Viral and Developmental Cell Fusion Mechanisms: Conservation and Divergence

Developmental Cell

Volumn 14, Issue 1, 2008, Pages 11-21

  Sapir, Amir ^a   Avinoam, Ori ^a   Podbilewicz, Benjamin ^a   Chernomordik, Leonid V ^b  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANCHOR CELL FUSION FAILURE 1; CELL PROTEIN; CELL SURFACE RECEPTOR; EPITHELIAL FUSION FAILURE 1; FUSION ASSOCIATED SMALL TRANSMEMBRANE PROTEIN; HEMAGGLUTININ; MEMBRANE PHOSPHOLIPID; PHOSPHOLIPASE; SNARE PROTEIN; SYNCYTIN 1; SYNCYTIN 2; UNCLASSIFIED DRUG; VIRAL FUSOGEN; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN;

CAENORHABDITIS ELEGANS; CELL FUSION; DEVELOPMENTAL STAGE; EUKARYOTE; GAMETE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA VIRUS A; INFLUENZA VIRUS B; INFLUENZA VIRUS C; MACROPHAGE; MOLECULAR MECHANICS; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; TROPHOBLAST; VIRUS CELL INTERACTION;

AGING; AMINO ACID SEQUENCE; ANIMALS; CELL FUSION; CELL MEMBRANE; CONSERVED SEQUENCE; FEMALE; HUMANS; MEMBRANE FUSION; MEMBRANE LIPIDS; MOLECULAR SEQUENCE DATA; PLACENTA; PREGNANCY; VIRAL PHYSIOLOGY;

EUKARYOTA;

EID: 37749019200     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2007.12.008     Document Type: Review

References (99)

