Thiol/disulfide exchange is required for membrane fusion directed by the Newcastle disease virus fusion protein

Journal of Virology

Volumn 81, Issue 5, 2007, Pages 2328-2339

  Jain, Surbhi ^a   McGinnes, Lori W ^a   Morrison, Trudy G ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); BACITRACIN; DISULFIDE; GLYCOPROTEIN; PROTEIN DISULFIDE ISOMERASE; SIALIC ACID; SIALIDASE; THIOL; VIRUS FUSION PROTEIN;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL MEMBRANE; CELL VIABILITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; MEMBRANE FUSION; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; PARAMYXOVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RNA VIRUS INFECTION; VIRUS CELL INTERACTION; VIRUS ENVELOPE;

ANIMALS; BACITRACIN; CERCOPITHECUS AETHIOPS; COS CELLS; DISULFIDES; DITHIONITROBENZOIC ACID; ENZYME INHIBITORS; HN PROTEIN; MEMBRANE FUSION; MODELS, BIOLOGICAL; NEWCASTLE DISEASE VIRUS; PROTEIN DISULFIDE-ISOMERASE; RECOMBINANT PROTEINS; SULFHYDRYL COMPOUNDS; VIRAL FUSION PROTEINS; VIRUS ATTACHMENT;

AVES; NEWCASTLE DISEASE VIRUS; PARAMYXOVIRIDAE;

EID: 33847222149     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01940-06     Document Type: Article

References (77)

