Changes in the hemagglutinin of H5N1 viruses during human infection - Influence on receptor binding

Virology

Volumn 447, Issue 1-2, 2013, Pages 326-337

  Crusat, Martin ^a,b,k   Liu, Junfeng ^c,l   Palma, Angelina S ^d,e   Childs, Robert A ^d   Liu, Yan ^d   Wharton, Stephen A ^c   Lin, Yi Pu ^c   Coombs, Peter J ^c,m   Martin, Stephen R ^c   Matrosovich, Mikhail ^f   Chen, Zi ^c,n   Stevens, David J ^c   Hien, Vo Minh ^g   Thanh, Tran Tan ^a   Nhu, Le Nguyen Truc ^a   Nguyet, Lam Anh ^g   Ha, Do Quang ^a   van Doorn, H Rogier ^a   Hien, Tran Tinh ^g   Conradt, Harald S ^h   Kiso, Makoto ⁱ   Gamblin, Steve J ^c   Chai, Wengang ^d   Skehel, John J ^c   Hay, Alan J ^c   Farrar, Jeremy ^a,j   De Jong, Menno D ^a,b   Feizi, Ten ^d   more..

^a OXFORD UNIVERSITY CLINICAL RESEARCH UNIT   (Viet Nam)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^f PHILIPPS UNIVERSITY MARBURG   (Germany)

^g UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^h GlycoThera GmbH   (Germany)

ⁱ GIFU UNIVERSITY   (Japan)

^j NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^k Instituto de Salud Carlos III   (Spain)

^l CHINA AGRICULTURAL UNIVERSITY   (China)

^m MEDICAL RESEARCH COUNCIL   (United Kingdom)

ⁿ CENTRAL SOUTH UNIVERSITY   (China)

more..

Author keywords

Biolayer interferometry; Carbohydrate microarray; H5N1 influenza infection; Hemagglutination assays; Hemagglutinin; Hemagglutinin X ray crystal structure; Pyrosequencing; Receptor binding; Receptor specificity; Synthetic sialylglycopolymers

Indexed keywords

COPOLYMER; INFLUENZA VIRUS HEMAGGLUTININ; OLIGOSACCHARIDE; SIALIC ACID; SOLUBLE SIALYLGLYCOPOLYMER; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CRYSTALLOGRAPHY; ERYTHROCYTE; GUINEA PIG; HEMAGGLUTINATION; HORSE; HUMAN; HUMAN CELL; INFLUENZA VIRUS A H5N1; MDCK CELL; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR BINDING; STRUCTURE ANALYSIS; VIRUS MUTANT; VIRUS RECOMBINANT;

AVES; INFLUENZA A VIRUS;

EID: 84886397294     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.08.010     Document Type: Article

References (49)

