Soluble respiratory syncytial virus fusion protein in the fully cleaved, pretriggered state is triggered by exposure to low-molarity buffer

Journal of Virology

Volumn 85, Issue 8, 2011, Pages 3968-3977

  Chaiwatpongsakorn, Supranee ^a,c   Epand, Raquel F ^d   Collins, Peter L ^e   Epand, Richard M ^d   Peeples, Mark E ^a,b  

^a NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; FURIN; IMIDAZOLE; LIPOSOME; SODIUM CHLORIDE; VIRUS FUSION PROTEIN;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; HEAT TREATMENT; MEMBRANE FUSION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN SECRETION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; VIRION; VIRUS ATTACHMENT;

BUFFERS; HUMANS; OSMOTIC PRESSURE; RESPIRATORY SYNCYTIAL VIRUSES; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

PARAMYXOVIRIDAE; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 79952820810     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01813-10     Document Type: Article

References (48)

1. 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.
2. Barretto, N., L. K. Hallak, and M. E. Peeples. 2003. Neuraminidase treatment of respiratory syncytial virus-infected cells or virions, but not target cells, enhances cell-cell fusion and infection. Virology 313:33-43.
3. Beeler, J. A., and K. van Wyke Coelingh. 1989. Neutralization epitopes of the F glycoprotein of respiratory syncytial virus: effect of mutation upon fusion function. J. Virol. 63:2941-2950. (Pubitemid 19156013)
4. Begona Ruiz-Arguello, M., et al. 2002. Effect of proteolytic processing at two distinct sites on shape and aggregation of an anchorless fusion protein of human respiratory syncytial virus and fate of the intervening segment. Virology 298:317-326. (Pubitemid 35034547)
5. Byrappa, S., D. K. Gavin, and K. C. Gupta. 1995. A highly efficient procedure for site-specific mutagenesis of full-length plasmids using Vent DNA polymerase. Genome Res. 5:404-407.
6. Calder, L. J., et al. 2000. Electron microscopy of the human respiratory syncytial virus fusion protein and complexes that it forms with monoclonal antibodies. Virology 271:122-131. (Pubitemid 30341521)
7. Carr, C. M., C. Chaudhry, and P. S. Kim. 1997. Influenza hemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl. Acad. Sci. U. S. A. 94:14306-14313.
8. Chen, L., et al. 2001. The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure (Camb.) 9:255-266. (Pubitemid 32245876)
9. Collins, P. L., and J. E. J. Crowe. 2007. Respiratory syncytial virus and metapneumovirus, p. 1601-1646. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
10. Connolly, S. A., G. P. Leser, T. S. Jardetzky, and R. A. Lamb. 2009. Bimolecular complementation of paramyxovirus fusion and hemagglutinin- neuraminidase proteins enhances fusion: implications for the mechanism of fusion triggering. J. Virol. 83:10857-10868.
11. Connolly, S. A., G. P. Leser, H. S. Yin, T. S. Jardetzky, and R. A. Lamb. 2006. Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 103:17903-17908.
12. Damico, R. L., J. Crane, and P. Bates. 1998. Receptor-triggered membrane association of a model retroviral glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 95:2580-2585.
13. Day, N. D., et al. 2006. Contribution of cysteine residues in the extracellular domain of the F protein of human respiratory syncytial virus to its function. Virol. J. 3:34.
14. Deng, R., Z. Wang, A. M. Mirza, and R. M. Iorio. 1995. Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike. Virology 209:457-469.
15. Dominy, B. N., D. Perl, F. X. Schmid, and C. L. Brooks III. 2002. The effects of ionic strength on protein stability: the cold shock protein family. J. Mol. Biol. 319:541-554.
16. Doms, R. W., A. Helenius, and J. White. 1985. Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change. J. Biol. Chem. 260:2973-2981.
17. Ebata, S. N., M. J. Cote, C. Y. Kang, and K. Dimock. 1991. The fusion and hemagglutinin-neuraminidase glycoproteins of human parainfluenza virus 3 are both required for fusion. Virology 183:437-441.
18. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
19. Elcock, A. H., and J. A. McCammon. 1998. Electrostatic contributions to the stability of halophilic proteins. J. Mol. Biol. 280:731-748.
20. Falsey, A. R., P. A. Hennessey, M. A. Formica, C. Cox, and E. E. Walsh. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352:1749-1759.
21. Gonzalez-Reyes, L., et al. 2001. Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 98:9859-9864.
