N-Linked Glycosylation in the Hemagglutinin of Influenza A Viruses

Yonsei Medical Journal

Volumn 53, Issue 5, 2012, Pages 886-893

  Kim, Jin Il ^a   Park, Man Seong ^a  

^a Hallym University   (South Korea)

Author keywords

Glycosylation; Hemagglutinin; Influenza virus; Pandemic

Indexed keywords

ALPHA 2,3 SIALIC ACID; AMINO ACID; ASPARAGINE; GLYCAN; GLYCOPROTEIN; SIALIC ACID; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ;

ANTIBODY DETECTION; ANTIGENICITY; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; N LINKED GLYCOSYLATION; NONHUMAN; PANDEMIC INFLUENZA; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; RECEPTOR BINDING; REVIEW; VIRUS MUTATION; VIRUS VIRULENCE;

EID: 84864585610     PISSN: 05135796     EISSN: None     Source Type: Journal    
DOI: 10.3349/ymj.2012.53.5.886     Document Type: Review

References (59)

1. Taubenberger JK, Kash JC. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 2010;7:440-51.
2. Salomon R, Webster RG. The influenza virus enigma. Cell 2009;136:402-10.
3. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, et al. A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A 2012;109:4269-74.
4. Bouvier NM, Palese P. The biology of influenza viruses. Vaccine 2008;26 Suppl 4:D49-53.
5. WHO. Global influenza programme (GIP). Available from: www.who.int/influenza/en/index.html. Accessed in May 31, 2012.
6. Barr IG, McCauley J, Cox N, Daniels R, Engelhardt OG, Fukuda K, et al. Epidemiological, antigenic and genetic characteristics of seasonal influenza A(H1N1), A(H3N2) and B influenza viruses: basis for the WHO recommendation on the composition of influenza vaccines for use in the 2009-2010 Northern Hemisphere season. Vaccine 2010;28:1156-67.
7. de Jong JC, Beyer WE, Palache AM, Rimmelzwaan GF, Osterhaus AD. Mismatch between the 1997/1998 influenza vaccine and the major epidemic A(H3N2) virus strain as the cause of an inadequate vaccine-induced antibody response to this strain in the elderly. J Med Virol 2000;61:94-9.
8. Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine 2007;25:6852-62.
9. Plotkin JB, Dushoff J, Levin SA. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc Natl Acad Sci U S A 2002;99:6263-8.
10. Palese P. Making better influenza virus vaccines? Emerg Infect Dis 2006;12:61-5.
11. Kreijtz JH, Fouchier RA, Rimmelzwaan GF. Immune responses to influenza virus infection. Virus Res 2011;162:19-30.
12. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011;333:850-6.
13. Fleishman SJ, Whitehead TA, Ekiert DC, Dreyfus C, Corn JE, Strauch EM, et al. Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 2011; 332:816-21.
14. Krause JC, Tsibane T, Tumpey TM, Huffman CJ, Basler CF, Crowe JE Jr. A broadly neutralizing human monoclonal antibody that recognizes a conserved, novel epitope on the globular head of the influenza H1N1 virus hemagglutinin. J Virol 2011;85:10905-8.
15. Whittle JR, Zhang R, Khurana S, King LR, Manischewitz J, Golding H, et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci U S A 2011;108:14216-21.
16. Kilbourne ED, Couch RB, Kasel JA, Keitel WA, Cate TR, Quarles JH, et al. Purified influenza A virus N2 neuraminidase vaccine is immunogenic and non-toxic in humans. Vaccine 1995;13:1799-803.
17. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 1999;5:1157-63.
18. Nayak B, Kumar S, DiNapoli JM, Paldurai A, Perez DR, Collins PL, et al. Contributions of the avian influenza virus HA, NA, and M2 surface proteins to the induction of neutralizing antibodies and protective immunity. J Virol 2010;84:2408-20.
19. Wei CJ, Boyington JC, Dai K, Houser KV, Pearce MB, Kong WP, et al. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci Transl Med 2010;2:24-21.
20. Sun S, Wang Q, Zhao F, Chen W, Li Z. Glycosylation site alteration in the evolution of influenza A (H1N1) viruses. PLoS One 2011;6:e22844.
21. Schulze IT. Effects of glycosylation on the properties and functions of influenza virus hemagglutinin. J Infect Dis 1997;176 Suppl 1:S24-8.
22. Aytay S, Schulze IT. Single amino acid substitutions in the hemagglutinin can alter the host range and receptor binding properties of H1 strains of influenza A virus. J Virol 1991;65:3022-8.
23. Gambaryan AS, Marinina VP, Tuzikov AB, Bovin NV, Rudneva IA, Sinitsyn BV, et al. Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs. Virology 1998;247:170-7.
24. Deshpande KL, Fried VA, Ando M, Webster RG. Glycosylation affects cleavage of an H5N2 influenza virus hemagglutinin and regulates virulence. Proc Natl Acad Sci U S A 1987;84:36-40.
25. Vigerust DJ, Shepherd VL. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol 2007;15:211-8.
26. Skehel JJ, Stevens DJ, Daniels RS, Douglas AR, Knossow M, Wilson IA, et al. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proc Natl Acad Sci U S A 1984;81:1779-83.
27. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE Jr, Wilson IA. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 2010;328:357-60.
28. Fukuyama S, Kawaoka Y. The pathogenesis of influenza virus infections: the contributions of virus and host factors. Curr Opin Immunol 2011;23:481-6.
