Hemagglutinin mutation D222N of the 2009 pandemic H1N1 influenza virus alters receptor specificity without affecting virulence in mice

Virus Research

Volumn 189, Issue , 2014, Pages 79-86

  Kong, Weili ^a   Liu, Linqing ^a   Wang, Yu ^a   Gao, Huijie ^a   Wei, Kai ^a   Sun, Honglei ^a   Sun, Yipeng ^a   Liu, Jinhua ^a   Ma, Guangpeng ^b   Pu, Juan ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b CHINA RURAL TECHNOLOGY DEVELOPMENT CENTER   (China)

Author keywords

2009 A (H1N1); D222N; HA receptor binding site; Pathogenicity

Indexed keywords

CYTOKINE; INFLUENZA VIRUS HEMAGGLUTININ; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ RECEPTOR; VIRUS RECEPTOR; H1N1 VIRUS HEMAGGLUTININ; MUTANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELL CULTURE; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; LUNG ALVEOLUS; MOUSE; NONHUMAN; PANDEMIC INFLUENZA; PATHOGENICITY; PRIORITY JOURNAL; RECEPTOR BINDING; RECOMBINANT D222N VIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS MUTANT; VIRUS MUTATION; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS VIRULENCE; WESTERN BLOTTING; AMINO ACID SUBSTITUTION; ANIMAL; BAGG ALBINO MOUSE; BODY WEIGHT; CELL LINE; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; LUNG; METABOLISM; MISSENSE MUTATION; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; VIROLOGY; VIRULENCE; VIRUS ATTACHMENT; VIRUS LOAD;

AMINO ACID SUBSTITUTION; ANIMALS; BODY WEIGHT; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLAMMATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; MICE, INBRED BALB C; MUTANT PROTEINS; MUTATION, MISSENSE; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL LOAD; VIRULENCE; VIRUS ATTACHMENT;

EID: 84905978656     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.05.001     Document Type: Article

References (42)

