Receptor specificity of influenza viruses and its alteration during interspecies transmission

Monographs in Virology

Volumn 27, Issue , 2008, Pages 134-155

  Matrosovich, Mikhail N ^a   Gambaryan, Alexandra S ^b   Klenk, Hans Dieter ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AVES; ORTHOMYXOVIRIDAE;

EID: 50549091277     PISSN: 00770965     EISSN: 16623851     Source Type: Book Series    
DOI: 10.1159/000151617     Document Type: Article

References (88)

1. Schauer R, Kamerling JP: Chemistry, biochemistry and biology of sialic acids; in Montreuil J, Vliegenthart JFG, Schachter H (eds): Glycoproteins II. New Comprehensive Biochemistry. Amsterdam, Elsevier Science, 1997, vol 29b, pp 243-402.
2. Schauer R: Sialic acids: fascinating sugars in higher animals and man. Zoology (Jena) 2004;107:49-64.
3. Kelm S, Schauer R: Sialic acids in molecular and cellular interactions. Intern Rev Cytol 1997;175:137-240.
4. Lehmann F, Tiralongo E, Tiralongo J: Sialic acid-specific lectins: occurrence, specificity and function. Cell Mol Life Sci 2006;63:1331-1354.
5. Varki A: Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 2007;446:1023-1029.
6. Suzuki Y: Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull 2005;28:399-408.
7. Matrosovich MN, Klenk H-D, Kawaoka Y: Receptor specificity, host range and pathogenicity of influenza viruses; in Kawaoka Y (ed): Influenza Virology: Current Topics. Wymondham, Caister Academic Press, 2006, pp 95-137.
8. Paulson JC: Interactions of animal viruses with cell surface receptors; in Conn M (ed): The Receptors. Orlando, Academic Press, 1985, vol 2, pp 131-219.
9. Herrler G, Hausmann J, Klenk H-D: Sialic acid as receptor determinant of ortho- andparamixoviruses; in Rosenberg A (ed): Biology of the Sialic Acids. New York, Plenum, 1995, pp 315-336.
10. Bergelson LD, Bukrinskaya AG, Prokazova NV, Shaposhnikova GI, Kocharov SL, Shevchenko VP, Kornilaeva GV, Fomina-Ageeva EV: Role of gangliosides in reception of influenza virus. Eur J Biochem 1982;128:467-474.
11. Matrosovich M, Suzuki T, Hirabayashi Y, Garten W, Webster RG, Klenk HD: Gangliosides are not essential for influenza virus infection. Glycoconj J 2006;23:107-113.
12. Skehel JJ, Wiley DC: Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 2000;69:531-569.
13. Eisen MB, Sabesan S, Skehel JJ, Wiley DC: 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.
14. Ha Y, Stevens DJ, Skehel JJ, Wiley DC: 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.
15. Ha Y, Stevens DJ, Skehel JJ, Wiley DC: X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus. Virology 2003;309:209-218.
16. Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ: The structure and receptorbinding properties of the 1918 influenza hemagglutinin. Science 2004;303:1838-1842.
17. Wang Q, Tian X, Chen X, Ma J: Structural basis for receptor specificity of influenza B virus hemagglutinin. Proc Natl Acad Sci USA 2007;104:16874-16879.
18. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992;56:152-179.
19. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA: Global patterns of influenza a virus in wild birds. Science 2006;312:384-388.
20. Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B, Osterhaus AD, Fouchier RA: Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 2007;3:e61.
21. Matrosovich M, Klenk HD: Natural and synthetic sialic acid-containing inhibitors of influenza virus receptor binding. Rev Med Virol 2003;13:85-97.
22. Rogers GN, D'Souza BL: Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989;173:317-322.
23. Connor RJ, Kawaoka Y, Webster RG, Paulson JC: Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 1994;205:17-23.
24. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y: Early alterations of receptor-binding properties of H1, H2 and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 2000;74:8502-8512.
25. 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.
26. Gambaryan AS, Tuzikov AB, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Bovin NV, Matrosovich MN: Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: nonegg-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.
27. Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA: Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997;233:224-234.
28. Matrosovich MN, Gambaryan AS, Tuzikov AB, Byramova NE, Mochalova LV, Golbraikh AA, Shenderovich MD, Finne J, Bovin NV: Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology 1993;196:111-121.
29. Matrosovich M, Zhou N, Kawaoka Y, Webster R: The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 1999;73:1146-1155.
30. Gambaryan AS, Robertson JS, Matrosovich MN: Effects of egg adaptation on the receptor-binding properties of human influenza viruses. Virology 1999;258:232-239.
31. Banks J, Speidel ES, Moore E, Plowright L, Piccirillo A, Capua I, Cordioli P, Fioretti A, Alexander DJ: Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 2001;146:963-973.