29. Luo M. Influenza virus entry. Adv Exp Med Biol 2012;726:201-21.
30. Gerhard W. The role of the antibody response in influenza virus infection. Curr Top Microbiol Immunol 2001;260:171-90.
31. Okuno Y, Isegawa Y, Sasao F, Ueda S. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 1993;67:2552-8.
32. Corti D, Suguitan AL Jr, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest 2010;120:1663-73.
33. Sun S, Wang Q, Zhao F, Chen W, Li Z. Prediction of biological functions on glycosylation site migrations in human influenza H1N1 viruses. PLoS One 2012;7:e32119.
34. Das SR, Puigbò P, Hensley SE, Hurt DE, Bennink JR, Yewdell JW. Glycosylation focuses sequence variation in the influenza A virus H1 hemagglutinin globular domain. PLoS Pathog 2010;6: e1001211.
35. Das SR, Hensley SE, David A, Schmidt L, Gibbs JS, Puigbò P, et al. Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. Proc Natl Acad Sci U S A 2011;108:E1417-22.
36. Schwarz F, Aebi M. Mechanisms and principles of N-linked protein glycosylation. Curr Opin Struct Biol 2011;21:576-82.
37. Alberts B, Wilson JH, Hunt T. Molecular biology of the cell. 5th ed. New York: Garland Science; 2008.
38. Ohuchi M, Ohuchi R, Feldmann A, Klenk HD. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J Virol 1997;71:8377-84.
39. Wagner R, Wolff T, Herwig A, Pleschka S, Klenk HD. Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics. J Virol 2000;74:6316-23.
40. Tsuchiya E, Sugawara K, Hongo S, Matsuzaki Y, Muraki Y, Li ZN, et al. Effect of addition of new oligosaccharide chains to the globular head of influenza A/H2N2 virus haemagglutinin on the intracellular transport and biological activities of the molecule. J Gen Virol 2002;83(Pt 5):1137-46.
41. Vigerust DJ, Ulett KB, Boyd KL, Madsen J, Hawgood S, McCullers JA. N-linked glycosylation attenuates H3N2 influenza viruses. J Virol 2007;81:8593-600.
42. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 1982;31(2 Pt 1):417-27.
43. Reading PC, Pickett DL, Tate MD, Whitney PG, Job ER, Brooks AG. Loss of a single N-linked glycan from the hemagglutinin of influenza virus is associated with resistance to collectins and increased virulence in mice. Respir Res 2009;10:117.
44. Tate MD, Job ER, Brooks AG, Reading PC. Glycosylation of the hemagglutinin modulates the sensitivity of H3N2 influenza viruses to innate proteins in airway secretions and virulence in mice. Virology 2011;413:84-92.
45. Tate MD, Brooks AG, Reading PC. Specific sites of N-linked glycosylation on the hemagglutinin of H1N1 subtype influenza A virus determine sensitivity to inhibitors of the innate immune system and virulence in mice. J Immunol 2011;187:1884-94.
46. Rudneva IA, Ilyushina NA, Timofeeva TA, Webster RG, Kaverin NV. Restoration of virulence of escape mutants of H5 and H9 influenza viruses by their readaptation to mice. J Gen Virol 2005; 86(Pt 10):2831-8.
47. O'Donnell CD, Vogel L, Wright A, Das SR, Wrammert J, Li GM, et al. Antibody Pressure by a Human Monoclonal Antibody Targeting the 2009 Pandemic H1N1 Virus Hemagglutinin Drives the Emergence of a Virus with Increased Virulence in Mice. MBio 2012;3. pii: e00120-12.
48. Reading PC, Tate MD, Pickett DL, Brooks AG. Glycosylation as a target for recognition of influenza viruses by the innate immune system. Adv Exp Med Biol 2007;598:279-92.
49. Rogers GN, D'Souza BL. Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989;173:317-22.
50. Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 1994;205:17-23.
51. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, Wiley DC. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 1983;304:76-8.
52. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, et al. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 2000;74:8502-12.
53. Nobusawa E, Ishihara H, Morishita T, Sato K, Nakajima K. Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Virology 2000; 278:587-96.
54. Crecelius DM, Deom CM, Schulze IT. Biological properties of a hemagglutinin mutant of influenza virus selected by host cells. Virology 1984;139:164-77.
55. Deom CM, Caton AJ, Schulze IT. Host cell-mediated selection of a mutant influenza A virus that has lost a complex oligosaccharide from the tip of the hemagglutinin. Proc Natl Acad Sci U S A 1986; 83:3771-5.
56. Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, et al. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 2004;303:1838-42.
57. Wang W, Lu B, Zhou H, Suguitan AL Jr, Cheng X, Subbarao K, et al. Glycosylation at 158N of the hemagglutinin protein and receptor binding specificity synergistically affect the antigenicity and immunogenicity of a live attenuated H5N1 A/Vietnam/1203/2004 vaccine virus in ferrets. J Virol 2010;84:6570-7.
58. Gao Y, Zhang Y, Shinya K, Deng G, Jiang Y, Li Z, et al. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathog 2009;5:e1000709.
59. Wang CC, Chen JR, Tseng YC, Hsu CH, Hung YF, Chen SW, et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc Natl Acad Sci U S A 2009;106:18137-42.