Mutations in the parainfluenza virus 5 fusion protein reveal domains important for fusion triggering and metastability

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13520-13531

  Bose, Sayantan ^a   Heath, Carissa M ^a   Shah, Priya A ^a   Alayyoubi, Maher ^a   Jardetzky, Theodore S ^b   Lamb, Robert A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARAMYXOVIRUS MEMBRANE GLYCOPROTEINS F PROTEIN; PARAMYXOVIRUS MEMBRANE GLYCOPROTEINS G PROTEIN; PARAMYXOVIRUS MEMBRANE GLYCOPROTEINS HN PROTEIN; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; DISULFIDE BOND; ELECTRON MICROSCOPY; FLOW CYTOMETRY; HUMAN; HYDROPHOBICITY; IMMUNOPRECIPITATION; MEMBRANE FUSION; NONHUMAN; PARAINFLUENZA VIRUS; PARAINFLUENZA VIRUS 5; POINT MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RECEPTOR BINDING; SYNCYTIUM; VIRUS MUTATION;

ANIMALS; CELL LINE; HN PROTEIN; HUMANS; MUTATION; PARAINFLUENZA VIRUS 5; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; RUBULAVIRUS INFECTIONS; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 84888072258     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02123-13     Document Type: Article

References (62)

1. Lamb RA. 2007. Mononegavirales, p 1357-1361. In Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott, Williams and Wilkins, Philadelphia, PA.
2. Schowalter RM, Chang A, Robach JG, Buchholz UJ, Dutch RE. 2009. Low-pH triggering of human metapneumovirus fusion:essential residues and importance in entry. J. Virol. 83:1511-1522.
3. Heminway BR, Yu Y, Galinski MS. 1994. Paramyxovirus mediated cell fusion requires co-expression of both the fusion and hemagglutininneuraminidase glycoproteins. Virus Res. 31:1-16.
4. Horvath CM, Paterson RG, Shaughnessy MA, Wood R, Lamb RA. 1992. Biological activity of paramyxovirus fusion proteins:factors influencing formation of syncytia. J. Virol. 66:4564-4569.
5. Hu X, Ray R, Compans RW. 1992. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses. J. Virol. 66:1528-1534.
6. Morrison T, McQuain C, McGinnes L. 1991. Complementation between avirulent Newcastle disease virus and a fusion protein gene expressed from a retrovirus vector:requirements for membrane fusion. J. Virol. 65:813-822.
7. Yao Q, Hu X, Compans RW. 1997. Association of the parainfluenza virus fusion and hemagglutinin-neuraminidase glycoproteins on cell surfaces. J. Virol. 71:650-656.
8. Connolly SA, Leser GP, Yin HS, Jardetzky TS, Lamb RA. 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.
9. Bose S, Zokarkar A, Welch BD, Leser GP, Jardetzky TS, Lamb RA. 2012. Fusion activation by a headless parainfluenza virus 5 hemagglutininneuraminidase stalk suggests a modular mechanism for triggering. Proc. Natl. Acad. Sci. U.S.A. 109:E2625-E2634.
10. Ader N, Brindley M, Avila M, Orvell C, Horvat B, Hiltensperger G, Schneider-Schaulies J, Vandevelde M, Zurbriggen A, Plemper RK, Plattet P. 2013. Mechanism for active membrane fusion triggering by morbillivirus attachment protein. J. Virol. 87:314-326.
11. Chan YP, Lu M, Dutta S, Yan L, Barr J, Flora M, Feng YR, Xu K, Nikolov DB, Wang LF, Skiniotis G, Broder CC. 2012. Biochemical, conformational and immunogenic analysis of soluble trimeric forms of henipavirus fusion glycoproteins. J. Virol. 86:11457-11471.
12. Baker KA, Dutch RE, Lamb RA, Jardetzky TS. 1999. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3:309-319.
13. Lamb RA, Jardetzky TS. 2007. Structural basis of viral invasion:lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17:427-436.
14. Chang A, Dutch RE. 2012. Paramyxovirus fusion and entry:multiple paths to a common end. Viruses 4:613-636.
15. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38-44.
16. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, Zhou T, Baxa U, Yasuda E, Beaumont T, Kumar A, Modjarrad K, Zheng Z, Zhao M, Xia N, Kwong PD, Graham BS. 2013. Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340:1113-1117.
17. Welch BD, Liu Y, Kors CA, Leser GP, Jardetzky TS, Lamb RA. 2012. Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc. Natl. Acad. Sci. U.S.A. 109:16672-16677.
18. Yin H-S, Paterson RG, Wen X, Lamb RA, Jardetzky TS. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. U.S.A. 102:9288-9293.
19. Swanson K, Wen X, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 2010. Structure of the Newcastle disease virus F protein in the post-fusion conformation. Virology 402:372-379.
