Bat-Derived Influenza Hemagglutinin H17 Does Not Bind Canonical Avian or Human Receptors and Most Likely Uses a Unique Entry Mechanism

Cell Reports

Volumn 3, Issue 3, 2013, Pages 769-778

  Sun, Xiaoman ^a,c   Shi, Yi ^a,b   Lu, Xishan ^a,e   He, Jianhua ^f   Gao, Feng ^d   Yan, Jinghua ^a   Qi, Jianxun ^a   Gao, George F ^a,b,c,g  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d INSTITUTE OF BIOPHYSICS   (China)

^e CHINA AGRICULTURAL UNIVERSITY   (China)

^f SHANGHAI INSTITUTE OF APPLIED PHYSICS   (China)

^g CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; SIALIC ACID; SIALIC ACID RECEPTOR; TRYPSIN; UNCLASSIFIED DRUG;

ARTICLE; BAT; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; INFLUENZA VIRUS A; INFLUENZA VIRUS A H17N10; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; RECEPTOR BINDING; THERMOSTABILITY; VIRUS ENTRY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHICKENS; CHIROPTERA; CRYSTALLOGRAPHY, X-RAY; DOGS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN DENATURATION; RECEPTORS, VIRUS;

AVES; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 84875807120     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.01.025     Document Type: Article