1. Abdel-Latif, L., B. K. Murray, R. L. Renberg, K. L. O'Neill, H. Porter, J. B. Jensen, and F. B. Johnson. 2006. Cell death in bovine parvovirus-infected embryonic bovine tracheal cells is mediated by necrosis rather than apoptosis. J. Gen. Virol. 87:2539-2548.
2. Abell, B. A., and D. T. Brown. 1993. Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface. J. Virol. 67:5496-5501.
3. Baker, K. A., R. E. Dutch, R. A. Lamb, and T. S. Jardetzky. 1999. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3:309-319.
4. Barbouche, R., R. Miquelis, I. M. Jones, and E. Fenouillet. 2003. Protein-disulfide isomerase-mediated reduction of two disulfide bonds of HIV envelope glycoprotein 120 occurs post-CXCR4 binding and is required for fusion. J. Biol. Chem. 278:3131-3136.
5. Bousse, T., T. Takimoto, K. G. Murti, and A. Portner. 1997. Elevated expression of the human parainfluenza virus type 1 F gene downregulates HN expression. Virology 252:44-52.
6. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43.
7. Chen, L., J. J. Gorman, J. McKimm-Breschkin, L. J. Lawrence, P. A. Tulloch, B. J. Smith, P. M. Colman, and M. C. Lawrence. 2001. The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure 9:255-266.
8. Cleverley, D. Z., and J. Lenard. 1998. 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.
9. Colman, P. M., and M. C. Lawrence. 2003. The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell. Biol. 4:309-319.
10. Dolganiuc, V., L. McGinnes, E. J. Luna, and T. G. Morrison. 2003. Role of the cytoplasmic domain of the Newcastle disease virus fusion protein in association with lipid rafts. J. Virol. 77:12968-12979.
11. Earl, P. L., C. C. Broder, D. Long, S. A. Lee, J. Peterson, S. Chakrabarti, R. W. Doms, and B. Moss. 1994. Native oligomeric human immunodeficiency virus type 1 envelope glycoprotein elicits diverse monoclonal antibody reactivities. J. Virol. 68:3015-3026.
12. Earp, L. J., S. E. Deios, H. E. Park, and J. M. White. 2005. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285:25-66.
13. Edwards, J., E. Mann, and D. T. Brown. 1983. Conformational changes in Sindbis virus envelope proteins accompanying exposure to low pH. J. Virol. 45:1090-1097.
14. Ellgaard, L., and L. W. Ruddock. 2005. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6:28-32.
15. Feener, E. P., W. C. Shen, and H. J. Ryser. 1990. Cleavage of disulfide bonds in endocytosed macromolecules. A processing not associated with lysosomes or endosomes. J. Biol. Chem. 265:18780-18785.
16. Fenouillet, E., R. Barbouche, J. Courageot, and R. Miquelis. 2001. The catalytic activity of protein disulfide isomerase is involved in human immunodeficiency virus envelope-mediated membrane fusion after CD4 cell binding. J. Infect. Dis. 183:744-752.
17. Ferrari, D. M., and H. D. Soling. 1999. The protein disulphide-isomerase family: unravelling a string of folds. Biochem. J. 339:1-10.
18. Finnegan, C. M., W. Berg, G. K. Lewis, and A. L. DeVico. 2002. Antigenic properties of the human immunodeficiency virus transmembrane glycoprotein during cell-cell fusion. J. Virol. 76:12123-12134.
19. Gallina, A., T. M. Hanley, R. Mandel, M. Trahey, C. C. Broder, G. A. Viglianti, and H. J. Ryser. 2002. Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J. Biol. Chem. 277:50579-50588.
20. Gilbert, H. F. 1997. Protein disulfide isomerase and assisted protein folding. J. Biol. Chem. 272:29399-29402.
21. Gilbert, J., W. Ou, J. Silver, and T. Benjamin. 2006. Downregulation of protein disulfide isomerase inhibits infection by the mouse polyomavirus. J. Virol. 80:10868-10870.
22. Heinz, F. X., and S. L. Allison. 2001. The machinery for flavivirus fusion with host cell membranes. Curr. Opin. Microbiol. 4:450-455.
23. Hernandez, L. D., L. R. Hoffman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-661.
24. Hernandez, L. D., R. J. Peters, S. E. Delos, J. A. Young, D. A. Agard, and J. M. White. 1997. Activation of a retroviral membrane fusion protein: soluble receptor-induced liposome binding of the ALSV envelope glycoprotein. J. Cell Biol. 139:1455-1464.
25. Hogg, P. J. 2003. Disulfide bonds as switches for protein function. Trends Biochera. Sci. 28:210-214.
26. Jardetzky, T. S., and R. A. Lamb. 2004. Virology: a class act. Nature 427:307-308.
27. Jordan, P. A., and J. M. Gibbins. 2006. Extracellular disulfide exchange and the regulation of cellular function. Antioxid. Redox. Signal 8:312-324.