22. Hernandez, L. D., et al. 1997. Activation of a retroviral membrane fusion protein: soluble receptor-induced liposome binding of the ALSV envelope glycoprotein. J. Cell Biol. 139:1455-1464. (Pubitemid 28013666)
23. Hu, X. L., R. Ray, and R. W. Compans. 1992. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses. J. Virol. 66:1528-1534.
24. Johnson, P. R., Jr., et al. 1987. Antigenic relatedness between glycoproteins of human respiratory syncytial virus subgroups A and B: evaluation of the contributions of F and G glycoproteins to immunity. J. Virol. 61:3163-3166.
25. Kahn, J. S., M. J. Schnell, L. Buonocore, and J. K. Rose. 1999. Recombinant vesicular stomatitis virus expressing respiratory syncytial virus (RSV) glycoproteins: RSV fusion protein can mediate infection and cell fusion. Virology 254:81-91.
26. Karron, R. A., et al. 1997. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl. Acad. Sci. U. S. A. 94:13961-13966.
27. Kohn, W. D., C. M. Kay, and R. S. Hodges. 1997. Salt effects on protein stability: two-stranded alpha-helical coiled-coils containing interor intrahelical ion pairs. J. Mol. Biol. 267:1039-1052.
28. Liao, M., C. Sanchez-San Martin, A. Zheng, and M. Kielian. 2010. In vitro reconstitution reveals key intermediate states of trimer formation by the dengue virus membrane fusion protein. J. Virol. 84:5730-5740.
29. Paterson, R. G., C. J. Russell, and R. A. Lamb. 2000. Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30.
30. Pollack, P., and J. R. Groothuis. 2002. Development and use of palivizumab (Synagis): a passive immunoprophylactic agent for RSV. J. Infect. Chemother. 8:201-206.
31. Rao, J. K., and P. Argos. 1981. Structural stability of halophilic proteins. Biochemistry 20:6536-6543.
32. Record, M. T., Jr., W. Zhang, and C. F. Anderson. 1998. Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: a practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects, and osmotic effects of salts. Adv. Protein Chem. 51:281-353.
33. Ruiz-Arguello, M. B., et al. 2004. Thermostability of the human respiratory syncytial virus fusion protein before and after activation: implications for the membrane-fusion mechanism. J. Gen. Virol. 85:3677-3687.
34. 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.
35. Sanchez-San Martin, C., H. Sosa, and M. Kielian. 2008. A stable prefusion intermediate of the alphavirus fusion protein reveals critical features of class II membrane fusion. Cell Host Microbe 4:600-608. (Pubitemid 352762956)
36. Shay, D. K., et al. 1999. Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 282:1440-1446.
37. Tanabayashi, K., and R. W. Compans. 1996. Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70:6112-6118.
38. Techaarpornkul, S., N. Barretto, and M. E. Peeples. 2001. Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J. Virol. 75:6825-6834.
39. Ternette, N., D. Stefanou, S. Kuate, K. Uberla, and T. Grunwald. 2007. Expression of RNA virus proteins by RNA polymerase II dependent expression plasmids is hindered at multiple steps. Virol. J. 4:51.
40. Ugwu, S. O., and S. P. Apte. 2004. The effect of buffers on protein conformational stability. Pharm. Technol. 2004:86-113.
41. Vonhippel, P. H., and K. Y. Wong. 1964. Neutral salts: the generality of their effects on the stability of macromolecular conformations. Science 145:577-580.
42. Wharton, S. A., J. J. Skehel, and D. C. Wiley. 2000. Temperature dependence of fusion by Sendai virus. Virology 271:71-78. (Pubitemid 30341516)
43. 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. U. S. A. 102:9288-9293.
44. 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, prefusion conformation. Nature 439:38-44.
45. Yunus, A. S., et al. 2010. Elevated temperature triggers human respiratory syncytial virus F protein six-helix bundle formation. Virology 396:226-237.
46. Zhao, X., M. Singh, V. N. Malashkevich, and P. S. Kim. 2000. Structural characterization of the human respiratory syncytial virus fusion protein core. Proc. Natl. Acad. Sci. U. S. A. 97:14172-14177.
47. Zimmer, G., L. Budz, and G. Herrler. 2001. Proteolytic activation of respiratory syncytial virus fusion protein. Cleavage at two furin consensus sequences. J. Biol. Chem. 276:31642-31650.
48. Zimmer, G., I. Trotz, and G. Herrler. 2001. N-glycans of F protein differentially affect fusion activity of human respiratory syncytial virus. J. Virol. 75:4744-4751. (Pubitemid 32381517)