32. Campitelli L, Mogavero E, De Marco MA, Delogu M, Puzelli S, Frezza F, Facchini M, Chiapponi C, Foni E, Cordioli P, Webby R, Barigazzi G, Webster RG, Donatelli I: Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. Virology 2004;323:24-36.
33. Lin YP, Shaw M, Gregory V, Cameron K, Lim W, Klimov A, Subbarao K, Guan Y, Krauss S, Shortridge K, Webster R, Cox N, Hay A: Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci USA 2000;97:9654-9658.
34. Matrosovich MN, Krauss S, Webster RG: H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 2001;281:156-162.
35. Saito T, Lim W, Suzuki T, Suzuki Y, Kida H, Nishimura SI, Tashiro M: Characterization of a human H9N2 influenza virus isolated in Hong Kong. Vaccine 2001;20:125-133.
36. Bovin NV: Polyacrylamide-based glycoconjugates as tools in glycobiology. Glycoconj J 1998;15:431-446.
37. Gambaryan AS, Tuzikov AB, Bovin NV, Yamnikova SS, Lvov DK, Webster RG, Matrosovich MN: Differences between influenza virus receptors on target cells of duck and chicken and receptor specificity of the 1997 H5N1 chicken and human influenza viruses from Hong Kong. Avian Dis 2003;47(suppl): 1154-1160.
38. Yamnikova SS, Gambaryan AS, Tuzikov AB, Bovin NV, Matrosovich MN, Fedyakina IT, Grinev AA, Blinov VM, Lvov DK, Suarez DL, Swayne DE: Differences between HA receptor-binding sites of avian influenza viruses isolated from Laridae and Anatidae. Avian Dis 2003;47(suppl):1164-1168.
39. Gambaryan AS, Tuzikov AB, Pazynina GV, Webster RG, Matrosovich MN, Bovin NV: H5N1 chicken influenza viruses display a high binding affinity for Neu5Acα2-3Galβ1-4(6-HSO3)GlcNAc-containing receptors. Virology 2004;326:310-316.
40. Gambaryan A, Yamnikova S, Lvov D, Tuzikov A, Chinarev A, Pazynina G, Webster R, Matrosovich M, Bovin N: Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology 2005;334:276-283.
41. Gambaryan A, Tuzikov A, Pazynina G, Bovin N, Balish A, Klimov A: Evolution of the receptor binding phenotype of influenza A (H5) viruses. Virology 2006;344:432-438.
42. Gambaryan A, Webster R, Matrosovich M: Differences between influenza virus receptors on target cells of duck and chicken. Arch Virol 2002;147:1197-1208.
43. Kawaoka Y, Chambers TM, Sladen WL, Webster RG: Is the gene pool of influenza viruses in shore-birds and gulls different from that in wild ducks? Virology 1988;163:247-250.
44. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD: Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 2005;79:2814-2822.
45. Gambarian A, Tuzikov A, Chinarev A, Pazynina G, Yamnikova S, Lvov D, Bovin N, Klimov A: Receptor specificity of influenza viruses from wild ducks, gulls, poultry, and mammals. Abstracts of The European Influenza Congress II, The European Scientific Group on Influenza, Malta, October 2005, P-S06-1a.
46. Paulson JC, Blixt O, Collins BE: Sweet spots in functional glycomics. Nat Chem Biol 2006;2:238-248.
47. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA: Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 2006;312:404-410.
48. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA: Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 2006;355:1143-1155.
49. Stevens J, Blixt O, Paulson JC, Wilson IA: Glycan microarray technologies: tools to survey host specificity of influenza viruses. Nat Rev Microbiol 2006;4:857-864.
50. Ito T, Couceiro JNSS, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 1998;72:7367-7373.
51. Wan H, Perez DR: Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. Virology 2006;346:278-286.
52. Guo CT, Takahashi N, Yagi H, Kato K, Takahashi T, Yi SQ, Chen Y, Ito T, Otsuki K, Kida H, Kawaoka Y, Hidari KI, Miyamoto D, Suzuki T, Suzuki Y: The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 2007;17:713-724.
53. Gambaryan AS, Marinina VP, Solodar' TA, Bovin NV, Tuzikov AB, Pazynina GV, Iamnikova SS, L'vov DK, Klimov AI, Matrosovich MN: Different receptor specificity of influence viruses from ducks and chickens and its reflection in the composition of sialosides on host cells and mucins. Vopr Virusol 2006;51:24-32.
54. Knibbs RN, Goldstein IJ, Ratcliffe RM, Shibuya N: Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J Biol Chem 1991;266:83-88.
55. Scholtissek C, Hinshaw VS, Olsen CW: Influenza in pigs and their role as the intermediate host; in Nicholson KG, Webster RG, Hay AJ (eds): Textbook of Influenza. London, Blackwell Science, 1998, pp 137-145.
56. Gambaryan AS, Karasin AI, Tuzikov AB, Chinarev AA, Pazynina GV, Bovin NV, Matrosovich MN, Olsen CW, Klimov AI: Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Res 2005;114:15-22.
57. Mochalova L, Gambaryan A, Romanova J, Tuzikov A, Chinarev A, Katinger D, Katinger H, Egorov A, Bovin N: Receptor-binding properties of modern human influenza viruses primarily isolated in Vero and MDCK cells and chicken embryonated eggs. Virology 2003;313:473-480.
58. Kobasa D, Takada A, Shinya K, Hatte M, Halfmann P, Theriault S, Suzuki H, Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y: Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 2004;431:703-707.
