Mutations that promote furin-independent growth of Semliki Forest virus affect p62-E1 interactions and membrane fusion

Virology

Volumn 327, Issue 2, 2004, Pages 287-296

  Zhang, Xinyong ^a   Kielian, Margaret ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Alphavirus; Endocytosis; Furin; Membrane fusion; Protein processing; Semliki Forest virus; Virus entry

Indexed keywords

FURIN; GLYCOPROTEIN E1; PROTEIN; PROTEIN P62; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; MEMBRANE FUSION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SEMLIKI FOREST ALPHAVIRUS; SEQUENCE ANALYSIS; VIROGENESIS; VIRUS ISOLATION; VIRUS MUTANT;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CRICETINAE; DIMERIZATION; FURIN; GENE EXPRESSION REGULATION, VIRAL; MEMBRANE FUSION; MUTATION; PROTEIN PRECURSORS; SEMLIKI FOREST VIRUS; VIRAL ENVELOPE PROTEINS;

ALPHAVIRUS; RABBIT FIBROMA VIRUS; SEMLIKI FOREST VIRUS;

EID: 4444338218     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.06.037     Document Type: Article

References (54)

1. A. Ahn, M.R. Klimjack, P.K. Chatterjee, and M. Kielian An epitope of the Semliki Forest virus fusion protein exposed during virus-membrane fusion J. Virol. 73 1999 10029 10039
2. H. Andersson, B.U. Barth, M. Ekström, and H. Garoff Oligomerization-dependent folding of the membrane fusion protein of Semliki Forest virus J. Virol. 71 1997 9654 9663
3. R. Blumenthal, M.J. Clague, S.R. Durell, and R.M. Epand Membrane fusion Chem. Rev. 103 2003 53 69
4. M. Carleton, H. Lee, M. Mulvey, and D.T. Brown Role of glycoprotein PE2 in formation and maturation of the Sindbis virus spike J. Virol. 71 1997 1558 1566
5. R.H. Cheng, R.J. Kuhn, N.H. Olson, M.G. Rossman, H.-K. Choi, T.J. Smith, and T.S. Baker Nucleocapsid and glycoprotein organization in an enveloped virus Cell 80 1995 621 630
6. N.L. Davis, K.W. Brown, G.F. Greenwald, A.J. Zajac, V.L. Zacny, J.F. Smith, and R.E. Johnston Attenuated mutants of venezuelan equine encephalitis virus containing lethal mutations in the PE2 cleavage signal combined with a second-site suppressor mutation in E1 Virology 212 1995 102 110
7. L. DeTulleo, and T. Kirchhausen The clathrin endocytic pathway in viral infection EMBO J. 17 1998 4585 4593
8. W.A. Duffus, P. Levy-Mintz, M.R. Klimjack, and M. Kielian Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly J. Virol. 69 1995 2471 2479
9. D.M. Eckert, and P.S. Kim Mechanisms of viral membrane fusion and its inhibition Annu. Rev. Biochem. 70 2001 777 810
10. M. Ekstrom, P. Liljeström, and H. Garoff Membrane protein lateral interactions control Semliki Forest virus budding EMBO J. 13 1994 1058 1064
11. I. Ferlenghi, B. Gowen, F.D. Haas, E.J. Mancini, H. Garoff, M. Sjoberg, and S.D. Fuller The first step: maturation of the Semliki Forest virus spike occurs through a dramatic localized conformational change J. Mol. Biol. 283 1998 71 81
12. S.D. Fuller, J.A. Berriman, S.J. Butcher, and B.E. Gowen Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex Cell 81 1995 715 725
13. D.L. Gibbons, A. Ahn, P.K. Chatterjee, and M. Kielian Formation and characterization of the trimeric form of the fusion protein of Semliki Forest virus J. Virol. 74 2000 7772 7780
14. D.L. Gibbons, I. Erk, B. Reilly, J. Navaza, M. Kielian, F.A. Rey, and J. Lepault Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography Cell 114 2003 573 583
