Influenza a virus hemagglutinin trimerization completes monomer folding and antigenicity

Journal of Virology

Volumn 87, Issue 17, 2013, Pages 9742-9753

  Magadán, Javier G ^a   Khurana, Surender ^b   Das, Suman R ^a,d   Frank, Gregory M ^b   Stevens, James ^c   Golding, Hana ^b   Bennink, Jack R ^a   Yewdell, Jonathan W ^a  

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

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^c NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; INFLUENZA VIRUS HEMAGGLUTININ; MONOCLONAL ANTIBODY; MONOMER;

ANIMAL CELL; ANTIGENICITY; ARTICLE; BINDING SITE; BIOCHEMISTRY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOGENICITY; INFLUENZA VIRUS A; ISOTOPE LABELING; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; TRIMERIZATION; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CELL LINE; DOGS; EPITOPES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; MICE; MODELS, MOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY;

EID: 84883292796     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00471-13     Document Type: Article

References (46)

1. Hers JF. 1966. Disturbances of the ciliated epithelium due to influenza virus. Am. Rev. Respir. Dis. 93(Suppl):162-177.
2. Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531- 569.
3. Russ G, Bennink JR, Bachi T, Yewdell JW. 1991. Influenza virus hemagglutinin trimers and monomers maintain distinct biochemical modifications and intracellular distribution in brefeldin A-treated cells. Cell Regul. 2:549-563.
4. Han Y, David A, Liu B, Magadan JG, Bennink JR, Yewdell JW, Qian SB. 2012. Monitoring cotranslational protein folding in mammalian cells at codon resolution. Proc. Natl. Acad. Sci. U. S. A. 109:12467-12472.
5. Copeland CS, Zimmer KP, Wagner KR, Healey GA, Mellman I, Helenius A. 1988. Folding, trimerization, and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell 53:197-209.
6. Yewdell JW, Yellen A, Bachi T. 1988. Monoclonal antibodies localize events in the folding, assembly, and intracellular transport of the influenza virus hemagglutinin glycoprotein. Cell 52:843-852.
7. Gething MJ, McCammon K, Sambrook J. 1986. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell 46:939-950.
8. Copeland CS, Doms RW, Bolzau EM, Webster RG, Helenius A. 1986. Assembly of influenza hemagglutinin trimers and its role in intracellular transport. J. Cell Biol. 103:1179-1191.
9. Couch RB, Kasel JA. 1983. Immunity to influenza in man. Annu. Rev. Microbiol. 37:529-549.
10. Webster RG, Laver WG, Kilbourne ED. 1975. Antigenic variation of influenza viruses, p 269-314. In Kilbourne ED (ed), The influenza viruses and influenza. Academic Press, New York, NY.
11. Lambkin R, Dimmock NJ. 1995. All rabbits immunized with type A influenza virions have a serum haemagglutination-inhibition antibody response biased to a single epitope in antigenic site B. J. Gen. Virol. 76(Pt 4):889 - 897.
12. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W. 1982. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31:417-427.
13. Gerhard W, Yewdell J, Frankel ME, Webster R. 1981. Antigenic structure of influenza virus haemagglutinin defined by hybridoma antibodies. Nature 290:713-717.
14. Yewdell JW. 2011. Viva la revolucion: rethinking influenza a virus antigenic drift. Curr. Opin. Virol. 1:177-183.
15. Yewdell JW, Taylor A, Yellen A, Caton A, Gerhard W, Bachi T. 1993. Mutations in or near the fusion peptide of the influenza virus hemagglutinin affect an antigenic site in the globular region. J. Virol. 67:933-942.
16. Yewdell JW, Caton AJ, Gerhard W. 1986. Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. J. Virol. 57:623-628.
17. Yewdell JW, Frank E, Gerhard W. 1981. Expression of influenza A virus internal antigens on the surface of infected P815 cells. J. Immunol. 126: 1814-1819.
18. Yewdell JW, Gerhard W. 1981. Antigenic characterization of viruses by monoclonal antibodies. Annu. Rev. Microbiol. 35:185-206.
19. Yewdell JW, Webster RG, Gerhard WU. 1979. Antigenic variation in three distinct determinants of an influenza type A haemagglutinin molecule. Nature 279:246-248.
20. Dolan BP, Li L, Takeda K, Bennink JR, Yewdell JW. 2010. Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase. J. Immunol. 184: 1419-1424.
21. Bonifacino JS, Dell'Angelica EC. 2001. Immunoprecipitation. Curr. Protoc. Cell Biol. Chapter 7:Unit 7.2.
