Molecular characterizations of surface proteins hemagglutinin and neuraminidase from recent H5Nx avian influenza viruses

Journal of Virology

Volumn 90, Issue 12, 2016, Pages 5770-5784

  Yang, Hua ^a   Carney, Paul J ^a   Mishin, Vasiliy P ^a   Guo, Zhu ^a   Chang, Jessie C ^a   Wentworth, David E ^a   Gubareva, Larisa V ^a   Stevens, James ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE ANTIGEN; VIRUS HEMAGGLUTININ; VIRUS SIALIDASE; HEMAGGLUTININ, AVIAN INFLUENZA A VIRUS; INFLUENZA VIRUS HEMAGGLUTININ; SIALIDASE;

ARTICLE; AVIAN INFLUENZA VIRUS; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; GEOGRAPHIC DISTRIBUTION; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H5N1); INFLUENZA A VIRUS (H5N2); INFLUENZA A VIRUS (H5N6); INFLUENZA A VIRUS (H5N8); MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS IDENTIFICATION; ANIMAL; ASIA; CANADA; CHEMISTRY; ENZYMOLOGY; EPIDEMIC; EUROPE; GENETIC REASSORTMENT; GENETICS; HUMAN; INFLUENZA; INFLUENZA IN BIRDS; METABOLISM; NORTH AMERICA; PHYLOGENY; POULTRY; VIROLOGY; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; ASIA; CANADA; DISEASE OUTBREAKS; EUROPE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H5N2 SUBTYPE; INFLUENZA A VIRUS, H5N8 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; NEURAMINIDASE; NORTH AMERICA; PHYLOGENY; POULTRY; REASSORTANT VIRUSES;

EID: 84971472473     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00180-16     Document Type: Article

References (75)

1. Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, Shortridge KF, Cheung PT, To WK, Ho ET, Sung R, Cheng AF. 1998. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467-471. http://dx.doi.org/10.1016/S0140-6736(98)01182-9.
2. WHO. 17 July 2015. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003-2015. World Health Organization, Geneva, Switzerland. http://www.who.int/influenza/human_animal_interface/EN_GIP_20150717cumulativeNumberH5N1cases.pdf?ua=1.
3. Vijaykrishna D, Bahl J, Riley S, Duan L, Zhang JX, Chen H, Peiris JS, Smith GJ, Guan Y. 2008. Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4:e1000161. http://dx.doi.org/10.1371/journal.ppat.1000161.
4. Smith GJ, Donis RO, World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization H5 Evolution Working Group. 2015. Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza Other Respir Viruses 9:271-276. http://dx.doi.org/10.1111/irv.12324.
5. Pan M, Gao R, Lv Q, Huang S, Zhou Z, Yang L, Li X, Zhao X, Zou X, Tong W, Mao S, Zou S, Bo H, Zhu X, Liu L, Yuan H, Zhang M, Wang D, Li Z, Zhao W, Ma M, Li Y, Li T, Yang H, Xu J, Zhou L, Zhou X, Tang W, Song Y, Chen T, Bai T, Zhou J, Wang D, Wu G, Li D, Feng Z, Gao GF, Wang Y, He S, Shu Y. 2015. Human infection with a novel highly pathogenic avian influenza A (H5N6) virus: virological and clinical findings. J Infect http://dx.doi.org/10.1016/j.jinf.2015.06.009.
6. World Organisation for Animal Health. 2014. Summary of immediate notifications and follow-ups-2014. Highly pathogenic avian influenza. OIE, Paris, France. http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/Immsummary.
7. Ip HS, Torchetti MK, Crespo R, Kohrs P, DeBruyn P, Mansfield KG, Baszler T, Badcoe L, Bodenstein B, Shearn-Bochsler V, Killian ML, Pedersen JC, Hines N, Gidlewski T, DeLiberto T, Sleeman JM. 2015. Novel Eurasian highly pathogenic avian influenza A H5 viruses in wild birds, Washington, USA, 2014. Emerg Infect Dis 21:886-890. http://dx.doi.org/10.3201/eid2105.142020.
8. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol Rev 56:152-179.
9. Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA. 1997. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of theHAreceptor-binding site. Virology 233:224-234. http://dx.doi.org/10.1006/viro.1997.8580.
10. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, Wiley DC. 1983. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304:76-78. http://dx.doi.org/10.1038/304076a0.
11. Liu C, Eichelberger MC, Compans RW, Air GM. 1995. Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. J Virol 69:1099-1106.
12. Moscona A. 2005. Neuraminidase inhibitors for influenza. N Engl J Med 353:1363-1373. http://dx.doi.org/10.1056/NEJMra050740.
13. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870. http://dx.doi.org/10.1126/science.1093373.
14. Kuhnel K, Jarchau T, Wolf E, Schlichting I, Walter U, Wittinghofer A, Strelkov SV. 2004. The VASP tetramerization domain is a right-handed coiled coil based on a 15-residue repeat. Proc Natl Acad Sci U S A 101: 17027-17032. http://dx.doi.org/10.1073/pnas.0403069101.
15. Xu X, Zhu X, Dwek R, Stevens J, Wilson I. 2008. Structural characterization of the 1918 influenza H1N1 neuraminidase. J Virol 82:10493-10501. http://dx.doi.org/10.1128/JVI.00959-08.
16. Chayen NE. 2007. Optimization techniques for automation and high throughput. Methods Mol Biol 363:175-190. http://dx.doi.org/10.1007/978-1-59745-209-0_9.
17. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. http://dx.doi.org/10.1016/S0076-6879(97)76066-X.
18. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ. 2005. Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61:458-464. http://dx.doi.org/10.1107/S0907444905001617.
19. Shore DA, Yang H, Balish AL, Shepard SS, Carney PJ, Chang JC, Davis CT, Donis RO, Villanueva JM, Klimov AI, Stevens J. 2013. Structural and antigenic variation among diverse clade 2 H5N1 viruses. PLoS One 8:e75209. http://dx.doi.org/10.1371/journal.pone.0075209.
20. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158.
21. CCP4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763. http://dx.doi.org/10.1107/S0907444994003112.
22. Winn MD, Isupov MN, Murshudov GN. 2001. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57:122-133. http://dx.doi.org/10.1107/S0907444900014736.
23. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221. http://dx.doi.org/10.1107/S0907444909052925.
24. Vavricka CJ, Li Q, Wu Y, Qi J, Wang M, Liu Y, Gao F, Liu J, Feng E, He J, Wang J, Liu H, Jiang H, Gao GF. 2011. Structural and functional analysis of laninamivir and its octanoate prodrug reveals group specific mechanisms for influenza NA inhibition. PLoS Pathog 7:e1002249. http://dx.doi.org/10.1371/journal.ppat.1002249.
25. Sun X, Li Q, Wu Y, Wang M, Liu Y, Qi J, Vavricka CJ, Gao GF. 2014. Structure of influenza virus N7: the last piece of the neuraminidase "jigsaw" puzzle. J Virol 88:9197-9207. http://dx.doi.org/10.1128/JVI.00805-14.
26. Yang H, Nguyen HT, Carney PJ, Guo Z, Chang JC, Jones J, Davis CT, Villanueva JM, Gubareva LV, Stevens J. 2015. Structural and functional analysis of surface proteins from an A(H3N8) influenza virus isolated from New England harbor seals. J Virol 89:2801-2812. http://dx.doi.org/10.1128/JVI.02723-14.
27. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, III, Snoeyink J, Richardson JS, Richardson DC. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35:W375-383. http://dx.doi.org/10.1093/nar/gkm216.
28. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA. 2006. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355:1143-1155. http://dx.doi.org/10.1016/j.jmb.2005.11.002.
29. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312:404-410. http://dx.doi.org/10.1126/science.1124513.
30. Yang H, Carney P, Stevens J. 2010. Structure and receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr 2:RRN1152.
31. Yang H, Carney PJ, Donis RO, Stevens J. 2012. Structure and receptor complexes of the hemagglutinin from a highly pathogenic H7N7 influenza virus. J Virol 86:8645-8652. http://dx.doi.org/10.1128/JVI.00281-12.
32. Yang H, Chen LM, Carney PJ, Donis RO, Stevens J. 2010. Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog 6:e1001081. http://dx.doi.org/10.1371/journal.ppat.1001081.
33. Potier M, Mameli L, Belisle M, Dallaire L, Melancon SB. 1979. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-DN-acetylneuraminate) substrate. Anal Biochem 94:287-296. http://dx.doi.org/10.1016/0003-2697(79)90362-2.
34. Klenk HD, Garten W. 1994. Host cell proteases controlling virus pathogenicity. Trends Microbiol 2:39-43. http://dx.doi.org/10.1016/0966-842X(94)90123-6.
35. Hulse-Post DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Govorkova EA, Krauss S, Scholtissek C, Puthavathana P, Buranathai C, Nguyen TD, Long HT, Naipospos TS, Chen H, Ellis TM, Guan Y, Peiris JS, Webster RG. 2005. Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc Natl Acad Sci U S A 102:10682-10687. http://dx.doi.org/10.1073/pnas.0504662102.
36. Ha Y, Stevens DJ, Skehel JJ, Wiley DC. 2001. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci U S A 98:11181-11186. http://dx.doi.org/10.1073/pnas.201401198.
37. Ha Y, Stevens DJ, Skehel JJ, Wiley DC. 2003. X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus. Virology 309:209-218. http://dx.doi.org/10.1016/S0042-6822(03)00068-0.
38. Liu J, Stevens DJ, Haire LF, Walker PA, Coombs PJ, Russell RJ, Gamblin SJ, Skehel JJ. 2009. Structures of receptor complexes formed by hemagglutinins from the Asian influenza pandemic of 1957. Proc Natl Acad Sci U S A 106:17175-17180. http://dx.doi.org/10.1073/pnas.0906849106.
39. Russell RJ, Gamblin SJ, Haire LF, Stevens DJ, Xiao B, Ha Y, Skehel JJ. 2004. H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology 325:287-296. http://dx.doi.org/10.1016/j.virol.2004.04.040.
40. Russell RJ, Kerry PS, Stevens DJ, Steinhauer DA, Martin SR, Gamblin SJ, Skehel JJ. 2008. Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci U S A 105:17736-17741. http://dx.doi.org/10.1073/pnas.0807142105.
41. Wilson IA, Skehel JJ, Wiley DC. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289: 366-373. http://dx.doi.org/10.1038/289366a0.
42. Lu X, Qi J, Shi Y, Wang M, Smith DF, Heimburg-Molinaro J, Zhang Y, Paulson JC, Xiao H, Gao GF. 2013. Structure and receptor binding specificity of hemagglutinin H13 from avian influenza A virus H13N6. J Virol 87:9077-9085. http://dx.doi.org/10.1128/JVI.00235-13.
43. Lu X, Shi Y, Gao F, Xiao H, Wang M, Qi J, Gao GF. 2012. Insights into avian influenza virus pathogenicity: the hemagglutinin precursor HA0 of subtype H16 has an α-helix structure in its cleavage site with inefficient HA1/HA2 cleavage. J Virol 86:12861-12870. http://dx.doi.org/10.1128/JVI.01606-12.
44. Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ. 2004. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838-1842. http://dx.doi.org/10.1126/science.1093155.
45. Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, Wiley DC. 1998. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95:409-417. http://dx.doi.org/10.1016/S0092-8674(00)81771-7.
46. Shakin-Eshleman SH, Spitalnik SL, Kasturi L. 1996. The amino acid at the X position of an Asn-X-Ser sequon is an important determinant of N-linked core-glycosylation efficiency. J Biol Chem 271:6363-6366. http://dx.doi.org/10.1074/jbc.271.11.6363.
47. Brownlee GG, Fodor E. 2001. The predicted antigenicity of the haemagglutinin of the 1918 Spanish influenza pandemic suggests an avian origin. Philos Trans R Soc Lond B Biol Sci 356:1871-1876. http://dx.doi.org/10.1098/rstb.2001.1001.
48. Wiley DC, Wilson IA, Skehel JJ. 1981. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373-378. http://dx.doi.org/10.1038/289373a0.
49. Velkov T, Ong C, Baker MA, Kim H, Li J, Nation RL, Huang JX, Cooper MA, Rockman S. 2013. The antigenic architecture of the hemagglutinin of influenza H5N1 viruses. Mol Immunol 56:705-719. http://dx.doi.org/10.1016/j.molimm.2013.07.010.
50. Anonymous. 2015. Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly Epidemiol Rec 90:109-120.
51. Neumann G, Kawaoka Y. 2006. Host range restriction and pathogenicity in the context of influenza pandemic. Emerg Infect Dis 12:881-886. http://dx.doi.org/10.3201/eid1206.051336.