20. McLellan JS, Yang Y, Graham BS, Kwong PD. 2011. Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J. Virol. 85:7788-7796.
21. Swanson KA, Settembre EC, Shaw CA, Dey AK, Rappuoli R, Mandl CW, Dormitzer PR, Carfi A. 2011. Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc. Natl. Acad. Sci. U.S.A. 108:9619-9624.
22. Russell CJ, Jardetzky TS, Lamb RA. 2001. Membrane fusion machines of paramyxoviruses:capture of intermediates of fusion. EMBO J. 20:4024-4034.
23. Kim YH, Donald JE, Grigoryan G, Leser GP, Fadeev AY, Lamb RA, DeGrado WF. 2011. Capture and imaging of a prehairpin fusion intermediate of the paramyxovirus PIV5. Proc. Natl. Acad. Sci. U.S.A. 108:20992-20997.
24. Crennell S, Takimoto T, Portner A, Taylor G. 2000. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat. Struct. Biol. 7:1068-1074.
25. Lawrence MC, Borg NA, Streltsov VA, Pilling PA, Epa VC, Varghese JN, McKimm-Breschkin JL, Colman PM. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335:1343-1357.
26. Yuan P, Thompson T, Wurzburg BA, Paterson RG, Lamb RA, Jardetzky TS. 2005. Structural studies of the parainfluenza virius 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803-815.
27. Yuan P, Leser GP, Demeler B, Lamb RA, Jardetzky TS. 2008. Domain architecture and oligomerization properties of the paramyxovirus PIV 5 hemagglutinin-neuraminidase (HN) protein. Virology 378:282-291.
28. Yuan P, Swanson KA, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 2011. Structure of the Newcastle disease virus hemagglutininneuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc. Natl. Acad. Sci. U.S.A. 108:14920-14925.
29. Yuan P, Paterson RG, Leser GP, Lamb RA, Jardetzky TS. 2012. Structure of the Ulster strain Newcastle disease virus hemagglutininneuraminidase reveals auto-inhibitory interactions associated with low virulence. PLoS Pathog. 8:e1002855. doi:10.1371/journal.ppat.1002855.
30. Colf LA, Juo ZS, Garcia KC. 2007. Structure of the measles virus hemagglutinin. Nat. Struct. Mol. Biol. 14:1227-1228.
31. Hashiguchi T, Kajikawa M, Maita N, Takeda M, Kuroki K, Sasaki K, Kohda D, Yanagi Y, Maenaka K. 2007. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc. Natl. Acad. Sci. U.S.A. 104:19535-19540.
32. Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, Stuart DI. 2008. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat. Struct. Biol. 15:567-572.
33. Xu K, Rajashankar KR, Chan YP, Himanen JP, Broder CC, Nikolov DB. 2008. Host cell recognition by the henipaviruses:crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc. Natl. Acad. Sci. U.S.A. 105:9953-9958.
34. Bose S, Welch BD, Kors CA, Yuan P, Jardetzky TS, Lamb RA. 2011. Structure and mutagenesis of the parainfluenza virus 5 hemagglutininneuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J. Virol. 85:12855-12866.
35. Maar D, Harmon B, Chu D, Schulz B, Aguilar HC, Lee B, Negrete OA. 2012. Cysteines in the stalk of the Nipah virusGglycoprotein are located in a distinct subdomain critical for fusion activation. J. Virol. 86:6632-6642.
36. Ader N, Brindley MA, Avila M, Origgi FC, Langedijk J, Orvell C, Vandevelde M, Zurbriggen A, Plemper RK, Plattet P. 2012. Structural rearrangements of the central region of the morbillivirus attachment protein stalk domain trigger F protein refolding for membrane fusion. J. Biol. Chem. 287:16324-16334.
37. Paal T, Brindley MA, St Clair C, Prussia A, Gaus D, Krumm SA, Snyder JP, Plemper RK. 2009. Probing the spatial organization of measles virus fusion complexes. J. Virol. 83:10480-10493.
38. Lee JK, Prussia A, Paal T, White LK, Snyder JP, Plemper RK. 2008. Functional interaction between paramyxovirus fusion and attachment proteins. J. Biol. Chem. 283:16561-16572.
39. Bishop KA, Hickey AC, Khetawat D, Patch JR, Bossart KN, Zhu Z, Wang LF, Dimitrov DS, Broder CC. 2008. Residues in the stalk domain of the Hendra virus G glycoprotein modulate conformational changes associated with receptor binding. J. Virol. 82:11398-11409.
40. Bousse T, Takimoto T, Gorman WL, Takahashi T, Portner A. 1994. Regions on the hemagglutinin-neuraminidase proteins of human parainfluenza virus type-1 and Sendai virus important for membrane fusion. Virology 204:506-514.
41. Deng R, Wang Z, Mirza AM, Iorio RM. 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.