1. Abed Y., Pizzorno A., Hamelin M.E., Leung A., Joubert P., Couture C., Kobasa D., Boivin G. The 2009 pandemic H1N1 D222G hemagglutinin mutation alters receptor specificity and increases virulence in mice but not in ferrets. J. Infect. Dis. 2011, 204(7):1008-1016.
2. Baldanti F., Campanini G., Piralla A., Rovida F., Braschi A., Mojoli F., Iotti G., Belliato M., Conaldi P.G., Arcadipane A., Pariani E., Zanetti A., Minoli L., Emmi V. Severe outcome of influenza A/H1N1/09v infection associated with 222G/N polymorphisms in the haemagglutinin: a multicentre study. Clin. Microbiol. Infect. 2010, 17:1166-1179.
3. Belser J.A., Jayaraman A., Raman R., Pappas C., Zeng H., Cox N.J., Katz J.M., Sasisekharan R., Tumpey T.M. Effect of D222G mutation in the hemagglutinin protein on receptor binding, pathogenesis and transmissibility of the 2009 pandemic H1N1 influenza virus. PLoS One 2011, 6:e25091.
4. Berdal J.E., Mollnes T.E., Wæhre T., Olstad O.K., Halvorsen B., Ueland T., Laake J.H., Furuseth M.T., Maagaard A., Kjekshus H., Aukrust P., Jonassen C.M. Excessive innate immune response and mutant D222G/N in severe A (H1N1) pandemic influenza. J. Infect. 2011, 63(4):308-316.
5. Chen L.M., Rivailler P., Hossain J., Carney P., Balish A., Perry I., Davis C.T., Garten R., Shu B., Xu X., Klimov A., Paulson J.C., Cox N.J., Swenson S., Stevens J., Vincent A., Gramer M., Donis R.O. Receptor specificity of subtype H1 influenza A viruses isolated from swine and humans in the United States. Virology 2011, 412(2):401-410.
6. Childs R.A., Palma A.S., Wharton S., Matrosovich T., Liu Y., Chai W., Campanero-Rhodes M.A., Zhang Y., Eickmann M., Kiso M., Hay A., Matrosovich M., Feizi T. Receptor-binding specificity of pandemic influenza A (H1N1) 2009 virus determined by carbohydrate microarray. Nat. Biotechnol. 2009, 27:797-799.
7. Chutinimitkul S., Herfst S., Steel J., Lowen A.C., Ye J., van Riel D., Schrauwen E.J., Bestebroer T.M., Koel B., Burke D.F., Sutherland-Cash K.H., Whittleston C.S., Russell C.A., Wales D.J., Smith D.J., Jonges M., Meijer A., Koopmans M., Rimmelzwaan G.F., Kuiken T., Osterhaus A.D., García-Sastre A., Perez D.R., Fouchier R.A. Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A(H1N1) virus affects receptor binding. J. Virol. 2010, 84:11802-11813.
8. Cortese A., Baldanti F., Tavazzi E., Carnevale L., Minoli L., Lozza A., Marchioni E. Guillain-Barré syndrome associated with the D222E variant of the 2009 pandemic influenza A (H1N1) virus: case report and review of the literature. J. Neurol. Sci. 2012, 312(1-2):173-176.
9. Dawood F.S., Jain S., Finelli L., Shaw M.W., Lindstrom S., Garten R.J., Gubareva L.V., Xu X., Bridges C.B., Uyeki T.M. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N. Engl. J. Med. 2009, 360:2605-2615.
10. Fraser C., Donnelly C.A., Cauchemez S., Hanage W.P., Van Kerkhove M.D., Hollingsworth T.D., Griffin J., Baggaley R.F., Jenkins H.E., Lyons E.J., Jombart T., Hinsley W.R., Grassly N.C., Balloux F., Ghani A.C., Ferguson N.M., Rambaut A., Pybus O.G., Lopez-Gatell H., Alpuche-Aranda C.M., Chapela I.B., Zavala E.P., Guevara D.M., Checchi F., Garcia E., Hugonnet S., Roth C. Pandemic potential of a strain of influenza A (H1N1): early findings. Science 2009, 324:1557-1561. WHO Rapid Pandemic Assessment Collaboration.
11. Glinsky Gennadi V. Genomic analysis of pandemic (H1N1) 2009 reveals association of increasing disease severity with emergence of novel hemagglutinin mutations. Cell. Cycle 2010, 9(5):958-970.
12. Gilca R., De Serres G., Boulianne N., Ouhoummane N., Papenburg J., Douville-Fradet M., Fortin É., Dionne M., Boivin G., Skowronski D.M. Risk factors for hospitalization and severe outcomes of 2009 pandemic H1N1 influenza in Quebec, Canada. Influenza Other Respir. Viruses 2011, 5(4):247-255.