1. Alper S., and Kenyon C. REF-1, a protein with two bHLH domains, alters the pattern of cell fusion in C. elegans by regulating Hox protein activity. Development 128 (2001) 1793-1804
2. Alper S., and Kenyon C. The zinc finger protein REF-2 functions with the Hox genes to inhibit cell fusion in the ventral epidermis of C. elegans. Development 129 (2002) 3335-3348
3. Bentz J. Membrane fusion mediated by coiled coils: a hypothesis. Biophys. J. 78 (2000) 886-900
4. Blaise S., de Parseval N., Benit L., and Heidmann T. Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc. Natl. Acad. Sci. USA 100 (2003) 13013-13018
5. Blond J.L., Beseme F., Duret L., Bouton O., Bedin F., Perron H., Mandrand B., and Mallet F. Molecular characterization and placental expression of HERV-W, a new human endogenous retrovirus family. J. Virol. 73 (1999) 1175-1185
6. Blond J.L., Lavillette D., Cheynet V., Bouton O., Oriol G., Chapel-Fernandes S., Mandrand B., Mallet F., and Cosset F.L. An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J. Virol. 74 (2000) 3321-3329
7. Bonifacino J.S., and Glick B.S. The mechanisms of vesicle budding and fusion. Cell 116 (2004) 153-166
8. Borrego-Diaz E., Peeples M.E., Markosyan R.M., Melikyan G.B., and Cohen F.S. Completion of trimeric hairpin formation of influenza virus hemagglutinin promotes fusion pore opening and enlargement. Virology 316 (2003) 234-244
9. Byrne R.D., Garnier-Lhomme M., Han K., Dowicki M., Michael N., Totty N., Zhendre V., Cho A., Pettitt T.R., Wakelam M.J., et al. PLCgamma is enriched on poly-phosphoinositide-rich vesicles to control nuclear envelope assembly. Cell. Signal. 19 (2007) 913-922
10. Cai H., Reinisch K., and Ferro-Novick S. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 12 (2007) 671-682
11. Cassata G., Shemer G., Morandi P., Donhauser R., Podbilewicz B., and Baumeister R. ceh-16/engrailed patterns the embryonic epidermis of Caenorhabditis elegans. Development 132 (2005) 739-749
12. Chandran K., Sullivan N.J., Felbor U., Whelan S.P., and Cunningham J.M. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308 (2005) 1643-1645
13. Chen E.H., and Olson E.N. Unveiling the mechanisms of cell-cell fusion. Science 308 (2005) 369-373
14. Chen E.H., Grote E., Mohler W., and Vignery A. Cell-cell fusion. FEBS Lett. 581 (2007) 2181-2193
15. Cheng L.T., Plemper R.K., and Compans R.W. Atypical fusion peptide of Nelson Bay virus fusion-associated small transmembrane protein. J. Virol. 79 (2005) 1853-1860
16. Chernomordik L.V., and Kozlov M.M. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72 (2003) 175-207
17. Chernomordik L.V., and Kozlov M.M. Membrane hemifusion: crossing a chasm in two leaps. Cell 123 (2005) 375-382
18. Chernomordik L.V., Vogel S.S., Sokoloff A., Onaran H.O., Leikina E.A., and Zimmerberg J. Lysolipids reversibly inhibit Ca(2+)-, GTP- and pH-dependent fusion of biological membranes. FEBS Lett. 318 (1993) 71-76
19. Chernomordik L.V., Zimmerberg J., and Kozlov M.M. Membranes of the world unite!. J. Cell Biol. 175 (2006) 201-207
20. Cheynet V., Ruggieri A., Oriol G., Blond J.L., Boson B., Vachot L., Verrier B., Cosset F.L., and Mallet F. Synthesis, assembly, and processing of the Env ERVWE1/syncytin human endogenous retroviral envelope. J. Virol. 79 (2005) 5585-5593
21. Choi J., Richards K.L., Cinar H.N., and Newman A.P. N-ethylmaleimide sensitive factor is required for fusion of the C. elegans uterine anchor cell. Dev. Biol. 297 (2006) 87-102
22. Clamp M., Cuff J., Searle S.M., and Barton G.J. The Jalview Java alignment editor. Bioinformatics 20 (2004) 426-427
23. Cohen F.S., and Melikyan G.B. The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199 (2004) 1-14
24. Danieli T., Pelletier S.L., Henis Y.I., and White J.M. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J. Cell Biol. 133 (1996) 559-569
25. de Parseval N., and Heidmann T. Human endogenous retroviruses: from infectious elements to human genes. Cytogenet. Genome Res. 110 (2005) 318-332
26. de Parseval N., Lazar V., Casella J.F., Benit L., and Heidmann T. Survey of human genes of retroviral origin: identification and transcriptome of the genes with coding capacity for complete envelope proteins. J. Virol. 77 (2003) 10414-10422
