Intracellular curvature-generating proteins in cell-to-cell fusion

Biochemical Journal

Volumn 440, Issue 2, 2011, Pages 185-193

  Richard, Jean Philippe ^a,e   Leikina, Evgenia ^a   Langen, Ralf ^b   Henne, William Mike ^c,f   Popova, Margarita ^a   Balla, Tamas ^a   Mcmahon, Harvey T ^c   Kozlov, Michael M ^d   Chernomordik, Leonid V ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d TEL AVIV UNIVERSITY   (Israel)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHYSIN; CURVED DNA; DYNAMIN; EPSIN; FOCAL ADHESION KINASE 1; GUANOSINE TRIPHOSPHATASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACULOVIRUS; CELL FUSION; CELL MEMBRANE; INFLUENZA VIRUS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SYNCYTIUM;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL FUSION; CELL MEMBRANE; DYNAMINS; GIANT CELLS; HEMAGGLUTININS, VIRAL; MEMBRANE FUSION; MEMBRANE PROTEINS; MICE; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN STRUCTURE, TERTIARY;

ORTHOMYXOVIRIDAE;

EID: 81155132276     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111243     Document Type: Article

References (68)

1. Jahn, R., Lang, T. and Sudhof, T. C. (2003) Membrane fusion. Cell 112, 519-533 (Pubitemid 36263084)
2. Earp, L. J., Delos, S. E., Park, H. E. and White, J. M. (2005) The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285, 25-66
3. Chen, E. H., Grote, E., Mohler, W. and Vignery, A. (2007) Cell-cell fusion. FEBS Lett. 581, 2181-2193 (Pubitemid 46722606)
4. Duelli, D. and Lazebnik, Y. (2007) Cell-to-cell fusion as a link between viruses and cancer. Nat. Rev. Cancer 7, 968-976 (Pubitemid 350165858)
5. Sapir, A., Avinoam, O., Podbilewicz, B. and Chernomordik, L. V. (2008) Viral and developmental cell fusion mechanisms: conservation and divergence. Dev. Cell 14, 11-21
6. Kielian, M. and Rey, F. A. (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4, 67-76 (Pubitemid 43135288)
7. Weissenhorn, W., Hinz, A. and Gaudin, Y. (2007) Virus membrane fusion. FEBS Lett. 581, 2150-2155 (Pubitemid 46722604)
8. Martens, S. and McMahon, H. T. (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9, 543-556 (Pubitemid 351881838)
9. Cohen, F. S. and Melikyan, G. B. (2004) The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199, 1-14 (Pubitemid 38766422)
10. Chernomordik, L. V., Zimmerberg, J. and Kozlov, M. M. (2006) Membranes of the world unite. J. Cell Biol. 175, 201-207
11. 2+-triggered exocytosis. Nat. Struct. Mol. Biol. 15, 684-689
12. Richard, J. P., Leikina, E. and Chernomordik, L. V. (2009) Cytoskeleton reorganization in influenza hemagglutinin-initiated syncytium formation. Biochim. Biophys. Acta 1788, 450-457
13. Chen, A., Leikina, E., Melikov, K., Podbilewicz, B., Kozlov, M. M. and Chernomordik, L. V. (2008) Fusion-pore expansion during syncytium formation is restricted by an actin network. J. Cell Sci. 121, 3619-3628
14. Plonsky, I. and Zimmerberg, J. (1996) The initial fusion pore induced by baculovirus GP64 is large and forms quickly. J. Cell Biol. 135, 1831-1839 (Pubitemid 27036444)
15. Zimmerberg, J., Blumenthal, R., Sarkar, D. P., Curran, M. and Morris, S. J. (1994) Restricted movement of lipid and aqueous dyes through pores formed by influenza hemagglutinin during cell fusion. J. Cell Biol. 127, 1885-1894
16. Zheng, Q. A. and Chang, D. C. (1991) Reorganization of cytoplasmic structures during cell fusion. J. Cell Sci. 100, 431-442
17. Massarwa, R., Carmon, S., Shilo, B. Z. and Schejter, E. D. (2007) WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila . Dev. Cell 12, 557-569 (Pubitemid 46523636)
18. Gildor, B., Massarwa, R., Shilo, B. Z. and Schejter, E. D. (2009) The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep. 10, 1043-1050
19. Wurth, M. A., Schowalter, R. M., Smith, E. C., Moncman, C. L., Dutch, R. E. and McCann, R. O. (2010) The actin cytoskeleton inhibits pore expansion during PIV5 fusion protein-promoted cell-cell fusion. Virology 404, 117-126
20. Dawson, J. C., Legg, J. A. and Machesky, L. M. (2006) Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16, 493-498 (Pubitemid 44442959)
21. Doherty, G. J. and McMahon, H. T. (2008) Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu. Rev. Biophys. 37, 65-95
22. Hinshaw, J. E. (2000) Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16, 483-519
