflet of the cell membrane. ChemBioChem 7, 1998–2003 (2006).
Churchward, M.A. et al. Specific lipids supply critical negative spontaneous curvature–an essential component of native Ca2+-triggered membrane fusion. Biophys. J. 94, 3976–3986 (2008).
Ramos, C., Rafikova, E.R., Melikov, K. & Chernomordik, L.V. Transmembrane proteins are not required for early stages of nuclear envelope assembly. Biochem. J. 400, 393–400 (2006).
Podbilewicz, B. et al. The C. elegans developmental fusogen EFF-1 mediates homotypic fusion in heterologous cells and in vivo. Dev. Cell 11, 471–481 (2006).
Kobayashi, T. et al. Separation and characterization of late endosomal membrane domains. J. Biol. Chem. 277, 32157–32164 (2002).
Byrne, R.D. et al. PLCγ is enriched on poly-phosphoinositide-rich vesicles to control nuclear envelope assembly. Cell Signal. 19, 913–922 (2006).
Rigoni, M. et al. Equivalent effects of snake PLA2 neurotoxins and lysophospholipid-fatty acid mixtures. Science 310, 1678–1680 (2005).
Blumenthal, R., Clague, M.J., Durell, S.R. & Epand, R.M. Membrane fusion. Chem. Rev. 103, 53–69 (2003).
Lai, A.L., Park, H., White, J.M. & Tamm, L.K. Fusion peptide of influenza hemagglutinin requires a fixed angle boomerang structure for activity. J. Biol. Chem. 281, 5760–5770 (2006).
Shmulevitz, M. & Duncan, R. A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses. EMBO J. 19, 902–912 (2000).
Roche, S., Bressanelli, S., Rey, F.A. & Gaudin, Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313, 187–191 (2006). This high resolution x-ray study, along with an earlier work of this group, characterizes a new class of viral fusion proteins (class III) that uses a bipartite fusion domain consisting of two short, noncontiguous hydrophobic loops.
McMahon, H.T. & Gallop, J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590–596 (2005).
Chapman, E.R. & Davis, A.F. Direct interaction of a Ca2+-binding loop of synaptotagmin with lipid bilayers. J. Biol. Chem. 273, 13995–14001 (1998).
Cohen, F.S. & Melikyan, G.B. The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199, 1–14 (2004).
Zimmerberg, J., Akimov, S.A. & Frolov, V. Synaptotagmin: fusogenic role for calcium sensor? Nat. Struct. Mol. Biol. 13, 301–303 (2006).
Kozlov, M.M. & Chernomordik, L.V. The protein coat in membrane fusion: lessons from fission. Traffic 3, 256–267 (2002).
Leikina, E. et al. Influenza hemagglutinins outside of the contact zone are necessary for fusion pore expansion. J. Biol. Chem. 279, 26526–26532 (2004).
Yang, X., Kurteva, S., Ren, X., Lee, S. & Sodroski, J. Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1. J. Virol. 79, 12132–12147 (2005).