13. Houng H.S., Garner J., Zhou Y., Lyons A., Kuschner R., Deye G., St Clair K., Douce R.W., Chicaiza W., Blair P.J., Myers C.A., Burke R.L., Sanchez J.L., Williams M., Halsey E.S. Emergent 2009 influenza A(H1N1) viruses containing HA D222N mutation associated with severe clinical outcomes in the Americas. J. Clin. Virol. 2012, 53(1):12-15.
14. Ilyushina N.A., Khalenkov A.M., Seiler J.P., Forrest H.L., Bovin N.V., Marjuki H., Barman S., Webster R.G., Webby R.J. Adaptation of pandemic H1N1 influenza viruses in mice. J. Virol. 2010, 84:8607-8616.
15. Jackson D., Hossain M.J., Hickman D., Perez D.R., Lamb R.A. A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:4381-4386.
16. Jagger B.W., Wise H.M., Kash J.C., Walters K.A., Wills N.M., Xiao Y.L., Dunfee R.L., Schwartzman L.M., Ozinsky A., Bell G.L., Dalton R.M., Lo A., Efstathiou S., Atkins J.F., Firth A.E., Taubenberger J.K., Digard P. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 2012, 337(6091):199-204.
17. Kilander A., Rykkvin R., Dudman S.G., Hungnes O. Observed association between the HA1 mutation D222G in the 2009 pandemic influenza A(H1N1) virus and severe clinical outcome, Norway 2009-2010. Euro Surveill. 2010, 15(9):pii=19498.
18. L'vov D.K., Burtseva E.I., Prilipov A.G., Bogdanova V.S., Shchelkanov M.Iu., Bovin N.V., Samokhvalov E.I., Fediakina I.T., Deriabin P.G., Kolobukhina L.V., Shtyria IuA, Shevchenko E.S., Malyshev N.A., Merkulova L.N., Bazarova M.V., Maslov A.I., Ishchenko N.M., Iskhakova E.A., Al'khovskiǐ S.V., Grebennikova T.V., Sadykova G.K., L'vov D.N., Zhuravleva M.M., Iamnikova S.S., Shliapnikova O.V., Poglazov A.B., Trushakova S.V., Lavrishcheva V.V., Aristova V.A., Proshina E.S., Vereshchagin N.N., Kuz'michev A.G., Iashkulov K.B., Dzhambinov S.D., Bushkieva B.Ts., Eliseeva S.M., Bystrakov S.I., Sokolova I.A., Dzhaparidzhe N.I., Ledenev I.u.A., Rosolovskiǐ A.P., Gareev R.V., Boldyreva V.V., Anan'ev V.I.u., Baranov N.I., Gorelikov V.N., Garbuz IuA, Reznik V.I., Ivanov L.I., Zdanovskaia N.N., Sergeeva N.M., Podolianko I.A., Elovskiǐ O.V., Gromova M.A., Kalaeva E.E., Grigor'ev S.N., Eremeeva I.u.V, Dovgal' M.V., Fedelesh I.I.u., Sakharova E.A., Burtnik V.I., Avdoshina L.N., Shapiro N.P., Maslov D.V., Ianovich V.A., Ott V.A., Lebedev G.B. A possible association of fatal pneumonia with mutations of pandemic influenza A/H1N1 sw1 virus in the receptor-binding site of the HA1 subunit. Vopr. Virusol. 2010, 55(4):4-9.
19. Ledesma J., Pozo F., Pérez Ruiz M., Navarro J.M., Piñeiro L., Montes M., Pérez Castro S., Suárez Fernández J., García Costa J., Fernández M., Galán J.C., Cuevas M.T., Casas I., Pérez Breña P. Substitutions in position 222 of haemagglutinin of pandemic influenza A (H1N1) 2009 viruses in Spain. J. Clin. Virol. 2011, 51:75-78. Spanish Influenza Surveillance System (SISS).
20. Liu Y., Childs R.A., Matrosovich T., Wharton S., Palma A.S., Chai W., Daniels R., Gregory V., Uhlendorff J., Kiso M., Klenk H.D., Hay A., Feizi T., Matrosovich M. Altered receptor specificity and cell tropism of D222G hemagglutinin mutants isolated from fatal cases of pandemic A(H1N1) 2009 influenza virus. J. Virol. 2010, 84(22):12069-12074.
21. Mak G.C., Au K.W., Tai L.S., Chuang K.C., Cheng K.C., Shiu T.C., Lim W. Association of D222G substitution in haemagglutinin of 2009 pandemic influenza A (H1N1) with severe disease. Euro Surveill. 2010, 15(14):pii=19534.
22. Matrosovich M., Tuzikov A., Bovin N., Gambaryan A., Klimov A., Castrucci M.R., Donatelli I., Kawaoka Y. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J. Virol. 2000, 74:8502-8512.
23. Miller R.S., MacLean A.R., Gunson R.N., Carman W.F. Occurrence of haemagglutinin mutation D222G in pandemic infuenza A(H1N1) infected patients in the West of Scotland, United Kingdom, 2009-10. Euro Surveill. 2010, 15(16):pii=19546.
24. Mosby L.G., Rasmussen S.A., Jamieson D.J. 2009 Pandemic influenza A (H1N1) in pregnancy: a systematic review of the literature. Am. J. Obstet. Gynecol. 2011, 205:10-18.