27. del Campo J.J., Opoku-Serebuoh E., Isaacson A.B., Scranton V.L., Tucker M., Han M., and Mohler W.A. Fusogenic activity of EFF-1 is regulated via dynamic localization in fusing somatic cells of C. elegans. Curr. Biol. 15 (2005) 413-423
28. Dupressoir A., Marceau G., Vernochet C., Benit L., Kanellopoulos C., Sapin V., and Heidmann T. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc. Natl. Acad. Sci. USA 102 (2005) 725-730
29. Earp L.J., Delos S.E., Park H.E., and White J.M. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285 (2005) 25-66
30. Frendo J.L., Olivier D., Cheynet V., Blond J.L., Bouton O., Vidaud M., Rabreau M., Evain-Brion D., and Mallet F. Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol. Cell. Biol. 23 (2003) 3566-3574
31. Gattegno T., Mittal A., Valansi C., Nguyen K.C., Hall D.H., Chernomordik L.V., and Podbilewicz B. Genetic control of fusion pore expansion in the epidermis of Caenorhabditis elegans. Mol. Biol. Cell 18 (2007) 1153-1166
32. Gaudin Y. Rabies virus-induced membrane fusion pathway. J. Cell Biol. 150 (2000) 601-612
33. Gaudin Y., Raux H., Flamand A., and Ruigrok R.W. Identification of amino acids controlling the low-pH-induced conformational change of rabies virus glycoprotein. J. Virol. 70 (1996) 7371-7378
34. Gibbons D.L., Erk I., Reilly B., Navaza J., Kielian M., Rey F.A., and Lepault J. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell 114 (2003) 573-583
35. Gibbons D.L., Vaney M.C., Roussel A., Vigouroux A., Reilly B., Lepault J., Kielian M., and Rey F.A. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427 (2004) 320-325
36. Giraudo C.G., Hu C., You D., Slovic A.M., Mosharov E.V., Sulzer D., Melia T.J., and Rothman J.E. SNAREs can promote complete fusion and hemifusion as alternative outcomes. J. Cell Biol. 170 (2005) 249-260
37. Gutierrez A., and Sommer R.J. Evolution of dnmt-2 and mbd-2-like genes in the free-living nematodes Pristionchus pacificus, Caenorhabditis elegans and Caenorhabditis briggsae. Nucleic Acids Res. 32 (2004) 6388-6396
38. Heldwein E.E., Lou H., Bender F.C., Cohen G.H., Eisenberg R.J., and Harrison S.C. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313 (2006) 217-220
39. Hu C., Ahmed M., Melia T.J., Sollner T.H., Mayer T., and Rothman J.E. Fusion of cells by flipped SNAREs. Science 300 (2003) 1745-1749
40. Huppertz B., Bartz C., and Kokozidou M. Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion. Micron 37 (2006) 509-517
41. Jahn R., and Scheller R.H. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7 (2006) 631-643
42. Jahn R., Lang T., and Sudhof T.C. Membrane fusion. Cell 112 (2003) 519-533
43. Kanaseki T., Kawasaki K., Murata M., Ikeuchi Y., and Ohnishi S. Structural features of membrane fusion between influenza virus and liposome as revealed by quick-freezing electron microscopy. J. Cell Biol. 137 (1997) 1041-1056
44. Kerbel R.S., Lagarde A.E., Dennis J.W., and Donaghue T.P. Spontaneous fusion in vivo between normal host and tumor cells: possible contribution to tumor progression and metastasis studied with a lectin-resistant mutant tumor. Mol. Cell. Biol. 3 (1983) 523-538
45. Kielian M., and Rey F.A. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4 (2006) 67-76
46. Kim S., Shilagardi K., Zhang S., Hong S.N., Sens K.L., Bo J., Gonzalez G.A., and Chen E.H. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev. Cell 12 (2007) 571-586
47. Kirsch T., Sebald W., and Dreyer M.K. Crystal structure of the BMP-2-BRIA ectodomain complex. Nat. Struct. Biol. 7 (2000) 492-496
48. Koh K., and Rothman J.H. ELT-5 and ELT-6 are required continuously to regulate epidermal seam cell differentiation and cell fusion in C. elegans. Development 128 (2001) 2867-2880
49. Koh K., Peyrot S.M., Wood C.G., Wagmaister J.A., Maduro M.F., Eisenmann D.M., and Rothman J.H. Cell fates and fusion in the C. elegans vulval primordium are regulated by the EGL-18 and ELT-6 GATA factors-apparent direct targets of the LIN-39 Hox protein. Development 129 (2002) 5171-5180
