2,003
Views
22
CrossRef citations to date
0
Altmetric
Research Paper

Site-specific glycosylation profile of influenza A (H1N1) hemagglutinin through tandem mass spectrometry

, , &
Pages 508-517 | Received 14 Jun 2017, Accepted 06 Sep 2017, Published online: 17 Nov 2017

References

  • Taubenberger JK, Kash JC. Influenza Virus Evolution, Host Adaptation, and Pandemic Formation. Cell Host & Microbe. 2010;7(6):440-51. doi:10.1016/j.chom.2010.05.009
  • Nelson MI, Holmes EC. The evolution of epidemic influenza. Nat Rev Genet. 2007;8(3):196-205. doi:10.1038/nrg2053. PMID:17262054
  • Potter CW, Oxford JS. Determinants of immunity to influenza infection in man. Br Med Bull. 1979;35(1):69-75. doi:10.1093/oxfordjournals.bmb.a071545. PMID:367490
  • Mancini N, Solforosi L, Clementi N, De Marco D, Clementi M, Burioni R. A potential role for monoclonal antibodies in prophylactic and therapeutic treatment of influenza. Antiviral Res. 2011;92(1):15-26. doi:10.1016/j.antiviral.2011.07.013. PMID:21798290
  • Stohr K, Bucher D, Colgate T, Wood J. Influenza virus surveillance, vaccine strain selection, and manufacture. Methods Mol Biol. 2012;865:147-62. doi:10.1007/978-1-61779-621-0_9. PMID:22528158
  • Johansson BE, Bucher DJ, Kilbourne ED. Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J Virol. 1989;63(3):1239-46. PMID:2915381
  • Johansson BE, Moran TM, Bona CA, Popple SW, Kilbourne ED. Immunologic response to influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. II. Sequential infection of mice simulates human experience. J Immunol. 1987;139(6):2010-4. PMID:3624874
  • Virk RK, Gunalan V, Tambyah PA. Influenza infection in human host: Challenges in making a better influenza vaccine. Expert Rev Anti Infect Ther. 2016;14(4):365-75. doi:10.1586/14787210.2016.1155450. PMID:26885890
  • Sriwilaijaroen N, Suzuki Y. Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad Ser B Phys Biol Sci. 2012;88(6):226-49. doi:10.2183/pjab.88.226. PMID:22728439
  • Wang CC, Chen JR, Tseng YC, Hsu CH, Hung YF, Chen SW, Chen CM, Khoo KH, Cheng TJ, Cheng YS, et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc Natl Acad Sci U S A. 2009;106(43):18137-42. doi:10.1073/pnas.0909696106. PMID:19822741
  • Wanzeck K, Boyd KL, McCullers JA. Glycan shielding of the influenza virus hemagglutinin contributes to immunopathology in mice. Am J Respir Crit Care Med. 2011;183(6):767-73. doi:10.1164/rccm.201007-1184OC. PMID:20935106
  • Chen W, Zhong Y, Qin Y, Sun S, Li Z. The Evolutionary Pattern of Glycosylation Sites in Influenza Virus (H5N1) Hemagglutinin and Neuraminidase. PLoS ONE. 2012;7(11):e49224. doi:10.1371/journal.pone.0049224. PMID:23133677
  • Kim JI, Park MS. N-linked glycosylation in the hemagglutinin of influenza A viruses. Yonsei Med J. 2012;53(5):886-93. doi:10.3349/ymj.2012.53.5.886. PMID:22869469
  • Sun X, Jayaraman A, Maniprasad P, Raman R, Houser KV, Pappas C, Zeng H, Sasisekharan R, Katz JM, Tumpey TM. N-Linked Glycosylation of the Hemagglutinin Protein Influences Virulence and Antigenicity of the 1918 Pandemic and Seasonal H1N1 Influenza A Viruses. J Virol. 2013;87(15):8756-66. doi:10.1128/JVI.00593-13. PMID:23740978
  • de Vries RP, de Vries E, Bosch BJ, de Groot RJ, Rottier PJ, de Haan CA. The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity. Virology. 2010;403(1):17-25. doi:10.1016/j.virol.2010.03.047. PMID:20441997
  • Zhang X, Chen S, Yang D, Wang X, Zhu J, Peng D, Liu X. Role of stem glycans attached to haemagglutinin in the biological characteristics of H5N1 avian influenza virus. J Gen Virol. 2015;96(Pt 6):1248-57. doi:10.1099/vir.0.000082. PMID:25667326
  • Roberts PC, Garten W, Klenk HD. Role of conserved glycosylation sites in maturation and transport of influenza A virus hemagglutinin. J Virol. 1993;67(6):3048-60. PMID:8497042
  • Herve PL, Lorin V, Jouvion G, Da Costa B, Escriou N. Addition of N-glycosylation sites on the globular head of the H5 hemagglutinin induces the escape of highly pathogenic avian influenza A H5N1 viruses from vaccine-induced immunity. Virology. 2015;486:134-45. doi:10.1016/j.virol.2015.08.033. PMID:26433051
  • Medina RA, Stertz S, Manicassamy B, Zimmermann P, Sun X, Albrecht RA, Uusi-Kerttula H, Zagordi O, Belshe RB, Frey SE, et al. Glycosylations in the globular head of the hemagglutinin protein modulate the virulence and antigenic properties of the H1N1 influenza viruses. Sci Transl Med. 2013;5(187):187ra70. doi:10.1126/scitranslmed.3005996. PMID:23720581
  • 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(7):e22844. doi:10.1371/journal.pone.0022844. PMID:21829533
  • Tate MD, Job ER, Deng YM, Gunalan V, Maurer-Stroh S, Reading PC. Playing hide and seek: how glycosylation of the influenza virus hemagglutinin can modulate the immune response to infection. Viruses. 2014;6(3):1294-316. doi:10.3390/v6031294. PMID:24638204
  • Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE, Wilson IA. Structural basis of pre-existing immunity to the 2009 H1N1 pandemic influenza virus. Science (New York, NY). 2010;328(5976):357-60. doi:10.1126/science.1186430
  • Igarashi M, Ito K, Yoshida R, Tomabechi D, Kida H, Takada A. Predicting the Antigenic Structure of the Pandemic (H1N1) 2009 Influenza Virus Hemagglutinin. PLoS ONE. 2010;5(1):e8553. doi:10.1371/journal.pone.0008553. PMID:20049332
  • NetNGlyc. NetNGlyc 1.0 Server Available: http://www.cbs.dtu.dk/services/NetNGlyc/. Accessed 22 may, 2016.
  • Doll S, Burlingame AL. Mass spectrometry-based detection and assignment of protein posttranslational modifications. ACS Chem Biol. 2015;10(1):63-71. doi:10.1021/cb500904b. PMID:25541750
  • Thaysen-Andersen M, Packer NH. Advances in LC–MS/MS-based glycoproteomics: Getting closer to system-wide site-specific mapping of the N- and O-glycoproteome. Biochim Biophys Acta, Proteins Proteomics. 2014;1844(9):1437-52. doi:10.1016/j.bbapap.2014.05.002
  • Das SR, Hensley SE, David A, Schmidt L, Gibbs JS, Puigbò P, Ince WL, Bennink JR, Yewdell JW. Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. Proc Natl Acad Sci U S A. 2011;108(51):E1417-E22. doi:10.1073/pnas.1108754108. PMID:22106257
  • Das SR, Puigbo 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(11):e1001211. doi:10.1371/journal.ppat.1001211
  • Thaysen-Andersen M, Packer NH. Site-specific glycoproteomics confirms that protein structure dictates formation of N-glycan type, core fucosylation and branching. Glycobiology. 2012;22(11):1440-52. doi:10.1093/glycob/cws110. PMID:22798492
  • An Y, Rininger JA, Jarvis DL, Jing X, Ye Z, Aumiller JJ, Eichelberger M, Cipollo JF. Comparative Glycomics Analysis of Influenza Hemagglutinin (H5N1) Produced in Vaccine Relevant Cell Platforms. J Proteome Res. 2013;12(8):3707-20. doi:10.1021/pr400329k. PMID:23848607
  • Wei C-J, Boyington JC, Dai K, Houser KV, Pearce MB, Kong W-P, Yang Z-y, Tumpey TM, Nabel GJ. Cross-Neutralization of 1918 and 2009 Influenza Viruses: Role of Glycans in Viral Evolution and Vaccine Design. Sci Transl Med. 2010;2(24):24ra1-ra1. doi:10.1126/scitranslmed.3000799
  • 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(11):8377-84. PMID:9343193
  • Schauer R. Sialic acids as antigenic determinants of complex carbohydrates. Adv Exp Med Biol. 1988;228:47-72. doi:10.1007/978-1-4613-1663-3_2. PMID:2459931
  • Schauer R. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol. 2009;19(5):507-14. doi:10.1016/j.sbi.2009.06.003. PMID:19699080
  • Shi X, Jarvis DL. Protein N-Glycosylation in the Baculovirus-Insect Cell System. Curr drug targets. 2007;8(10):1116-25. doi:10.2174/138945007782151360. PMID:17979671
  • Mir-Shekari SY, Ashford DA, Harvey DJ, Dwek RA, Schulze IT. The glycosylation of the influenza A virus hemagglutinin by mammalian cells. A site-specific study. J Biol Chem. 1997;272(7):4027-36. doi:10.1074/jbc.272.7.4027. PMID:9020110
  • Fukuda M, Guan JL, Rose JK. A membrane-anchored form but not the secretory form of human chorionic gonadotropin-alpha chain acquires polylactosaminoglycan. J Biol Chem. 1988;263(11):5314-8. PMID:2451668
  • Soema PC, Kompier R, Amorij J-P, Kersten GFA. Current and next generation influenza vaccines: Formulation and production strategies. Eur J Phar Biopharm. 2015;94:251-63. doi:10.1016/j.ejpb.2015.05.023
  • Manini I, Domnich A, Amicizia D, Rossi S, Pozzi T, Gasparini R, Panatto D, Montomoli E. Flucelvax (Optaflu) for seasonal influenza. Expert Rev Vaccines. 2015;14(6):789-804. doi:10.1586/14760584.2015.1039520. PMID:25968069
  • Yang LP. Recombinant trivalent influenza vaccine (flublok((R))): A review of its use in the prevention of seasonal influenza in adults. Drugs. 2013;73(12):1357-66. doi:10.1007/s40265-013-0103-6. PMID:23928902
  • Zhang S. Comparative Characterization of the Glycosylation Profiles of an Influenza Hemagglutinin Produced in Plant and Insect Hosts. Proteomics. 2012;12(8):1269-88. doi:10.1002/pmic.201100474. PMID:22577028
  • Butler M, Spearman M. The choice of mammalian cell host and possibilities for glycosylation engineering. Curr Opin Biotechnol. 2014;30:107-12. doi:10.1016/j.copbio.2014.06.010. PMID:25005678
  • Squires RB, Noronha J, Hunt V, García-Sastre A, Macken C, Baumgarth N, Suarez D, Pickett BE, Zhang Y, Larsen CN, et al. Influenza Research Database: An integrated bioinformatics resource for influenza research and surveillance. Influenza Other Respir Viruses. 2012;6(6):404-16. doi:10.1111/j.1750-2659.2011.00331.x. PMID:22260278

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.