22. Magadan JG, Perez-Victoria FJ, Sougrat R, Ye Y, Strebel K, Bonifacino JS. 2010. Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Pathog. 6:e1000869. doi:10.1371/journal.ppat.1000869.
23. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870.
24. Khurana S, Suguitan AL, Jr, Rivera Y, Simmons CP, Lanzavecchia A, Sallusto F, Manischewitz J, King LR, Subbarao K, Golding H. 2009. Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med. 6:e1000049. doi:10.1371/journal.pmed.1000049.
25. Khurana S, Verma N, Yewdell JW, Hilbert AK, Castellino F, Lattanzi M, Del Giudice G, Rappuoli R, Golding H. 2011. MF59 adjuvant enhances diversity and affinity of antibody-mediated immune response to pandemic influenza vaccines. Sci. Transl. Med. 3:85ra48. doi:10.1126 /scitranslmed.3002336.
26. Braakman I, Hoover-Litty H, Wagner KR, Helenius A. 1991. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell Biol. 114: 401-411.
27. Griffiths G, Quinn P, Warren G. 1983. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J. Cell Biol. 96:835-850.
28. Strous GJ, Lodish HF. 1980. Intracellular transport of secretory and membrane proteins in hepatoma cells infected by vesicular stomatitis virus. Cell 22:709-717.
29. Tartakoff AM. 1983. Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell 32:1026-1028.
30. Yewdell JW, Gerhard W, Bachi T. 1983. Monoclonal anti-hemagglutinin antibodies detect irreversible antigenic alterations that coincide with the acid activation of influenza virus A/PR/834-mediated hemolysis. J. Virol. 48:239-248.
31. Skehel J, Bayley PM, Brown EB, Martin SR, Waterfield MD, White JM, Wilson IA, Wiley DC. 1982. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 79:968-972.
32. Ruigrok RW, Aitken A, Calder LJ, Martin SR, Skehel JJ, Wharton SA, Weis W, Wiley DC. 1988. Studies on the structure of the influenza virus haemagglutinin at the pH of membrane fusion. J. Gen. Virol. 69(Pt 11): 2785-2795.
33. Wharton SA, Ruigrok RW, Martin SR, Skehel JJ, Bayley PM, Weis W, Wiley DC. 1988. Conformational aspects of the acid-induced fusion mechanism of influenza virus hemagglutinin. Circular dichroism and fluorescence studies. J. Biol. Chem. 263:4474-4480.
34. Yewdell JW. 2010. Monoclonal antibodies specific for discontinuous epitopes direct refolding of influenza A virus hemagglutinin. Mol. Immunol. 47:1132-1136.
35. Barbey-Martin C, Gigant B, Bizebard T, Calder LJ, Wharton SA, Skehel JJ, Knossow M. 2002. An antibody that prevents the hemagglutinin low pH fusogenic transition. Virology 294:70-74.
36. Bizebard T, Gigant B, Rigolet P, Rasmussen B, Diat O, Bosecke P, Wharton SA, Skehel JJ, Knossow M. 1995. Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 376: 92-94.
37. Fleury D, Barrere B, Bizebard T, Daniels RS, Skehel JJ, Knossow M. 1999. Acomplex of influenza hemagglutinin with a neutralizing antibody that binds outside the virus receptor binding site. Nat. Struct. Biol. 6:530-534.
38. Fleury D, Wharton SA, Skehel JJ, Knossow M, Bizebard T. 1998. Antigen distortion allows influenza virus to escape neutralization. Nat. Struct. Biol. 5:119-123.
39. Knossow M, Daniels RS, Douglas AR, Skehel JJ, Wiley DC. 1984. Three-dimensional structure of an antigenic mutant of the influenza virus haemagglutinin. Nature 311:678-680.
40. Doms RW, Lamb RA, Rose JK, Helenius A. 1993. Folding and assembly of viral membrane proteins. Virology 193:545-562.
41. Hurtley SM, Helenius A. 1989. Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:277-307.
42. Locker JK, Opstelten DJ, Ericsson M, Horzinek MC, Rottier PJ. 1995. Oligomerization of a trans-Golgi/trans-Golgi network retained protein occurs in the Golgi complex and may be part of its retention. J. Biol. Chem. 270:8815-8821.
43. Musil LS, Goodenough DA. 1993. Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell 74:1065-1077.
44. DuBois RM, Aguilar-Yanez JM, Mendoza-Ochoa GI, Oropeza-Almazan Y, Schultz-Cherry S, Alvarez MM, White SW, Russell CJ. 2011. The receptor-binding domain of influenza virus hemagglutinin produced in Escherichia coli folds into its native, immunogenic structure. J. Virol. 85: 865-872.
45. Krammer F, Margine I, Tan GS, Pica N, Krause JC, Palese P. 2012. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS One 7:e43603. doi:10.1371/journal.pone.0043603.
46. Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ. 2004. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838-1842.