23. Praefcke, G. J. and McMahon, H. T. (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147 (Pubitemid 38160256)
24. Mettlen, M., Pucadyil, T., Ramachandran, R. and Schmid, S. L. (2009) Dissecting dynamin's role in clathrin-mediated endocytosis. Biochem. Soc. Trans. 37, 1022-1026
25. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R. and McMahon, H. T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366
26. Itoh, T. and De Camilli, P. (2006) BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912 (Pubitemid 44332330)
27. Doherty, G. J. and Lundmark, R. (2009) GRAF1-dependent endocytosis. Biochem. Soc. Trans. 37, 1061-1065
28. Lundmark, R., Doherty, G. J., Howes, M. T., Cortese, K., Vallis, Y., Parton, R. G. and McMahon, H. T. (2008) The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr. Biol. 18, 1802-1808
29. Lundmark, R. and Carlsson, S. R. (2010) Driving membrane curvature in clathrindependent and clathrin-independent endocytosis. Semin. Cell Dev. Biol. 21, 363-370
30. Henne, W. M., Boucrot, E., Meinecke, M., Evergren, E., Vallis, Y., Mittal, R. and McMahon, H. T. (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284
31. Takenawa, T. (2010) Phosphoinositide-binding interface proteins involved in shaping cell membranes. Proc. Jpn. Acad., Ser. B 86, 509-523
32. Doberstein, S. K., Fetter, R. D., Mehta, A. Y. and Goodman, C. S. (1997) Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J. Cell Biol. 136, 1249-1261 (Pubitemid 27421913)
33. Mohler, W. A., Simske, J. S., Williams-Masson, E. M., Hardin, J. D. and White, J. G. (1998) Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Curr. Biol. 8, 1087-1090 (Pubitemid 28451034)
34. Sens, K. L., Zhang, S., Jin, P., Duan, R., Zhang, G., Luo, F., Parachini, L. and Chen, E. H. (2010) An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J. Cell Biol. 191, 1013-1027
35. Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C. and Kirchhausen, T. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850 (Pubitemid 43779110)
36. Quan, A., McGeachie, A. B., Keating, D. J., van Dam, E. M., Rusak, J., Chau, N., Malladi, C. S., Chen, C., McCluskey, A., Cousin, M. A. and Robinson, P. J. (2007) Myristyl trimethyl ammonium bromide and octadecyl trimethyl ammonium bromide are surface-active small molecule dynamin inhibitors that block endocytosis mediated by dynamin I or dynamin II. Mol. Pharmacol. 72, 1425-1439 (Pubitemid 350146080)
37. Hill, T. A., Gordon, C. P., McGeachie, A. B., Venn-Brown, B., Odell, L. R., Chau, N., Quan, A., Mariana, A., Sakoff, J. A., Chircop, M. et al. (2009) Inhibition of dynamin mediated endocytosis by the dynoles-synthesis and functional activity of a family of indoles. J. Med. Chem. 52, 3762-3773
38. Cunningham, C. C., Vegners, R., Bucki, R., Funaki, M., Korde, N., Hartwig, J. H., Stossel, T. P. and Janmey, P. A. (2001) Cell permeant polyphosphoinositide-binding peptides that block cell motility and actin assembly. J. Biol. Chem. 276, 43390-43399
39. Holz, R. W., Hlubek, M. D., Sorensen, S. D., Fisher, S. K., Balla, T., Ozaki, S., Prestwich, G. D., Stuenkel, E. L. and Bittner, M. A. (2000) A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis. J. Biol. Chem. 275, 17878-17885 (Pubitemid 30430841)
40. Song, B. D., Leonard, M. and Schmid, S. L. (2004) Dynamin GTPase domain mutants that differentially affect GTP binding, GTP hydrolysis, and clathrin-mediated endocytosis. J. Biol. Chem. 279, 40431-40436 (Pubitemid 39287632)
41. Song, B. D., Yarar, D. and Schmid, S. L. (2004) An assembly-incompetent mutant establishes a requirement for dynamin self-assembly in clathrin-mediated endocytosis in vivo. Mol. Biol. Cell 15, 2243-2252 (Pubitemid 38580642)
42. Damke, H., Baba, T., Warnock, D. E. and Schmid, S. L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934 (Pubitemid 24355982)
43. Damke, H., Binns, D. D., Ueda, H., Schmid, S. L. and Baba, T. (2001) Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12, 2578-2589 (Pubitemid 33051926)
44. Marks, B., Stowell, M. H., Vallis, Y., Mills, I. G., Gibson, A., Hopkins, C. R. and McMahon, H. T. (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235 (Pubitemid 32216598)
45. Chernomordik, L. V., Frolov, V. A., Leikina, E., Bronk, P. and Zimmerberg, J. (1998) The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. J. Cell Biol. 140, 1369-1382 (Pubitemid 28152986)
