The Reovirus Fusion-Associated Small Transmembrane (FAST) Proteins: Virus-Encoded Cellular Fusogens

Current Topics in Membranes

Volumn 68, Issue , 2011, Pages 107-140

  Boutilier, Julie ^a   Duncan, Roy ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cell cell fusion; Fusion associated small transmembrane (FAST) proteins; Reovirus; Syncytium formation

Indexed keywords

VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELLS; CHEMISTRY; HUMAN; MEMBRANE FUSION; METABOLISM; MOLECULAR GENETICS; REOVIRUS; REVIEW; VIRUS ENTRY;

AMINO ACID SEQUENCE; ANIMALS; CELLS; HUMANS; MEMBRANE FUSION; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; REOVIRIDAE; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 79960417568     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-385891-7.00005-2     Document Type: Book

References (110)

1. Ahne W., Thomsen I., Winton J. Isolation of a reovirus from the snake, Python regius. Brief report. Archives of Virology 1987, 94:135-139.
2. Barry C., Duncan R. Multifaceted sequence-dependent and -independent roles for reovirus FAST protein cytoplasmic tails in fusion pore formation and syncytiogenesis. Journal of Virology 2009, 83:12185-12195.
3. Barry C., Key T., Haddad R., Duncan R. Features of a spatially constrained cystine loop in the p10 FAST protein ectodomain define a new class of viral fusion peptides. Journal of Biological Chemistry 2010, 285:16424-16433.
4. Benavente J., Martinez-Costas J. Avian reovirus: Structure and biology. Virus Research 2007, 123:105-119.
5. Bigay J., Casella J.F., Drin G., Mesmin B., Antonny B. ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO Journal 2005, 24:2244-2253.
6. Brown C.W., Stephenson K.B., Hanson S., Kucharczyk M., Duncan R., Bell J.C., et al. The p14 FAST protein of reptilian reovirus increases vesicular stomatitis virus neuropathogenesis. Journal of Virology 2009, 83:552-561.
7. Brown M.S., Ye J., Rawson R.B., Goldstein J.L. Regulated intramembrane proteolysis: A control mechanism conserved from bacteria to humans. Cell 2000, 100:391-398.
8. Campelo F., McMahon H.T., Kozlov M.M. The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophysical J. 2008, 95:2325-2339.
9. Cathomen T., Mrkic B., Spehner D., Drillien R., Naef R., Pavlovic J., et al. A matrix-less measles virus is infectious and elicits extensive cell fusion: Consequences for propagation in the brain. EMBO Journal 1998, 17:3899-3908.
10. Chen A., Leikina E., Melikov K., Podbilewicz B., Kozlov M.M., Chernomordik L.V. Fusion-pore expansion during syncytium formation is restricted by an actin network. Journal of Cell Science 2008, 121:3619-3628.
11. Cheng L.T., Plemper R.K., Compans R.W. Atypical fusion peptide of Nelson Bay virus fusion-associated small transmembrane protein. Journal of Virology 2005, 79:1853-1860.
12. Chernomordik L., Leikina E., Cho M.S., Zimmerberg J. Control of baculovirus gp64-induced syncytium formation by membrane lipid composition. Journal of Virology 1995, 69:3049-3058.
13. 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. The Journal of Cell Biology 1998, 140:1369-1382.
14. Chernomordik L.V., Kozlov M.M. Protein-lipid interplay in fusion and fission of biological membranes. Annual Review of Biochemistry 2003, 72:175-207.
15. Chernomordik L.V., Kozlov M.M. Membrane hemifusion: Crossing a chasm in two leaps. Cell 2005, 123:375-382.
16. Chernomordik L.V., Kozlov M.M. Mechanics of membrane fusion. Nature Structural & Molecular Biology 2008, 15:675-683.
17. Chernomordik L.V., Zimmerberg J., Kozlov M.M. Membranes of the world unite!. The Journal of Cell Biology 2006, 175:201-207.
18. Chua K.B., Crameri G., Hyatt A., Yu M., Tompang M.R., Rosli J., et al. A previously unknown reovirus of bat origin is associated with an acute respiratory disease in humans. Proceedings of the National Academy of Sciences United States of America 2007, 104:11424-11429.
19. Chua K.B., Voon K., Crameri G., Tan H.S., Rosli J., McEachern J.A., et al. Identification and characterization of a new orthoreovirus from patients with acute respiratory infections. PLoS One 2008, 3:e3803.