References (43)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Air G.M. Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc. Natl. Acad. Sci. USA 1981, 78:7639-7643.
3. Bullough P.A., Hughson F.M., Skehel J.J., Wiley D.C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 1994, 371:37-43.
4. 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.
5. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50:760-763. Collaborative Computational Project, Number 4.
6. Corti D., Voss J., Gamblin S.J., Codoni G., Macagno A., Jarrossay D., Vachieri S.G., Pinna D., Minola A., Vanzetta F., et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011, 333:850-856.
7. Eisen M.B., Sabesan S., Skehel J.J., Wiley D.C. Binding of the influenza A virus to cell-surface receptors: structures of five hemagglutinin-sialyloligosaccharide complexes determined by X-ray crystallography. Virology 1997, 232:19-31.
8. Ekiert D.C., Bhabha G., Elsliger M.A., Friesen R.H., Jongeneelen M., Throsby M., Goudsmit J., Wilson I.A. Antibody recognition of a highly conserved influenza virus epitope. Science 2009, 324:246-251.
9. Ekiert D.C., Friesen R.H., Bhabha G., Kwaks T., Jongeneelen M., Yu W., Ophorst C., Cox F., Korse H.J., Brandenburg B., et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 2011, 333:843-850.
10. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
11. Gambaryan A.S., Tuzikov A.B., Piskarev V.E., Yamnikova S.S., Lvov D.K., Robertson J.S., Bovin N.V., Matrosovich M.N. Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6'?-sialyl(N-acetyllactosamine). Virology 1997, 232:345-350.
12. Gamblin S.J., Skehel J.J. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J. Biol. Chem. 2010, 285:28403-28409.
13. Gao G.F., Sun Y. It is not just AIV: from avian to swine-origin influenza virus. Sci. China Life Sci. 2010, 53:151-153.
14. Garten W., Klenk H.D. Understanding influenza virus pathogenicity. Trends Microbiol. 1999, 7:99-100.
15. Guan Y., Vijaykrishna D., Bahl J., Zhu H., Wang J., Smith G.J. The emergence of pandemic influenza viruses. Protein Cell 2010, 1:9-13.
16. Harrison S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:690-698.
17. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. PROCHECK: a Program to Check the Stereochemical Quality of Protein Structures. J. Appl. Crystallogr. 1993, 26:283-291.
18. Li Q., Sun X., Li Z., Liu Y., Vavricka C.J., Qi J., Gao G.F. Structural and functional characterization of neuraminidase-like molecule N10 derived from bat influenza A virus. Proc. Natl. Acad. Sci. USA 2012, 109:18897-18902.
19. Liu D., Liu X., Yan J., Liu W.J., Gao G.F. Interspecies transmission and host restriction of avian H5N1 influenza virus. Sci. China C Life Sci. 2009, 52:428-438.
20. Lu X., Shi Y., Gao F., Xiao H., Wang M., Qi J., Gao G.F. Insights into avian influenza virus pathogenicity: the hemagglutinin precursor HA0 of subtype H16 has an alpha-helix structure in its cleavage site with inefficient HA1/HA2 cleavage. J. Virol. 2012, 86:12861-12870.
21. Medina R.A., García-Sastre A. Influenza A viruses: new research developments. Nat. Rev. Microbiol. 2011, 9:590-603.
22. Mühlebach M.D., Mateo M., Sinn P.L., Prüfer S., Uhlig K.M., Leonard V.H., Navaratnarajah C.K., Frenzke M., Wong X.X., Sawatsky B., et al. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 2011, 480:530-533.
23. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
24. Naniche D., Varior-Krishnan G., Cervoni F., Wild T.F., Rossi B., Rabourdin-Combe C., Gerlier D. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J. Virol. 1993, 67:6025-6032.
25. Neumann G., Noda T., Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 2009, 459:931-939.
26. Nobusawa E., Aoyama T., Kato H., Suzuki Y., Tateno Y., Nakajima K. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 1991, 182:475-485.
27. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
28. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:1373-1382.
29. Rosenthal P.B., Zhang X., Formanowski F., Fitz W., Wong C.H., Meier-Ewert H., Skehel J.J., Wiley D.C. Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus. Nature 1998, 396:92-96.
30. Sauter N.K., Bednarski M.D., Wurzburg B.A., Hanson J.E., Whitesides G.M., Skehel J.J., Wiley D.C. Hemagglutinins from two influenza virus variants bind to sialic acid derivatives with millimolar dissociation constants: a 500-MHz proton nuclear magnetic resonance study. Biochemistry 1989, 28:8388-8396.
31. Skehel J.J., Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 2000, 69:531-569.
32. Skehel J.J., Bayley P.M., Brown E.B., Martin S.R., Waterfield M.D., White J.M., Wilson I.A., Wiley D.C. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. USA 1982, 79:968-972.
33. Sui J., Hwang W.C., Perez S., Wei G., Aird D., Chen L.M., Santelli E., Stec B., Cadwell G., Ali M., et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 2009, 16:265-273.
34. Sun Y., Shi Y., Zhang W., Li Q., Liu D., Vavricka C., Yan J., Gao G.F. In silico characterization of the functional and structural modules of the hemagglutinin protein from the swine-origin influenza virus A (H1N1)-2009. Sci. China Life Sci. 2010, 53:633-642.
35. Takemoto D.K., Skehel J.J., Wiley D.C. A surface plasmon resonance assay for the binding of influenza virus hemagglutinin to its sialic acid receptor. Virology 1996, 217:452-458.
36. Tatsuo H., Ono N., Tanaka K., Yanagi Y. SLAM (CDw150) is a cellular receptor for measles virus. Nature 2000, 406:893-897.
37. Tong S., Li Y., Rivailler P., Conrardy C., Castillo D.A., Chen L.M., Recuenco S., Ellison J.A., Davis C.T., York I.A., et al. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 2012, 109:4269-4274.
38. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56:152-179.
39. Weis W., Brown J.H., Cusack S., Paulson J.C., Skehel J.J., Wiley D.C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 1988, 333:426-431.
40. Xuan C., Shi Y., Qi J., Zhang W., Xiao H., Gao G.F. Structural vaccinology: structure-based design of influenza A virus hemagglutinin subtype-specific subunit vaccines. Protein Cell 2011, 2:997-1005.
41. Zhang W., Qi J., Shi Y., Li Q., Gao F., Sun Y., Lu X., Lu Q., Vavricka C.J., Liu D., et al. Crystal structure of the swine-origin A (H1N1)-2009 influenza A virus hemagglutinin (HA) reveals similar antigenicity to that of the 1918 pandemic virus. Protein Cell 2010, 1:459-467.
42. Zhang X., Lu G., Qi J., Li Y., He Y., Xu X., Shi J., Zhang C.W., Yan J., Gao G.F. Structure of measles virus hemagglutinin bound to its epithelial receptor nectin-4. Nat. Struct. Mol. Biol. 2013, 20:67-72.
43. Zhu X., Yang H., Guo Z., Yu W., Carney P.J., Li Y., Chen L.M., Paulson J.C., Donis R.O., Tong S., et al. Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc. Natl. Acad. Sci. USA 2012, 109:18903-18908.