42. Deng R, Wang Z, Mahon PJ, Marinello M, Mirza A, Iorio RM. 1999. Mutations in the Newcastle disease virus hemagglutinin-neuraminidase protein that interfere with its ability to interact with the homologous F protein in the promotion of fusion. Virology 253:43-54.
43. Melanson VR, Iorio RM. 2004. Amino acid substitutions in the F-specific domain in the stalk of the newcastle disease virus HN protein modulate fusion and interfere with its interaction with the F protein. J. Virol. 78:13053-13061.
44. Melanson VR, Iorio RM. 2006. Addition of N-glycans in the stalk of the Newcastle disease virus HN protein blocks its interaction with the F protein and prevents fusion. J. Virol. 80:623-633.
45. Stone-Hulslander J, Morrison TG. 1999. Mutational analysis of heptad repeats in the membrane-proximal region of Newcastle disease virus HN protein. J. Virol. 73:3630-3637.
46. Tanabayashi K, Compans RW. 1996. Functional interaction of paramyxovirus glycoproteins:identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70:6112-6118.
47. Brindley MA, Takeda M, Plattet P, Plemper RK. 2012. Triggering the measles virus membrane fusion machinery. Proc. Natl. Acad. Sci. U.S.A. 109:E3018-E3027.
48. Navaratnarajah CK, Negi S, Braun W, Cattaneo R. 2012. Membrane fusion triggering:three modules with different structure and function in the upper half of the measles virus attachment protein stalk. J. Biol. Chem. 287:38543-38551.
49. Apte-Sengupta S, Negi S, Leonard VH, Oezguen N, Navaratnarajah CK, Braun W, Cattaneo R. 2012. Base of the measles virus fusion trimer head receives the signal that triggers membrane fusion. J. Biol. Chem. 287:33026-33035.
50. Tsurudome M, Ito M, Nishio M, Nakahashi M, Kawano M, Komada H, Nosaka T, Ito Y. 2011. Identification of domains on the fusion (F) protein trimer that influence the hemagglutinin-neuraminidase specificity of the F protein in mediating cell-cell fusion. J. Virol. 85:3153-3161.
51. Tsurudome M, Nakahashi M, Matsushima Y, Ito M, Nishio M, Kawano M, Komada H, Nosaka T. 2013. Full conversion of the hemagglutininneuraminidase specificity of the parainfluenza virus 5 fusion protein by replacement of 21 amino acids in its head region with those of the simian virus 41 fusion protein. J. Virol. 87:8342-8350.
52. Randall RE, Young DF, Goswami KKA, Russell WC. 1987. Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates. J. Gen. Virol. 68:2769-2780.
53. Paterson RG, Russell CJ, Lamb RA. 2000. Fusion protein of the paramyxovirus SV5:destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30.
54. Paterson RG, Lamb RA. 1993. The molecular biology of influenza viruses and paramyxoviruses, p 35-73. In Davidson A, Elliott RM(ed), Molecular virology:a practical approach. IRL Oxford University Press, Oxford, United Kingdom.
55. Paterson RG, Hiebert SW, Lamb RA. 1985. Expression at the cell surface of biologically active fusion and hemagglutinin-neuraminidase proteins of the paramyxovirus simian virus 5 from cloned cDNA. Proc. Natl. Acad. Sci. U.S.A. 82:7520-7524.
56. Tamada T, Honjo E, Maeda Y, Okamoto T, Ishibashi M, Tokunaga M, Kuroki R. 2006. Homodimeric cross-over structure of the human granulocyte colony-stimulating factor (GCSF) receptor signaling complex. Proc. Natl. Acad. Sci. U.S.A. 103:3135-3140.
57. Chow D, He X, Snow AL, Rose-John S, Garcia KC. 2001. Structure of an extracellular gp130 cytokine receptor signaling complex. Science 291:2150-2155.
58. Boulanger MJ, Chow DC, Brevnova EE, Garcia KC. 2003. Hexameric structure and assembly of the interleukin-6/IL-6 alpha-receptor/gp130 complex. Science 300:2101-2104.
59. Aguilar HC, Matreyek KA, Filone CM, Hashimi ST, Levroney EL, Negrete OA, Betrolotti-Ciarlet A, Choi DY, McHardy I, Fulcher JA, Su SV, Wolf MC, Kohatsu L, Baum LG, Lee B. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J. Virol. 80:4878-4889.
60. Plemper RK, Hammond AL, Gerlier D, Fielding AK, Cattaneo R. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J. Virol. 76:5051-5061.
61. Mirza AM, Iorio RM. 2013. A mutation in the stalk of the NDV HN protein prevents triggering of the F protein despite allowing efficient HN-F complex formation. J. Virol. 87:8813-8815.
62. Corey EA, Iorio RM. 2007. Mutations in the stalk of the measles virus hemagglutinin protein decrease fusion but do not interfere with virusspecific interaction with the homologous fusion protein. J. Virol. 81:9900-9910.