52. Connor RJ, Kawaoka Y, Webster RG, Paulson JC. 1994. Receptor specificity in human, avian, and equineH2andH3influenza virus isolates. Virology 205:17-23. http://dx.doi.org/10.1006/viro.1994.1615.
53. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y. 2000. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74:8502-8512. http://dx.doi.org/10.1128/JVI.74.18.8502-8512.2000.
54. Russell CA, Fonville JM, Brown AE, Burke DF, Smith DL, James SL, Herfst S, van Boheemen S, Linster M, Schrauwen EJ, Katzelnick L, Mosterin A, Kuiken T, Maher E, Neumann G, Osterhaus AD, Kawaoka Y, Fouchier RA, Smith DJ. 2012. The potential for respiratory droplettransmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336:1541-1547. http://dx.doi.org/10.1126/science.1222526.
55. Yang ZY, Wei CJ, Kong WP, Wu L, Xu L, Smith DF, Nabel GJ. 2007. Immunization by avian H5 influenza hemagglutinin mutants with altered receptor binding specificity. Science 317:825-828. http://dx.doi.org/10.1126/science.1135165.
56. Wang W, Lu B, Zhou H, Suguitan AL, Jr, Cheng X, Subbarao K, Kemble G, Jin H. 2010. 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 84:6570-6577. http://dx.doi.org/10.1128/JVI.00221-10.
57. Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, 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 LF, Stevens DJ, Russell RJ, Gamblin SJ, Skehel JJ, Kawaoka Y. 2006. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444:378-382. http://dx.doi.org/10.1038/nature05264.
58. Chen LM, Blixt O, Stevens J, Lipatov AS, Davis CT, Collins BE, Cox NJ, Paulson JC, Donis RO. 2012. In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 422:105-113. http://dx.doi.org/10.1016/j.virol.2011.10.006.
59. Yang H, Carney PJ, Chang JC, Villanueva JM, Stevens J. 2013. Structural analysis of the hemagglutinin from the recent 2013 H7N9 influenza virus. J Virol 87:12433-12446. http://dx.doi.org/10.1128/JVI.01854-13.
60. USDA Animal and Plant Health Inspection Service. 15 June 2015. Epidemiologic and other analyses of HPAI-affected poultry flocks. APHIS, Riverdale Park, MD. https://www.aphis.usda.gov/animal_health/animal_dis_spec/poultry/downloads/Epidemiologic-Analysis-June-15-2015.pdf.
61. Varghese JN, Laver WG, Colman PM. 1983. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 303: 35-40. http://dx.doi.org/10.1038/303035a0.
62. Baker AT, Varghese JN, Laver WG, Air GM, Colman PM. 1987. Threedimensional structure of neuraminidase of subtype N9 from an avian influenza virus. Proteins 2:111-117. http://dx.doi.org/10.1002/prot.340020205.
63. Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, Blackburn GM, Hay AJ, Gamblin SJ, Skehel JJ. 2006. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443:45-49. http://dx.doi.org/10.1038/nature05114.
64. Wang M, Qi J, Liu Y, Vavricka CJ, Wu Y, Li Q, Gao GF. 2011. Influenza A virus N5 neuraminidase has an extended 150-cavity. J Virol 85:8431-8435. http://dx.doi.org/10.1128/JVI.00638-11.
65. Burmeister WP, Ruigrok RW, Cusack S. 1992. The 2.2 Å resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J 11:49-56.
66. Li Q, Qi J, Wu Y, Kiyota H, Tanaka K, Suhara Y, Ohrui H, Suzuki Y, Vavricka CJ, Gao GF. 2013. Functional and structural analysis of influenza virus neuraminidase N3 offers further insight into the mechanisms of oseltamivir resistance. J Virol 87:10016-10024. http://dx.doi.org/10.1128/JVI.01129-13.
67. Zhu X, Yang H, Guo Z, Yu W, Carney PJ, Li Y, Chen LM, Paulson JC, Donis RO, Tong S, Stevens J, Wilson IA. 2012. Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc Natl Acad Sci U S A 109:18903-18908. http://dx.doi.org/10.1073/pnas.1212579109.
68. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO. 2013. New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657. http://dx.doi.org/10.1371/journal.ppat.1003657.
69. Air GM. 2012. Influenza neuraminidase. Influenza Other Respir Viruses 6:245-256. http://dx.doi.org/10.1111/j.1750-2659.2011.00304.x.
70. Air GM, Laver WG. 1989. The neuraminidase of influenza virus. Proteins 6:341-356. http://dx.doi.org/10.1002/prot.340060402.
71. Chong AK, Pegg MS, Taylor NR, von Itzstein M. 1992. Evidence for a sialosyl cation transition-state complex in the reaction of sialidase from influenza virus. Eur J Biochem 207:335-343. http://dx.doi.org/10.1111/j.1432-1033.1992.tb17055.x.
72. Burmeister WP, Cusack S, Ruigrok RW. 1994. Calcium is needed for the thermostability of influenza B virus neuraminidase. J Gen Virol 75(Part 2):381-388. http://dx.doi.org/10.1099/0022-1317-75-2-381.
73. Smith BJ, Huyton T, Joosten RP, McKimm-Breschkin JL, Zhang JG, Luo CS, Lou MZ, Labrou NE, Garrett TP. 2006. Structure of a calciumdeficient form of influenza virus neuraminidase: implications for substrate binding. Acta Crystallogr D Biol Crystallogr 62:947-952. http://dx.doi.org/10.1107/S0907444906020063.
74. Janakiraman MN, White CL, Laver WG, Air GM, Luo M. 1994. Structure of influenza virus neuraminidase B/Lee/40 complexed with sialic acid and a dehydro analog at 1.8-Å resolution: implications for the catalytic mechanism. Biochemistry 33:8172-8179. http://dx.doi.org/10.1021/bi00193a002.
75. DeLano WL. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, Palo Alto, CA. www.pymol.org.