50. Kontani K., Moskowitz I.P., and Rothman J.H. Repression of cell-cell fusion by components of the C. elegans vacuolar ATPase complex. Dev. Cell 8 (2005) 787-794
51. Kozlov M.M., and Chernomordik L.V. A mechanism of protein-mediated fusion: coupling between refolding of the influenza hemagglutinin and lipid rearrangements. Biophys. J. 75 (1998) 1384-1396
52. Kozlov M.M., and Chernomordik L.V. The protein coat in membrane fusion: lessons from fission. Traffic 3 (2002) 256-267
53. Kuzmin P.I., Zimmerberg J., Chizmadzhev Y.A., and Cohen F.S. A quantitative model for membrane fusion based on low-energy intermediates. Proc. Natl. Acad. Sci. USA 98 (2001) 7235-7240
54. Leikina E., Mittal A., Cho M.S., Melikov K., Kozlov M.M., and Chernomordik L.V. Influenza hemagglutinins outside of the contact zone are necessary for fusion pore expansion. J. Biol. Chem. 279 (2004) 26526-26532
55. Lemaire I., Falzoni S., Leduc N., Zhang B., Pellegatti P., Adinolfi E., Chiozzi P., and Di Virgilio F. Involvement of the purinergic P2X7 receptor in the formation of multinucleated giant cells. J. Immunol. 177 (2006) 7257-7265
56. Lenz O., Dittmar M.T., Wagner A., Ferko B., Vorauer-Uhl K., Stiegler G., and Weissenhorn W. Trimeric membrane-anchored gp41 inhibits HIV membrane fusion. J. Biol. Chem. 280 (2005) 4095-4101
57. Livingstone C.D., and Barton G.J. Protein sequence alignments: a strategy for the hierarchical analysis of residue conservation. Comput. Appl. Biosci. 9 (1993) 745-756
58. Malassine A., Blaise S., Handschuh K., Lalucque H., Dupressoir A., Evain-Brion D., and Heidmann T. Expression of the fusogenic HERV-FRD Env glycoprotein (syncytin 2) in human placenta is restricted to villous cytotrophoblastic cells. Placenta 28 (2007) 185-191
59. Margalit A., Neufeld E., Feinstein N., Wilson K.L., Podbilewicz B., and Gruenbaum Y. Barrier to autointegration factor blocks premature cell fusion and maintains adult muscle integrity in C. elegans. J. Cell Biol. 178 (2007) 661-673
60. Marin M., Lavillette D., Kelly S.M., and Kabat D. N-linked glycosylation and sequence changes in a critical negative control region of the ASCT1 and ASCT2 neutral amino acid transporters determine their retroviral receptor functions. J. Virol. 77 (2003) 2936-2945
61. Markosyan R.M., Cohen F.S., and Melikyan G.B. HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol. Biol. Cell 14 (2003) 926-938
62. Markosyan R.M., Bates P., Cohen F.S., and 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 (2004) 3291-3298
63. Markovic I., Leikina E., Zhukovsky M., Zimmerberg J., and Chernomordik L.V. Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machines. J. Cell Biol. 155 (2001) 833-844
64. Martens S., Kozlov M.M., and McMahon H.T. How synaptotagmin promotes membrane fusion. Science 316 (2007) 1205-1208
65. Massarwa R., Carmon S., Shilo B.Z., and Schejter E.D. WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev. Cell 12 (2007) 557-569
66. Mi S., Lee X., Li X.-p., Veldman G.M., Finnerty H., Racie L., LaVallie E., Tang X.-Y., Edouard P., Howes S., et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403 (2000) 785-789
67. Mitreva, M., and Jasmer, D.P. (2006). Biology and genome of Trichinella spiralis. In WormBook, The C. elegans Research Community, ed. (WormBook). 10.1895/wormbook.1.124.1 http://www.wormbook.org.
68. Mohler W.A., Shemer G., del Campo J., Valansi C., Opoku-Serebuoh E., Scranton V., Assaf N., White J.G., and Podbilewicz B. The type I membrane protein EFF-1 is essential for developmental cell fusion in C. elegans. Dev. Cell 2 (2002) 355-362
69. Mothes W., Boerger A.L., Narayan S., Cunningham J.M., and Young J.A. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103 (2000) 679-689
70. Nakatogawa H., Ichimura Y., and Ohsumi Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130 (2007) 165-178
71. Oren-Suissa M., and Podbilewicz B. Cell fusion during development. Trends Cell Biol. 17 (2007) 537-546
72. Palovuori R., and Eskelinen S. Role of vinculin in the maintenance of cell-cell contacts in kidney epithelial MDBK cells. Eur. J. Cell Biol. 79 (2000) 961-974