20. Clancy E.K., Barry C., Ciechonska M., Duncan R. Different activities of the reovirus FAST proteins and influenza hemagglutinin in cell-cell fusion assays and in response to membrane curvature agents. Virology 2010, 397:119-129.
21. Clancy E.K., Duncan R. Reovirus FAST protein transmembrane domains function in a modular, primary sequence-independent manner to mediate cell-cell membrane fusion. Journal of Virology 2009, 83:2941-2950.
22. Clancy E.K., Duncan R. Helix-destabilizing, β-branched and polar residues in the baboon reovirus p15 transmembrane domain influence the modularity of the FAST proteins. Journal of Virology 2011, 85:4707-4719.
23. Cohen F.S., Melikyan G.B. The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. Journal of Membrane Biology 2004, 199:1-14.
24. Corcoran J.A, Clancy E.K., Duncan R. Homomultimerization of the reovirus p14 fusion-associated small transmembrane protein during transit through the ER-Golgi complex secretory pathway. Journal of General Virology 2011, 92:162-166.
25. Corcoran J.A., Duncan R. Reptilian reovirus utilizes a small type III protein with an external myristylated amino terminus to mediate cell-cell fusion. Journal of Virology 2004, 78:4342-4351.
26. Corcoran J.A., Salsman J., de Antueno R., Touhami A., Jericho M.H., Clancy E.K., et al. The p14 fusion-associated small transmembrane (FAST) protein effects membrane fusion from a subset of membrane microdomains. The Journal of Biological Chemistry 2006, 281:31778-31789.
27. Corcoran J.A., Syvitski R., Top D., Epand R.M., Epand R.F., Jakeman D., et al. Myristoylation, a protruding loop, and structural plasticity are essential features of a nonenveloped virus fusion peptide motif. The Journal of Biological Chemistry 2004, 279:51386-51394.
28. Cortese M.S., Uversky V.N., Dunker A.K. Intrinsic disorder in scaffold proteins: Getting more from less. Progress in Biophysics and Molecular Biology 2008, 98:85-106.
29. Danieli T., Pelletier S.L., Henis Y.I., White J.M. Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. The Journal of Cell Biology 1996, 133:559-569.
30. Dawe S., Corcoran J.A., Clancy E.K., Salsman J., Duncan R. Unusual topological arrangement of structural motifs in the baboon reovirus fusion-associated small transmembrane protein. Journal of Virology 2005, 79:6216-6226.
31. Dawe S., Duncan R. The S4 genome segment of baboon reovirus is bicistronic and encodes a novel fusion-associated small transmembrane protein. Journal of Virology 2002, 76:2131-2140.
32. Drin G., Antonny B. Amphipathic helices and membrane curvature. FEBS Letters 2010, 584:1840-1847.
33. Duncan R. Extensive sequence divergence and phylogenetic relationships between the fusogenic and nonfusogenic orthoreoviruses: A species proposal. Virology 1999, 260:316-328.
34. Duncan R., Chen Z., Walsh S., Wu.S. Avian reovirus-induced syncytium formation is independent of infectious progeny virus production and enhances the rate, but is not essential, for virus-induced cytopathology and virus egress. Virology 1996, 224:453-464.
35. Duncan R., Corcoran J., Shou J., Stoltz D. Reptilian reovirus: A new fusogenic orthoreovirus species. Virology 2004, 319:131-140.
36. Duncan R., Murphy F.A., Mirkovic R.R. Characterization of a novel syncytium-inducing baboon reovirus. Virology 1995, 212:752-756.
37. Duncan R., Sullivan K. Characterization of two avian reoviruses that exhibit strain-specific quantitative differences in their syncytium-inducing and pathogenic capabilities. Virology 1998, 250:263-272.
38. Eitzen G. Actin remodeling to facilitate membrane fusion. Biochimica et Biophysica Acta 2003, 1641:175-181.
39. Gard G., Compans R.W. Structure and cytopathic effects of Nelson Bay virus. Journal of Virology 1970, 6:100-106.
40. Gibbons D.L., Vaney M.C., Roussel A., Vigouroux A., Reilly B., Lepault J., et al. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 2004, 427:320-325.