15. D.L. Gibbons, A. Ahn, M. Liao, L. Hammar, R.H. Cheng, and M. Kielian Multistep regulation of membrane insertion of the fusion peptide of Semliki Forest virus J. Virol. 78 2004 3312 3318
16. D.L. Gibbons, M.-C. Vaney, A. Roussel, A. Vigouroux, B. Reilly, J. Lepault, M. Kielian, and F.A. Rey Conformational change and protein†"protein interactions of the fusion protein of Semliki Forest virus Nature 427 2004 320 325
17. S. Glomb-Reinmund, and M. Kielian fus-1, a pH-shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit J. Virol. 72 1998 4281 4287
18. V.M. Gordon, K.R. Klimpel, N. Arora, M.A. Henderson, and S.H. Leppla Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases Infect. Immun. 63 1995 82 87
19. H.W. Heidner, K.L. McKnight, N.L. Davis, and R.E. Johnston Lethality of PE2 incorporation into Sindbis virus can be suppressed by second-site mutations in E3 and E2 J. Virol. 68 1994 2683 2692
20. A. Helenius, J. Kartenbeck, K. Simons, and E. Fries On the entry of Semliki Forest virus into BHK-21 cells J. Cell Biol. 84 1980 404 420
21. L.D. Hernandez, L.R. Hoffman, T.G. Wolfsberg, and J.M. White Virusâ€"cell and cellâ€"cell fusion Annu. Rev. Cell Dev. Biol. 12 1996 627 661
22. S.K. Jain, S. DeCandido, and M. Kielian Processing of the p62 envelope precursor protein of Semliki Forest virus J. Biol. Chem. 266 1991 5756 5761
23. J. Justman, M.R. Klimjack, and M. Kielian Role of spike protein conformational changes in fusion of Semliki Forest virus J. Virol. 67 1993 7597 7607
24. M. Kielian Membrane fusion and the alphavirus life cycle Adv. Virus Res. 45 1995 113 151
25. M.C. Kielian, S. Keränen, L. Kääriäinen, and A. Helenius Membrane fusion mutants of Semliki Forest virus J. Cell Biol. 98 1984 139 145
26. M. Kielian, S. Jungerwirth, K.U. Sayad, and S. DeCandido Biosynthesis, maturation, and acid-activation of the Semliki Forest virus fusion protein J. Virol. 64 1990 4614 4624
27. M. Kielian, M.R. Klimjack, S. Ghosh, and W.A. Duffus Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus J. Cell Biol. 134 1996 863 872
28. M. Kielian, P.K. Chatterjee, D.L. Gibbons, and Y.E. Lu Specific roles for lipids in virus fusion and exit: examples from the alphaviruses H. Hilderson S. Fuller Subcellular Biochemistry Fusion of Biological Membranes and Related Problems vol. 34 2000 Plenum Publishers New York 409 455
29. M.R. Klimjack, S. Jeffrey, and M. Kielian Membrane and protein interactions of a soluble form of the Semliki Forest virus fusion protein J. Virol. 68 1994 6940 6946
30. W.B. Klimstra, H.W. Heidner, and R.E. Johnston The furin protease cleavage recognition sequence of Sindbis virus PE2 can mediate virion attachment to cell surface heparan sulfate J. Virol. 73 1999 6299 6306
31. J. Lescar, A. Roussel, M.W. Wien, J. Navaza, S.D. Fuller, G. Wengler, and F.A. Rey The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH Cell 105 2001 137 148
32. M. Lobigs, and H. Garoff Fusion function of the Semliki Forest virus spike is activated by proteolytic cleavage of the envelope glycoprotein precursor p62 J. Virol. 64 1990 1233 1240
33. Y.E. Lu, C.H. Eng, S.G. Shome, and M. Kielian In vivo generation and characterization of a soluble form of the Semliki forest virus fusion protein J. Virol. 75 2001 8329 8339