73. Park H.E., Gruenke J.A., and White J.M. Leash in the groove mechanism of membrane fusion. Nat. Struct. Biol. 10 (2003) 1048-1053
74. Podbilewicz, B. (2006). Cell fusion. In WormBook, The C. elegans Research Community, ed. (WormBook). doi:10.1895/wormbook.1.52.1, http://www.wormbook.org.
75. Podbilewicz B., and White J.G. Cell fusions in the developing epithelia of C. elegans. Dev. Biol. 161 (1994) 408-424
76. Podbilewicz B., Leikina E., Sapir A., Valansi C., Suissa M., Shemer G., and Chernomordik L.V. The C. elegans developmental fusogen EFF-1 mediates homotypic fusion in heterologous cells and in vivo. Dev. Cell 11 (2006) 471-481
77. Renard M., Varela P.F., Letzelter C., Duquerroy S., Rey F.A., and Heidmann T. Crystal structure of a pivotal domain of human syncytin-2, a 40 million years old endogenous retrovirus fusogenic envelope gene captured by primates. J. Mol. Biol. 352 (2005) 1029-1034
78. Reporter M., and Raveed D. Plasma membranes: isolation from naturally fused and lysolecithin-treated muscle cells. Science 181 (1973) 863-865
79. Roche S., Bressanelli S., Rey F.A., and Gaudin Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313 (2006) 187-191
80. Roche S., Rey F.A., Gaudin Y., and Bressanelli S. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science 315 (2007) 843-848
81. Sapir A., Choi J., Leikina E., Avinoam O., Valansi C., Chernomordik L.V., Newman A.P., and Podbilewicz B. AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 12 (2007) 683-698
82. Shemer G., and Podbilewicz B. LIN-39/Hox triggers cell division and represses EFF-1/Fusogen-dependent vulval cell fusion. Genes Dev. 16 (2002) 3136-3141
83. Shemer G., and Podbilewicz B. The story of cell fusion: big lessons from little worms. Bioessays 25 (2003) 672-682
84. Shemer G., Suissa M., Kolotuev I., Nguyen K.C.Q., Hall D.H., and Podbilewicz B. EFF-1 is sufficient to initiate and execute tissue-specific cell fusion in C. elegans. Curr. Biol. 14 (2004) 1587-1591
85. Shmulevitz M., and Duncan R. A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses. EMBO J. 19 (2000) 902-912
86. Shmulevitz M., Corcoran J., Salsman J., and Duncan R. Cell-cell fusion induced by the avian reovirus membrane fusion protein is regulated by protein degradation. J. Virol. 78 (2004) 5996-6004
87. Simmons G., Gosalia D.N., Rennekamp A.J., Reeves J.D., Diamond S.L., and Bates P. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. USA 102 (2005) 11876-11881
88. Subramanian R.P., and Geraghty R.J. Herpes simplex virus type 1 mediates fusion through a hemifusion intermediate by sequential activity of glycoproteins D, H, L, and B. Proc. Natl. Acad. Sci. USA 104 (2007) 2903-2908
89. Tamm L.K. Hypothesis: spring-loaded boomerang mechanism of influenza hemagglutinin-mediated membrane fusion. Biochim. Biophys. Acta 1614 (2003) 14-23
90. Top D., de Antueno R., Salsman J., Corcoran J., Mader J., Hoskin D., Touhami A., Jericho M.H., and Duncan R. Liposome reconstitution of a minimal protein-mediated membrane fusion machine. EMBO J. 24 (2005) 2980-2988
91. Villesen P., Aagaard L., Wiuf C., and Pedersen F.S. Identification of endogenous retroviral reading frames in the human genome. Retrovirology 1 (2004) 32
92. Weissenhorn W., Dessen A., Harrison S.C., Skehel J.J., and Wiley D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387 (1997) 426-430
93. Weissenhorn W., Hinz A., and Gaudin Y. Virus membrane fusion. FEBS Lett. 581 (2007) 2150-2155
94. White J.M. Membrane fusion. Science 258 (1992) 917-924
95. White J.M. The first family of cell-cell fusion. Dev. Cell 12 (2007) 667-668
96. Xu Y., Zhang F., Su Z., McNew J.A., and Shin Y.K. Hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12 (2005) 417-422
97. Yang X., Kurteva S., Ren X., Lee S., and Sodroski J. Stoichiometry of envelope glycoprotein trimers in the entry of human immunodeficiency virus type 1. J. Virol. 79 (2005) 12132-12147
98. Zaitseva E., Mittal A., Griffin D.E., and Chernomordik L.V. Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J. Cell Biol. 169 (2005) 167-177
99. Zimmerberg J., Akimov S.A., and Frolov V. Synaptotagmin: fusogenic role for calcium sensor?. Nat. Struct. Mol. Biol. 13 (2006) 301-303