28. Joshi, S. B., R. E. Dutch, and R. A. Lamb. 1998. A core trimer of the paramyxovirus fusion protein: parallels to influenza virus hemagglutinin and HIV-1 gp41. Virology 248:20-34.
29. Kemble, G. W., Y. I. Henis, and J. M. White. 1993. GPI- and transraembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity. J. Cell Biol. 122:1253-1265.
30. Kielian, M., and A. Helenius. 1985. pH-induced alterations in the fusogenic spike protein of Semliki Forest virus. J. Cell Biol. 101:2284-2291.
31. Kielian, M., S. Jungerwirth, K. U. Sayad, and S. DeCandido. 1990. Biosynthesis, maturation, and acid activation of the Semliki Forest virus fusion protein. J. Virol. 64:4614-4624.
32. Knerr, I., M. Schnare, K. Hermann, S. Kausler, M. Lehner, T. Vogler, W. Rascher, and U. Meissner. 2 November 2006. Fusiogenic endogenous-retroviral syncytin-1 exerts anti-apoptotic functions in staurosporine-challenged CHO cells. Apoptosis. doi:10.1007/s10495-006-0329-9.
33. Kostolansky, F., G. Russ, V. Mucha, and B. Styk. 1988. Changes in the influenza virus haemagglutinin at acid pH detected by monoclonal antibodies to glycopolypeptides HA1 and HA2. Arch. Virol. 101:13-24.
34. Lamb, R. A. 1993. Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11.
35. Li, Y., X. Han, A. L. Lai, J. H. Bushweller, D. S. Cafiso, and L. K. Tamm. 2005. Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of influenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J. Virol. 79:12065-12076.
36. Locker, J. K., and G. Griffiths. 1999. An unconventional role for cytoplasmic disulfide bonds in vaccinia virus proteins. J. Cell Biol. 144:267-279.
37. Luz, J. M., and W. J. Lennarz. 1996. Protein disulfide isomerase: a multifunctional protein of the endoplasmic reticulum. EXS 77:97-117.
38. Mandel, R., H. J. Ryser, F. Ghani, M. Wu, and D. Peak. 1993. Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc. Natl. Acad. Sci. USA 90:4112-4116.
39. Markovic, I., H. Pulyaeva, A. Sokoloff, and L. V. Chernomordik. 1998. Membrane fusion mediated by baculovirus gp64 involves assembly of stable gp64 trimers into multiprotein aggregates. J. Cell Biol. 143:1155-1166.
40. Markovic, I., T. S. Stantchev, K. H. Fields, L. J. Tiffany, M. Tomic, C. D. Weiss, C. C. Broder, K. Strebel, and K. A. Clouse. 2004. Thiol/disulfide exchange is a prerequisite for CXCR4-tropic HIV-1 envelope-mediated T-cell fusion during viral entry. Blood 103:1586-1594.
41. Matthias, L. J., and P. J. Hogg. 2003. Redox control on the cell surface: implications for HIV-1 entry. Antioxid. Redox. Signal 5:133-138.
42. Mc Ginnes, L. W., J. Reiter, H. Pantua, and T. G. Morrison. 2006. Newcastle disease virus propagation, quantification and storage, 15F.2.3-15F.2.11. In R. Coica, T. Kowalik, J. Quarles, B. Steveman, and R. Taylor (ed.), Current protocols in microbiology, vol. 1. John Wiley and Sons, Inc., Hoboken, NJ.
43. McGinnes, L. W., K. Gravel, and T. G. Morrison. 2002. Newcastle disease virus HN protein alters the conformation of the F protein at cell surfaces. J. Virol. 76:12622-12633.
44. McGinnes, L. W., and T. G. Morrison. 2006. Inhibition of receptor binding stabilizes Newcastle disease virus HN and F protein-containing complexes. J. Virol. 80:2894-2903.
45. McGinnes, L. W., and T. G. Morrison. 1994. The role of the individual cysteine residues in the formation of the mature, antigenic HN protein of Newcastle disease virus. Virology 200:470-483.
46. McGinnes, L. W., T. Sergel, H. Chen, L. Hamo, S. Schwertz, D. Li, and T. G. Morrison. 2001. Mutational analysis of the membrane proximal heptad repeat of the Newcastle disease virus fusion protein. Virology 289:343-352.
47. Melikyan, G. B., S. Lin, M. G. Roth, and F. S. Cohen. 1999. Amino acid sequence requirements of the transmembrane and cytoplasmic domains of influenza virus hemagglutinin for viable membrane fusion. Mol. Biol. Cell 10:1821-1836.
48. Meyer, W. J., S. Gidwitz, V. K. Ayers, R. J. Schoepp, and R. E. Johnston. 1992. Conformational alteration of Sindbis virion glycoproteins induced by heat, reducing agents, or low pH. J. Virol. 66:3504-3513.
49. Morrison, T. G. 2003. Structure and function of a paramyxovirus fusion protein. Biochim. Biophys. Acta 1614:73-84.
50. Morrison, T. G., and L. W. McGinnes. 1989. Avian cells expressing the Newcastle disease virus hemagglutinin-neuraminidase protein are resistant to Newcastle disease virus infection. Virology 171:10-17.