1. Auewarakul P., Suptawiwat O., Kongchanagul A., Sangma C., Suzuki Y., Ungchusak K., Louisirirotchanakul S., Lerdsamran H., Pooruk P., Thitithanyanont A., Pittayawonganon C., Guo C.T., Hiramatsu H., Jampangern W., Chunsutthiwat S., Puthavathana P. An avian influenza H5N1 virus that binds to a human-type receptor. J. Virol. 2007, 81:9950-9955.
2. Beigel J.H., Farrar J., Han A.M., Hayden F.G., Hyer R., de Jong M.D., Lochindarat S., Nguyen T.K., Nguyen T.H., Tran T.H., Nicoll A., Touch S., Yuen K.Y. Avian influenza A (H5N1) infection in humans. N. Engl. J Med. 2005, 353:1374-1385.
3. Blasco R., Moss B. Selection of recombinant vaccinia viruses on the basis of plaque formation. Gene 1995, 158:157-162.
4. Bovin N.V., Korchagina E.Y., Zemlyanukhina T.V., Byramova N.E., Galanina O.E., Zemlyakov A.E., Ivanov A.E., Zubov V.P., Mochalova L.V. Synthesis of polymeric neoglycoconjugates based on N-substituted polyacrylamides. Glycoconjug. J. 1993, 10:142-151.
5. Chen J., Lee K.H., Steinhauer D.A., Stevens D.J., Skehel J.J., Wiley D.C. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 1998, 95:409-417.
6. Chen L.M., Blixt O., Stevens J., Lipatov A.S., Davis C.T., Collins B.E., Cox N.J., Paulson J.C., Donis R.O. In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 2012, 422:105-113.
7. 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.
8. Connor R.J., Kawaoka Y., Webster R.G., Paulson J.C. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 1994, 205:17-23.
9. de Jong M.D., Bach V.C., Phan T.Q., Vo M.H., Tran T.T., Nguyen B.H., Beld M., Le T.P., Truong H.K., Nguyen V.V., Tran T.H., Do Q.H., Farrar J. Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N. Engl. J. Med. 2005, 352:686-691.
10. de Jong M.D., Simmons C.P., Thanh T.T., Hien V.M., Smith G.J., Chau T.N., Hoang D.M., Chau N.V., Khanh T.H., Dong V.C., Qui P.T., Cam B.V., Ha d.Q., Guan Y., Peiris J.S., Chinh N.T., Hien T.T., Farrar J. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 2006, 12:1203-1207.
11. de Jong M.D., Tran T.T., Truong H.K., Vo M.H., Smith G.J., Nguyen V.C., Bach V.C., Phan T.Q., Do Q.H., Guan Y., Peiris J.S., Tran T.H., Farrar J. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N. Engl. J. Med. 2005, 353:2667-2672.
12. Do A.H., van Doorn H.R., Nghiem M.N., Bryant J.E., Hoang T.H., Do Q.H., Van T.L., Tran T.T., Wills B., Nguyen V.C., Vo M.H., Vo C.K., Nguyen M.D., Farrar J., Tran T.H., de Jong M.D. Viral etiologies of acute respiratory infections among hospitalized Vietnamese children in Ho Chi Minh City, 2004-2008. PLoS One 2011, 6:e18176.
13. Gambaryan A.S., Tuzikov A.B., Pazynina G.V., Webster R.G., Matrosovich M.N., Bovin N.V. H5N1 chicken influenza viruses display a high binding affinity for Neu5Acalpha2-3Galbeta1-4(6-HSO3)GlcNAc-containing receptors. Virology 2004, 326:310-316.
14. Glaser L., Stevens J., Zamarin D., Wilson I.A., Garcia-Sastre A., Tumpey T.M., Basler C.F., Taubenberger J.K., Palese P. A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J. Virol. 2005, 79:11533-11536.
15. Ha Y., Stevens D.J., Skehel J.J., Wiley D.C. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc. Natl. Acad. Sci. USA 2001, 98:11181-11186.
16. Ha Y., Stevens D.J., Skehel J.J., Wiley D.C. H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J. 2002, 21:865-875.
17. Hatta M., Gao P., Halfmann P., Kawaoka Y. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 2001, 293:1840-1842.
18. Herfst S., Schrauwen E.J., Linster M., Chutinimitkul S., de W.E., Munster V.J., Sorrell E.M., Bestebroer T.M., Burke D.F., Smith D.J., Rimmelzwaan G.F., Osterhaus A.D., Fouchier R.A. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012, 336:1534-1541.
19. Hoffmann E., Neumann G., Kawaoka Y., Hobom G., Webster R.G. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. USA 2000, 97:6108-6113.
20. Imai M., Watanabe T., Hatta M., Das S.C., Ozawa M., Shinya K., Zhong G., Hanson A., Katsura H., Watanabe S., Li C., Kawakami E., Yamada S., Kiso M., Suzuki Y., Maher E.A., Neumann G., Kawaoka Y. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012, 486:420-428.
21. Ito T., Suzuki Y., Mitnaul L., Vines A., Kida H., Kawaoka Y. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 1997, 227:493-499.
22. Ito T., Suzuki Y., Takada A., Kawamoto A., Otsuki K., Masuda H., Yamada M., Suzuki T., Kida H., Kawaoka Y. Differences in sialic acid-galactose linkages in the chicken egg amnion and allantois influence human influenza virus receptor specificity and variant selection. J. Virol. 1997, 71:3357-3362.
23. Le Q.M., Sakai-Tagawa Y., Ozawa M., Ito M., Kawaoka Y. Selection of H5N1 influenza virus PB2 during replication in humans. J. Virol. 2009, 83:5278-5281.
24. Le V.T., Phan T.Q., Do Q.H., Nguyen B.H., Lam Q.B., Bach V., Truong H., Tran T.H., Nguyen V., Tran T., Vo M., Tran V.T., Schultsz C., Farrar J., van Doorn H.R., de Jong M.D. Viral etiology of encephalitis in children in southern Vietnam: results of a one-year prospective descriptive study. PLoS Negl. Trop. Dis. 2010, 4:e854.