25. O'Donnell C.D., Vogel L., Wright A., Das S.R., Wrammert J., Li G.M., McCausland M., Zheng N.Y., Yewdell J.W., Ahmed R., Wilson P.C., Subbarao K. 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, 293(3).
26. Palacios G., Hornig M., Cisterna D., Savji N., Bussetti A.V., Kapoor V., Hui J., Tokarz R., Briese T., Baumeister E., Lipkin W.I. Streptococcus pneumoniae coinfection is correlated with the severity of H1N1 pandemic influenza. PLoS One 2009, 4:e8540.
27. Selleri M., Piralla A., Rozera G., Giombini E., Bartolini B., Abbate I., Campanini G., Rovida F., Dossena L., Capobianchi M.R., Baldanti F. Detection of haemagglutinin D222 polymorphisms in influenza A(H1N1)pdm09-infected patients by ultra-deep pyrosequencing. Clin. Microbiol. Infect. 2012, 10.1111/j.1469-0691.2012.03984.x.
28. Sheng Z.M., Chertow D.S., Ambroggio X., McCall S., Przygodzki R.M., Cunningham R.E., Maximova O.A., Kash J.C., Morens D.M., Taubenberger J.K. Autopsy series of 68 cases dying before and during the 1918 influenza pandemic peak. Proc. Nat. Acad. Sci. U.S.A. 2011, 108(39):16416-16421.
29. Song M.S., Pascua P.N., Choi Y.K. Virulence of pandemic (H1N1) 2009 influenza A polymerase reassortant viruses. Virulence 2011, 2(5):422-426.
30. Steel J., Lowen A.C., Mubareka S., Palese P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 2009, 5(1):e1000252.
31. Stevens J., Blixt O., Glaser L., Taubenberger J.K., Palese P., Paulson J.C., Wilson I.A. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 2006, 355(5):1143-1155.
32. Subbarao E.K., London W., Murphy B.R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J. Virol. 1993, 67:1761-1764.
33. Trifonov V., Khiabanian H., Rabadan R. Geographic dependence, surveillance, and origins of the 2009 influenza A (H1N1) virus. N. Engl. J. Med. 2009, 361:115-119.
34. Wu C., Cheng X., Wang X., Lv X., Yang F., Liu T., Fang S., Zhang R., Jinquan C. Clinical and molecular characteristics of the 2009 pandemic influenza H1N1 infection with severe or fatal disease from 2009 to 2011 in Shenzhen, China. J. Med. Virol. 2013, 85(3):405-412.
35. Xu R., McBride R., Nycholat C.M., Paulson J.C., Wilson I.A. Structural characterization of the hemagglutinin receptor specificity from the 2009 H1N1 influenza pandemic. J. Virol. 2012, 86(2):982-990.
36. Yang H., Carney P., Stevens J. Structure and receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr. 2010, 222:RRN1152.
37. Ye J., Sorrell E.M., Cai Y., Shao H., Xu K., Pena L., Hickman D., Song H., Angel M., Medina R.A., Manicassamy B., Garcia-Sastre A., Perez D.R. Variations in the hemagglutinin of the 2009 H1N1 pandemic virus: potential for strains with altered virulence phenotype?. PLoS Pathog. 2010, 146(10):e1001145.
38. Yen H.L., Aldridge J.R., Boon A.C., Ilyushina N.A., Salomon R., Hulse-Post D.J., Marjuki H., Franks J., Boltz D.A., Bush D., Lipatov A.S., Webby R.J., Rehg J.E., Webster R.G. Changes in H5N1 influenza virus hemagglutinin receptor binding domain affect systemic spread. Proc. Nat. Acad. Sci. U.S.A. 2009, 6106(1):286-291.
39. Zamarin D., Ortigoza M.B., Palese P. Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J. Virol. 2006, 80:7976-7983.
40. Zhao X., Sun Y., Pu J., Fan L., Shi W., Hu Y., Yang J., Xu Q., Wang J., Hou D., Ma G., Liu J. Characterization of an artificial swine-origin influenza virus with the same gene combination as H1N1/2009 virus: a genesis clue of pandemic strain. PLoS One 2011, 6(7):e22091.
41. Zheng B., Chan K.H., Zhang A.J., Zhou J., Chan C.C., Poon V.K., Zhang K., Leung V.H., Jin D.Y., Woo P.C., Chan J.F., To K.K., Chen H., Yuen K.Y. D225G mutation in hemagglutinin of pandemic influenza H1N1 (2009) virus enhances virulence in mice. Exp. Biol. Med. 2010, 235:981-988.
42. Zhu W., Zhu Y., Qin K., Yu Z., Gao R., Yu H., Zhou J., Shu Y. Mutations in polymerase genes enhanced the virulence of 2009 pandemic H1N1 influenza virus in mice. PLoS One 2012, 7(3):e33383.