34. E.J. Mancini, M. Clarke, B.E. Gowen, T. Rutten, and S.D. Fuller Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki forest virus Mol. Cell 5 2000 255 266
35. M. Marsh, and A. Helenius Adsorptive endocytosis of Semliki Forest virus J. Mol. Biol. 142 1980 439 454
36. M. Molinari, and A. Helenius Chaperone selection during glycoprotein translocation into the endoplasmic reticulum Science 288 2000 331 333
37. J.-H. Ou, E.G. Strauss, and J.H. Strauss Comparative studies of the 3′-terminal sequences of several alphavirus RNAs Virology 109 1981 281 289
38. S.V. Pletnev, W. Zhang, S. Mukhopadhyay, B.R. Fisher, R. Hernandez, D.T. Brown, T.S. Baker, M.G. Rossmann, and R.J. Kuhn Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold Cell 105 2001 127 136
39. D.L. Russell, J.M. Dalrymple, and R.E. Johnston Sindbis virus mutations which coordinately affect glycoprotein processing, penetration, and virulence in mice J. Virol. 63 1989 16l9 1629
40. A. Salminen, J.M. Wahlberg, M. Lobigs, P. Liljeström, and H. Garoff Membrane fusion process of Semliki Forest virus II: cleavage-dependent reorganization of the spike protein complex controls virus entry J. Cell Biol. 116 1992 349 357
41. S. Schlesinger, and M.J. Schlesinger Togaviridae: the viruses and their replication D.M. Knipe P.M. Howley Fields Virology 2001 Lippincott, Williams and Wilkins Philadelphia 895 916
42. S.B. Sieczkarski, and G.R. Whittaker Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis J. Virol. 76 2002 10455 10464
43. M. Sjoberg, and H. Garoff Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion J. Virol. 77 2003 3441 3450
44. J.M. Smit, W.B. Klimstra, K.D. Ryman, R. Bittman, R.E. Johnston, and J. Wilschut PE2 cleavage mutants of Sindbis virus: correlation between viral infectivity and pH-dependent membrane fusion activation of the spike heterodimer J. Virol. 75 2001 11196 11204
45. J.H. Strauss, and E.G. Strauss The alphaviruses: gene expression, replication, and evolution Microbiol. Rev. 58 1994 491 562
46. I. Tubulekas, and P. Liljeström Suppressors of cleavage-site mutations in the p62 envelope protein of Semliki Forest virus reveal dynamics in spike structure and function J. Virol. 72 1998 2825 2831
47. M. Vashishtha, T. Phalen, M.T. Marquardt, J.S. Ryu, A.C. Ng, and M. Kielian A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit J. Cell Biol. 140 1998 91 99
48. J.M. Wahlberg, and H. Garoff Membrane fusion process of Semliki Forest virus I: low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells J. Cell Biol. 116 1992 339 348
49. J.M. Wahlberg, W.A.M. Boere, and H. Garoff The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation J. Virol. 63 1989 4991 4997
50. J.M. Wahlberg, R. Bron, J. Wilschut, and H. Garoff Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein J. Virol. 66 1992 7309 7318
51. J.S. Yao, E.G. Strauss, and J.H. Strauss Interactions between PE2, E1, and 6K required for assembly of alphaviruses studied with chimeric viruses J. Virol. 70 1996 7910 7920
52. W. Zhang, S. Mukhopadhyay, S.V. Pletnev, T.S. Baker, R.J. Kuhn, and M.G. Rossmann Placement of the structural proteins in Sindbis virus J. Virol. 76 2002 11645 11658
53. X. Zhang, M. Fugere, R. Day, and M. Kielian Furin processing and proteolytic activation of Semliki Forest virus J. Virol. 77 2003 2981 2989
54. H. Zhao, and H. Garoff Role of cell surface spikes in alphavirus budding J. Virol. 66 1992 7089 7095