51. Morrison, T. G., M. E. Peeples, and L. W. McGinnes. 1987. Conformational change in a viral glycoprotein during maturation due to disulfide bond disruption. Proc. Natl. Acad. Sci. USA 84:1020-1024.
52. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63.
53. Mou, Y., H. Ni, and J. A. Wilkins. 1998. The selective inhibition of beta 1 and beta 7 integrin-mediated lymphocyte adhesion by bacitracin. J. Immunol. 161:6323-6329.
54. Noiva, R. 1999. Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Semin. Cell Dev. Biol. 10:481-493.
55. Ou, W., and J. Silver. 2006. Role of protein disulfide isomerase and other thiol-reactive proteins in HIV-1 envelope protein-mediated fusion. Virology 350:406-417.
56. Pinter, A., R. Kopelman, Z. Li, S. C. Kayman, and D. A. Sanders. 1997. Localization of the labile disulfide bond between SU and TM of the murine leukemia virus envelope protein complex to a highly conserved CWLC motif in SU that resembles the active-site sequence of thiol-disulfide exchange enzymes. J. Virol. 71:8073-8077.
57. Puri, A., F. P. Booy, R. W. Doms, J. M. White, and R. Blumenthal. 1990. Conformational changes and fusion activity of influenza virus hemagglutinin of the H2 and H3 subtypes: effects of acid pretreatment. J. Virol. 64:3824-3832.
58. Roche, S., S. Bressanelli, F. A. Rey, and Y. Gaudin. 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313:187-191.
59. Russell, C. J., T. S. Jardetzky, and R. A. Lamb. 2001. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 20:4024-4034.
60. Russell, C. J., and L. E. Luque. 2006. The structural basis of paramyxovirus invasion. Trends Microbiol. 14:243-246.
61. Ryser, H. J., E. M. Levy, R. Mandel, and G. J. DiSciullo. 1994. Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc. Natl. Acad. Sci. USA 91:4559-4563.
62. Sergel, T., L. W. McGinnes, and T. G. Morrison. 1993. The fusion promotion activity of the NDV HN protein does not correlate with neuraminidase activity. Virology 196:831-834.
63. Skehel, J. J., P. M. Bayley, E. B. Brown, S. R. Martin, M. D. Waterfield, J. M. White, I. A. Wilson, and D. C. Wiley. 1982. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. USA 79:968-972.
64. Takizawa, N., T. C. Smith, T. Nebl, J. L. Crowley, S. J. Palmieri, L. M. Lifshitz, A. G. Ehrhardt, L. M. Hoffman, M. C. Beckerle, and E. J. Luna. 2006. Supervillin modulation of focal adhesions involving TRIP6/ZRP-1. J. Cell Biol. 174:447-458.
65. Tamm, L. K., X. Han, Y. Li, and A. L. Lai. 2002. Structure and function of membrane fusion peptides. Biopolymers 66:249-260.
66. Turano, C., S. Coppari, F. Altieri, and A. Ferraro. 2002. Proteins of the PDI family: unpredicted non-ER locations and functions. J. Cell Physiol. 193:154-163.
67. Vitkovic, L., and H. L. Sadoff. 1977. Purification of the extracellular protease of Bacillus licheniformis and its inhibition by bacitracin. J. Bacteriol. 131:891-896.
68. Wahlberg, J. M., and H. Garoff. 1992. 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. 116:339-348.
69. Wallin, M., M. Ekstrom, and H. Garoff. 2004. Isomerization of the intersub-unit disulphide-bond in Env controls retrovirus fusion. EMBO J. 23:54-65.
70. Weissenhorn, W., A. Dessen, L. J. Calder, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1999. Structural basis for membrane fusion by enveloped viruses. Mol. Membr. Biol. 16:3-9.
71. Wilkinson, B., and H. F. Gilbert. 2004. Protein disulfide isomerase. Biochim. Biophys. Acta 1699:35-44.
72. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373.
73. Wouters, M. A., K. K. Lau, and P. J. Hogg. 2004. Cross-strand disulphides in cell entry proteins: poised to act. Bioessays 26:73-79.
74. Yin, H. S., R. G. Paterson, X. Wen, R. A. Lamb, and T. S. Jardetzky. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. USA 102:9288-9293.
75. Yin, H. S., X. Wen, R. G. Paterson, R. A. Lamb, and T. S. Jardetzky. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, profusion conformation. Nature 439:38-44.
76. Young, J. K., R. P. Hicks, G. E. Wright, and T. G. Morrison. 1997. Analysis of a peptide inhibitor of paramyxovirus (NDV) fusion using biological assays, NMR, and molecular modeling. Virology 238:291-304.
77. Zelenkov, P., R. Baumgartner, K. Bise, M. Heide, R. Meier, S. Stocker, R. Sroka, R. Goldbrunner, and W. Stummer. 27 September 2006. Acute morphological sequelae of photodynamic therapy with 5-aminolevulinic acid in the C6 spheroid model. J Neurooncol. doi:10.1007/sll060-006-9252-8.