46. Plonsky, I., Cho, M. S., Oomens, A. G., Blissard, G. and Zimmerberg, J. (1999) An analysis of the role of the target membrane on the Gp64-induced fusion pore. Virology 253, 65-76 (Pubitemid 29391559)
47. Chernomordik, L., Leikina, E. and Zimmerberg, J. (1995) Control of baculovirus gp64-induced syncytia formation by membrane lipid composition. J. Virol. 69, 3049-3058
48. Markovic, I., Leikina, E., Zhukovsky, M., Zimmerberg, J. and Chernomordik, L. V. (2001) Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machines. J. Cell Biol. 155, 833-844
49. Henne, W. M., Kent, H. M., Ford, M. G., Hegde, B. G., Daumke, O., Butler, P. J., Mittal, R., Langen, R., Evans, P. R. and McMahon, H. T. (2007) Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839-852 (Pubitemid 47042426)
50. Kruchten, A. E. and McNiven, M. A. (2006) Dynamin as a mover and pincher during cell migration and invasion. J. Cell Sci. 119, 1683-1690 (Pubitemid 43810995)
51. Boucrot, E., Saffarian, S., Massol, R., Kirchhausen, T. and Ehrlich, M. (2006) Role of lipids and actin in the formation of clathrin-coated pits. Exp. Cell Res. 312, 4036-4048 (Pubitemid 44828048)
52. Balla, T. and Varnai, P. (2009) Visualization of cellular phosphoinositide pools with GFP-fused protein-domains. Curr. Protoc. Cell Biol. 24, 24.4
53. Kempf, C., Kohler, U., Michel, M. R. and Koblet, H. (1987) Semliki Forest virus-induced polykaryocyte formation is an ATP-dependent event. Arch. Virol. 95, 111-122 (Pubitemid 17117788)
54. Wang, E., Cross, R. K. and Choppin, P. W. (1979) Involvement of microtubules and 10-nm filaments in the movement and positioning of nuclei in syncytia. J. Cell Biol. 83, 320-337 (Pubitemid 10205717)
55. Doherty, J., Lenhart, K., Cameron, M., Mack, C., Conlon, F. and Taylor, J. (2011) Skeletal muscle differentiation and fusion is regulated by the BAR-containing Rho GAP, GRAF1. J. Biol. Chem. 286, 25903-25921
56. Mittal, A., Leikina, E., Chernomordik, L. V. and Bentz, J. (2003) Kinetically differentiating influenza hemagglutinin fusion and hemifusion machines. Biophys. J. 85, 1713-1724 (Pubitemid 37052254)
57. Lai, W., Huang, L., Ho, P., Montefiori, D. and Chen, C. H. (2011) The role of dynamin in HIV type 1 env-mediated cell-cell fusion. AIDS Res. Hum. Retroviruses 27, 1013-1017
58. Rustom, A., Saffrich, R., Markovic, I., Walther, P. and Gerdes, H. H. (2004) Nanotubular highways for intercellular organelle transport. Science 303, 1007-1010 (Pubitemid 38209703)
59. Niu, X., Gupta, K., Yang, J. T., Shamblott, M. J. and Levchenko, A. (2009) Physical transfer of membrane and cytoplasmic components as a general mechanism of cell-cell communication. J. Cell Sci. 122, 600-610
60. Hoppins, S., Lackner, L. and Nunnari, J. (2007) The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780
61. Hoppins, S. and Nunnari, J. (2009) The molecular mechanism of mitochondrial fusion. Biochim. Biophys. Acta 1793, 20-26
62. Hu, J., Shibata, Y., Zhu, P. P., Voss, C., Rismanchi, N., Prinz, W. A., Rapoport, T. A. and Blackstone, C. (2009) A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 138, 549-561
63. Orso, G., Pendin, D., Liu, S., Tosetto, J., Moss, T. J., Faust, J. E., Micaroni, M., Egorova, A., Martinuzzi, A., McNew, J. A. and Daga, A. (2009) Homotypic fusion of ER membranes requires the dynamin-like GTPase atlastin. Nature 460, 978-983
64. Miyauchi, K., Kim, Y., Latinovic, O., Morozov, V. and Melikyan, G. B. (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137, 433-444
65. Jaiswal, J. K., Rivera, V. M. and Simon, S. M. (2009) Exocytosis of post-Golgi vesicles is regulated by components of the endocytic machinery. Cell 137, 1308-1319
66. Anantharam, A., Bittner, M. A., Aikman, R. L., Stuenkel, E. L., Schmid, S. L., Axelrod, D. and Holz, R. W. (2011) A new role for the dynamin GTPase in the regulation of fusion pore expansion. Mol. Biol. Cell 22, 1907-1918
67. Llobet, A., Wu, M. and Lagnado, L. (2008) The mouth of a dense-core vesicle opens and closes in a concerted action regulated by calcium and amphiphysin. J. Cell Biol. 182, 1017-1028
68. Kozlov, M. M., McMahon, H. T. and Chernomordik, L. V. (2010) Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35, 699-706