41. Harrison S.C. Viral membrane fusion. Nature Structural & Molecular Biology 2008, 15:690-698.
42. Helming L., Gordon S. Molecular mediators of macrophage fusion. Trends in Cell Biology 2009, 19:514-522.
43. Jahn R., Grubmuller H. Membrane fusion. Current Opinion in Cell Biology 2002, 14:488-495.
44. Jahn R., Scheller R.H. SNAREs-Engines for membrane fusion. Nature Reviews Molecular Cell Biology 2006, 7:631-643.
45. Kibenge F.S., Dhillon A.S. A comparison of the pathogenicity of four avian reoviruses in chickens. Avian Diseases 1987, 31:39-42.
46. Kielian M., Rey F.A. Virus membrane-fusion proteins: More than one way to make a hairpin. Nature Reviews Microbiology 2006, 4:67-76.
47. Koch A.W., Manzur K.L., Shan W. Structure-based models of cadherin-mediated cell adhesion: The evolution continues. Cellular and Molecular Life Sciences 2004, 61:1884-1895.
48. Kozlov M.M., McMahon H.T., Chernomordik L.V. Protein-driven membrane stresses in fusion and fission. Trends in Biochemical Sciences 2010, 35:699-706.
49. Lamb R.A., Jardetzky T.S. Structural basis of viral invasion: Lessons from paramyxovirus F. Current Opinion in Structural Biology 2007, 17:427-436.
50. Lamirande E.W., Nichols D.K., Owens J.W., Gaskin J.M., Jacobson E.R. Isolation and experimental transmission of a reovirus pathogenic in ratsnakes (Elaphe species). Virus Research 1999, 63:135-141.
51. Langosch D., Hofmann M., Ungermann C. The role of transmembrane domains in membrane fusion. Cellular and Molecular Life Sciences 2007, 64:850-864.
52. Lapthorn A.J., Janes R.W., Isaacs N.W., Wallace B.A. Cystine nooses and protein specificity. Nature Structural Biology 1995, 2:266-268.
53. Leland M.M., Hubbard G.B., Sentmore H.T., Soike K.F., Hilliard J.K. Outbreak of Orthoreovirus-induced meningoencephalomyelitis in baboons. Comparative Medicine 2000, 50:199-205.
54. Liu J., Sun Y., Oster G.F., Drubin D.G. Mechanochemical crosstalk during endocytic vesicle formation. Current Opinion in Cell Biology 2010, 22:36-43.
55. Markosyan R.M., Melikyan G.B., Cohen F.S. Evolution of intermediates of influenza virus hemagglutinin-mediated fusion revealed by kinetic measurements of pore formation. Biophysical J. 2001, 80:812-821.
56. Martens S., Kozlov M.M., McMahon H.T. How synaptotagmin promotes membrane fusion. Science 2007, 316:1205-1208.
57. Martens S., McMahon H.T. Mechanisms of membrane fusion: Disparate players and common principles. Nature Reviews Molecular Cell Biology 2008, 9:543-556.
58. McMahon H.T., Kozlov M.M., Martens S. Membrane curvature in synaptic vesicle fusion and beyond. Cell 2010, 140:601-605.
59. Melikyan G.B. Common principles and intermediates of viral protein-mediated fusion: The HIV-1 paradigm. Retrovirology 2008, 5:111.
60. Melikyan G.B., Brener S.A., Ok D.C., Cohen F.S. Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion. The Journal of Cell Biology 1997, 136:995-1005.
61. Melikyan G.B., White J.M., Cohen F.S. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. The Journal of Cell Biology 1995, 131:679-691.
62. Mertens P.P.C., Attoui H., Duncan R., Dermody T.S. Reoviridae 2005, Elsevier/Academic Press, London, 447-454.
63. Mittal A., Leikina E., Chernomordik L.V., Bentz J. Kinetically differentiating influenza hemagglutinin fusion and hemifusion machines. Biophysical J. 2003, 85:1713-1724.
64. Modis Y., Ogata S., Clements D., Harrison S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427:313-319.
65. Mohd Jaafar F., Goodwin A.E., Belhouchet M., Merry G., Fang Q., Cantaloube J.F., et al. Complete characterisation of the American grass carp reovirus genome (genus Aquareovirus: family Reoviridae) reveals an evolutionary link between aquareoviruses and coltiviruses. Virology 2008, 373:310-321.