59. Glaser L, Stevens J, Zamarin D, Wilson IA, Garcia-Sastre A, Tumpey TM, Basler CF, Taubenberger JK, Palese P: A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J Virol 2005;79:11533-11536.
60. Reid AH, Janczewski TA, Lourens RM, Elliot AJ, Daniels RS, Berry CL, Oxford JS, Taubenberger JK: 1918 influenza pandemic caused by highly conserved viruses with two receptor-binding variants. Emerg Infect Dis 2003;9:1249-1253.
61. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA: Structure of the undeaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 2004;303:1866-1870.
62. Rogers GN, Paulson JC: 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.
63. Vines A, Wells K, Matrosovich M, Castrucci MR, Ito T, Kawaoka Y: The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J Virol 1998;72:7626-7631.
64. Karasin AI, Brown IH, Carman S, Olsen CW: Isolation and characterization of H4N6 avian influenza viruses from pigs with pneumonia in Canada. J Virol 2000;74:9322-9327.
65. Bateman AC, Landolt GA, Karasin AI, Busch MG, Olsen CW: Amino acids 223 and 225 of H4N6 influenza virus HA determine receptor specificity and swine respiratory epithelial cell infectivity. Options for the Control of Influenza VI, Toronto, Canada, 2007, abstract P202.
66. Baum LG, Paulson JC: Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl 1990;40:S35-S38.
67. Couceiro JN, Paulson JC, Baum LG: Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 1993;29:155-165.
68. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD: Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci USA 2004;101:4620-4624.
69. Matrosovich M, Matrosovich T, Uhlendorff J, Garten W, Klenk HD: Avian-virus-like receptor specificity of the hemagglutinin impedes influenza virus replication in cultures of human airway epithelium. Virology 2007;361:384-390.
70. Thompson CI, Barclay WS, Zambon MC, Pickles RJ: Infection of human airway epithelium by human and avian strains of influenza a virus. J Virol 2006;80:8060-8068.
71. Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG, Holtzman MJ, Brody SL: Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol 2006;80:7469-7480.
72. Wan H, Perez DR: Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J Virol 2007;81:5181-5191.
73. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y: Avian flu: influenza virus receptors in the human airway. Nature 2006;440:435-436.
74. Van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T: H5N1 virus attachment to lower respiratory tract. Science 2006;312:399.
75. Van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T: Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 2007;171:1215-1223.
76. Nicholls JM, Chan MC, Chan WY, Wong HK, Cheung CY, Kwong DL, Wong MP, Chui WH, Poon LL, Tsao SW, Guan Y, Peiris JS: Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med 2007;13:147-149.
77. Yao L, Korteweg C, Hsueh W, Gu J: Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB J 2007 DOI: 10.1096/fj.06-7880com.
78. Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P: Influenza A H5N1 replication sites in humans. Emerg Infect Dis 2005;11:1036-1041.
79. Gu J, Xie Z, Gao Z, Liu J, Korteweg C, Ye J, Lau LT, Lu J, Gao Z, Zhang B, McNutt MA, Lu M, Anderson VM, Gong E, Yu AC, Lipkin WI: H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 2007;370:1137-1145.
80. De Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha dQ, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J: Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006;12:1203-1207.
81. Olofsson S, Kumlin U, Dimock K, Arnberg N: Avian influenza and sialic acid receptors: more than meets the eye? Lancet Infect Dis 2005;5:184-188.
82. Horimoto T, Kawaoka Y: Pandemic threat posed by avian influenza A viruses. Clin Microbiol Rev 2001;14:129-149.
83. Baigent SJ, McCauley JW: Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. Bioessays 2003;25:657-671.
84. Tumpey TM, Maines TR, Van Hoeven N, Glaser L, Solorzano A, Pappas C, Cox NJ, Swayne DE, Palese P, Katz JM, Garcia-Sastre A: A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 2007;315:655-659.
85. 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: Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 2006;444:378-382.
86. Shinya K, Hatta M, Yamada S, Takada A, Watanabe S, Halfmann P, Horimoto T, Neumann G, Kim JH, Lim W, Guan Y, Peiris M, Kiso M, Suzuki T, Suzuki Y, Kawaoka Y: Characterization of a human H5N1 influenza A virus isolated in 2003. J Virol 2005;79:9926-9932.
87. Auewarakul P, Suptawiwat O, Kongchanagul A, Sangma C, Suzuki Y, Ungchusak K, Louisirirotchanakul S, Lerdsamran H, Pooruk P, Thitithanyanont A, Pittayawonganon C, Guo CT, Hiramatsu H, Jampangem W, Chunsutthiwat S, Puthavathana P: An avian influenza H5N1 virus that binds to a human-type receptor. J Virol 2007;81:9950-9955.
88. Harvey R, Martin AC, Zambon M, Barclay WS: Restrictions to the adaptation of influenza a virus H5 hemagglutinin to the human host. J Virol 2004;78:502-507.