25. Li K.S., Guan Y., Wang J., Smith G.J., Xu K.M., Duan L., Rahardjo A.P., Puthavathana P., Buranathai C., Nguyen T.D., Estoepangestie A.T., Chaisingh A., Auewarakul P., Long H.T., Hanh N.T., Webby R.J., Poon L.L., Chen H., Shortridge K.F., Yuen K.Y., Webster R.G., Peiris J.S. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 2004, 430:209-213.
26. Lin Y.P., Xiong X., Wharton S.A., Martin S.R., Coombs P.J., Vachieri S., Christodoulou E., Walker P.A., Liu J., Skehel J.J., Gamblin S.J., Hay A., Daniels R.S., McCauley J.W. Evolution of the receptor binding properties of the influenza A(H3N2) haemagglutinin. Proc. Natl. Acad. Sci. USA. 2012, 109:21474-21479.
27. 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, 84:12069-12074.
28. Manz B., Matrosovich M., Bovin N., Schwemmle M. A polymorphism in the hemagglutinin of the human isolate of a highly pathogenic H5N1 influenza virus determines organ tropism in mice. J. Virol. 2010, 84:8316-8321.
29. Matrosovich M., Matrosovich T., Carr J., Roberts N.A., Klenk H.D. Overexpression of the alpha-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J. Virol. 2003, 77:8418-8425.
30. Matrosovich M., Matrosovich T., Uhlendorff J., Garten W., Klenk H.D. Avian-virus-like receptor specificity of the hemagglutinin impedes influenza virus replication in cultures of human airway epithelium. Virology 2007, 361:384-390.
31. 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.
32. Matrosovich M.N., Gambaryan A.S. Solid-phase assays of receptor-binding specificity. Methods Mol. Biol. 2012, 865:71-94.
33. Medeiros R., Escriou N., Naffakh N., Manuguerra J.C., van der Werf S. Hemagglutinin residues of recent human A(H3N2) influenza viruses that contribute to the inability to agglutinate chicken erythrocytes. Virology 2001, 289:74-85.
34. Rogers G.N., D'Souza B.L. Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989, 173:317-322.
35. Rogers G.N., Paulson J.C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127:361-373.
36. Shinya K., Hamm S., Hatta M., Ito H., Ito T., Kawaoka Y. PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 2004, 320:258-266.
37. Skehel J.J., Schild G.C. The polypeptide composition of influenza A viruses. Virology 1971, 44:396-408.
38. 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:e1000252.
39. 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, 355:1143-1155.
40. Stevens J., Blixt O., Paulson J.C., Wilson I.A. Glycan microarray technologies: tools to survey host specificity of influenza viruses. Nat. Rev. Microbiol. 2006, 4:857-864.
41. Tang D.J., Lam Y.M., Siu Y.L., Lam C.H., Chu S.L., Peiris J.S., Buchy P., Nal B., Bruzzone R. A single residue substitution in the receptor-binding domain of H5N1 hemagglutinin is critical for packaging into pseudotyped lentiviral particles. PLoS One 2012, 7:e43596.
42. Tran T.H., Nguyen T.L., Nguyen T.D., Luong T.S., Pham P.M., Nguyen V.C., Pham T.S., Vo C.D., Le T.Q., Ngo T.T., Dao B.K., Le P.P., Nguyen T.T., Hoang T.L., Cao V.T., Le T.G., Nguyen D.T., Le H.N., Nguyen K.T., Le H.S., Le V.T., Christiane D., Tran T.T., Menno d.J., Schultsz C., Cheng P., Lim W., Horby P., Farrar J. Avian influenza A (H5N1) in 10 patients in Vietnam. N. Engl. J. Med. 2004, 350:1179-1188.
43. Tumpey T.M., Maines T.R., Van H.N., Glaser L., Solorzano A., Pappas C., Cox N.J., Swayne D.E., Palese P., Katz J.M., Garcia-Sastre A. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 2007, 315:655-659.
44. Wang C.C., Chen J.R., Tseng Y.C., Hsu C.H., Hung Y.F., Chen S.W., Chen C.M., Khoo K.H., Cheng T.J., Cheng Y.S., Jan J.T., Wu C.Y., Ma C., Wong C.H. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc. Natl. Acad. Sci. USA 2009, 106:18137-18142.
45. Watanabe Y., Ibrahim M.S., Ellakany H.F., Kawashita N., Mizuike R., Hiramatsu H., Sriwilaijaroen N., Takagi T., Suzuki Y., Ikuta K. Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog. 2011, 7:e1002068.
46. WHO, 2012. Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1) Reported to WHO. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/.
47. Wood J.M., Robertson J.S. From lethal virus to life-saving vaccine: developing inactivated vaccines for pandemic influenza. Nat. Rev. Microbiol. 2004, 2:842-847.
48. Xiong X., Coombs P.J., Martin S.R., Liu J., Xiao H., McCauley J.W., Locher K., Walker P.A., Collins P.J., Kawaoka Y., Skehel J.J., Gamblin S.J. Receptor binding by a ferret-transmissible H5 avian influenza virus. Nature 2013, 497:392-396.
49. Yamada S., Suzuki Y., Suzuki T., Le M.Q., Nidom C.A., Sakai-Tagawa Y., Muramoto Y., Ito M., Kiso M., Horimoto T., Shinya K., Sawada T., Kiso M., Usui T., Murata T., Lin Y., Hay A., Haire L.F., Stevens D.J., Russell R.J., Gamblin S.J., Skehel J.J., Kawaoka Y. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 2006, 444:378-382.