66. Mohler W.A., Simske J.S., Williams-Masson E.M., Hardin J.D., White J.G. Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis. Current Biology 1998, 8:1087-1090.
67. Munro S. Lipid rafts: Elusive or illusive?. Cell 2003, 115:377-388.
68. Nolan S., Cowan A.E., Koppel D.E., Jin H., Grote E. FUS1 regulates the opening and expansion of fusion pores between mating yeast. Molecular Biology of the Cell 2006, 17:2439-2450.
69. Oren-Suissa M., Podbilewicz B. Evolution of programmed cell fusion: Common mechanisms and distinct functions. Developmental Dynamics 2010, 239:1515-1528.
70. Palacios G., Lovoll M., Tengs T., Hornig M., Hutchison S., Hui J., et al. Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS One 2010, 5:e11487.
71. Paterson R.G., Russell C.J., Lamb R.A. Fusion protein of the paramyxovirus SV5: Destabilizing and stabilizing mutants of fusion activation. Virology 2000, 270:17-30.
72. Perez-Moreno M., Jamora C., Fuchs E. Sticky business: Orchestrating cellular signals at adherens junctions. Cell 2003, 112:535-548.
73. Popovic M., De Biasio A., Pintar A., Pongor S. The intracellular region of the Notch ligand Jagged-1 gains partial structure upon binding to synthetic membranes. FEBS Journal 2007, 274:5325-5336.
74. Poschner B.C., Fischer K., Herrmann J.R., Hofmann M.W., Langosch D. Structural features of fusogenic model transmembrane domains that differentially regulate inner and outer leaflet mixing in membrane fusion. Molecular Membrane Biology 2010, 27:1-10.
75. Poschner B.C., Langosch D. Stabilization of conformationally dynamic helices by covalently attached acyl chains. Protein Science 2009, 18:1801-1805.
76. Poschner B.C., Quint S., Hofmann M.W., Langosch D. Sequence-specific conformational dynamics of model transmembrane domains determines their membrane fusogenic function. Journal of Molecular Biology 2009, 386:733-741.
77. Pritchard L.I., Chua K.B., Cummins D., Hyatt A., Crameri G., Eaton B.T., et al. Pulau virus: A new member of the Nelson Bay orthoreovirus species isolated from fruit bats in Malaysia. Archives of Virology 2006, 151:229-239.
78. Racine T., Hurst T., Barry C., Shou J., Kibenge F., Duncan R. Aquareovirus effects syncytiogenesis by using a novel member of the FAST protein family translated from a noncanonical translation start site. Journal of Virology 2009, 83:5951-5955.
79. Reese C., Mayer A. Transition from hemifusion to pore opening is rate limiting for vacuole membrane fusion. The Journal of Cell Biology 2005, 171:981-990.
80. Reiersen H., Rees A.R. The hunchback and its neighbours: Proline as an environmental modulator. Trends in Biochemical Sciences 2001, 26:679-684.
81. Rey F.A. Molecular gymnastics at the herpesvirus surface. EMBO Reports 2006, 7:1000-1005.
82. Richardson B.E., Nowak S.J., Baylies M.K. Myoblast fusion in fly and vertebrates: New genes, new processes and new perspectives. Traffic 2008, 9:1050-1059.
83. Roche S., Albertini A.A., Lepault J., Bressanelli S., Gaudin Y. Structures of vesicular stomatitis virus glycoprotein: Membrane fusion revisited. Cellular and Molecular Life Sciences 2008, 65:1716-1728.
84. Roche S., Bressanelli S., Rey F.A., Gaudin Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 2006, 313:187-191.
85. Russell C.J., Jardetzky T.S., Lamb R.A. Conserved glycine residues in the fusion peptide of the paramyxovirus fusion protein regulate activation of the native state. Journal of Virology 2004, 78:13727-13742.
86. Salsman J., Top D., Barry C., Duncan R. A virus-encoded cell-cell fusion machine dependent on surrogate adhesins. PLoS Pathogens 2008, 4:e1000016.
87. Salsman J., Top D., Boutilier J., Duncan R. Extensive syncytium formation mediated by the reovirus FAST proteins triggers apoptosis-induced membrane instability. Journal of Virology 2005, 79:8090-8100.
88. Sapir A., Avinoam O., Podbilewicz B., Chernomordik L.V. Viral and developmental cell fusion mechanisms: Conservation and divergence. Developmental Cell 2008, 14:11-21.
89. Shmulevitz M., Duncan R. A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses. EMBO Journal 2000, 19:902-912.
90. Shmulevitz M., Epand R.F., Epand R.M., Duncan R. Structural and functional properties of an unusual internal fusion peptide in a nonenveloped virus membrane fusion protein. Journal of Virology 2004, 78:2808-2818.
91. Shmulevitz M., Salsman J., Duncan R. Palmitoylation, membrane-proximal basic residues, and transmembrane glycine residues in the reovirus p10 protein are essential for syncytium formation. Journal of Virology 2003, 77:9769-9779.
92. Shmulevitz M, Yameen Z., Dawe S., Shou J., O'Hara D., et al. Sequential partially overlapping gene arrangement in the tricistronic S1 genome segments of avian reovirus and Nelson Bay reovirus: Implications for translation initiation. Journal of Virology 2002, 76:609-618.
93. Spiess M. Heads or tails-What determines the orientation of proteins in the membrane. FEBS Letters 1995, 369:76-79.
94. Stapley B.J., Creamer T.P. A survey of left-handed polyproline II helices. Protein Sciences 1999, 8:587-595.
95. Steain M.C., Wang B., Saksena N.K. The possible contribution of HIV-1-induced syncytia to the generation of intersubtype recombinants in vitro. Aids 2008, 22:1009-1017.
96. Stein A., Weber G., Wahl M.C., Jahn R. Helical extension of the neuronal SNARE complex into the membrane. Nature 2009, 460:525-528.
97. Tamm L.K. Hypothesis: Spring-loaded boomerang mechanism of influenza hemagglutinin-mediated membrane fusion. Biochimica et Biophysica Acta 2003, 1614:14-23.
98. Tamm L.K., Crane J., Kiessling V. Membrane fusion: A structural perspective on the interplay of lipids and proteins. Current Opinion in Structural Biology 2003, 13:453-466.
99. Tamm L.K., Han X. Viral fusion peptides: A tool set to disrupt and connect biological membranes. Bioscience Reports 2000, 20:501-518.
100. Tamm L.K., Han X., Li Y., Lai A.L. Structure and function of membrane fusion peptides. Biopolymers 2002, 66:249-260.
101. Thalmann C.M., Cummins D.M., Yu M., Lunt R., Pritchard L.I., Hansson E., et al. Broome virus, a new fusogenic Orthoreovirus species isolated from an Australian fruit bat. Virology 2010, 402:26-40.
102. Top D., Barry C., Racine T., Ellis C.L., Duncan R. Enhanced fusion pore expansion mediated by the trans-acting endodomain of the reovirus FAST proteins. PLoS Pathogens 2009, 5:e1000331.
103. Top D., de Antueno R., Salsman J., Corcoran J., Mader J., Hoskin D., et al. Liposome reconstitution of a minimal protein-mediated membrane fusion machine. EMBO Journal 2005, 24:2980-2988.
104. Vieler E., Baumgartner W., Herbst W., Kohler G. Characterization of a reovirus isolate from a rattle snake, Crotalus viridis, with neurological dysfunction. Archives of Virology 1994, 138:341-344.
105. Weber T., Zemelman B.V., McNew J.A., Westermann B., Gmachl M., Parlati F., et al. SNAREpins: Minimal machinery for membrane fusion. Cel 1998, 92:759-772.
106. White J.M., Delos S.E., Brecher M., Schornberg K. Structures and mechanisms of viral membrane fusion proteins: Multiple variations on a common theme. Critical Reviews in Biochemistry and Molecular Biology 2008, 43:189-219.
107. White S.H., Ladokhin A.S., Jayasinghe S., Hristova K. How membranes shape protein structure. The Journal of Biological Chemistry 2001, 276:32395-32398.
108. Wurth M.A., Schowalter R.M., Smith E.C., Moncman C.L., Dutch R.E., McCann.F R.O. The actin cytoskeleton inhibits pore expansion during PIV5 fusion protein-promoted cell-cell fusion. Virology 2010, 404:117-126.
109. 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. The Journal of Cell Biology 2005, 169:167-177.
110. Zhu B., Chappuis-Flament S., Wong E., Jensen I.E., Gumbiner B.M., Leckband D. Functional analysis of the structural basis of homophilic cadherin adhesion. Biophysical J. 2003, 84:4033-4042.