Insertion of a multibasic cleavage motif into the hemagglutinin of a low-pathogenic avian influenza H6N1 virus induces a highly pathogenic phenotype

Journal of Virology

Volumn 84, Issue 16, 2010, Pages 7953-7960

  Munster, Vincent J ^a   Schrauwen, Eefje J A ^a   De Wit, Emmie ^a,b   Van Den Brand, Judith M A ^a   Bestebroer, Theo M ^a   Herfst, Sander ^a   Rimmelzwaan, Guus F ^a   Osterhaus, Albert D M E ^a   Fouchier, Ron A M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; PROTEIN HA; TRYPSIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVIAN INFLUENZA VIRUS; CHICKEN; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VIRUS; INFLUENZA VIRUS H6N1; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN MOTIF; VIRUS REPLICATION; VIRUS VIRULENCE;

ANIMAL STRUCTURES; ANIMALS; BINDING SITES; CELL LINE; CHICKENS; DOGS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNOHISTOCHEMISTRY; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; MICROSCOPY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; POULTRY DISEASES; RECOMBINATION, GENETIC; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL LOAD; VIRULENCE; VIRULENCE FACTORS;

AVES; AVIAN INFLUENZA VIRUS; GALLUS GALLUS; INFLUENZA A VIRUS;

EID: 77954985098     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00449-10     Document Type: Article

References (47)

1. Abolnik, C., B. Z. Londt, R. J. Manvell, W. Shell, J. Banks, G. H. Gerdes, G. Akol, and I. H. Brown. 2009. Characterisation of a highly pathogenic influenza A virus of subtype H5N2 isolated from ostriches in South Africa in 2004. Influenza Other Respi. Viruses 3:63-68.
2. Alexander, D. J. 2003. Report on avian influenza in the Eastern Hemisphere during 1997-2002. Avian Dis. 47:792-797.
3. Alexander, D. J. 2000. A review of avian influenza in different bird species. Vet. Microbiol. 74:3-13.
4. Banks, J., E. S. Speidel, E. Moore, L. Plowright, A. Piccirillo, I. Capua, P. Cordioli, A. Fioretti, and D. J. Alexander. 2001. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch. Virol. 146:963-973.
5. Bosch, F. X., W. Garten, H. D. Klenk, and R. Rott. 1981. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of Avian influenza viruses. Virology 113:725-735.
6. Capua, I., and D. J. Alexander. 2004. Avian influenza: recent developments. Avian Pathol. 33:393-404.
7. Capua, I., F. Mutinelli, S. Marangon, and D. J. Alexander. 2000. H7N1 avian influenza in Italy (1999 to 2000) in intensively reared chickens and turkeys. Avian Pathol. 29:537-543.
8. Cheung, C. L., D. Vijaykrishna, G. J. D. Smith, X. H. Fan, J. X. Zhang, J. Bahl, L. Duan, K. Huang, H. Tai, J. Wang, L. L. M. Poon, J. S. M. Peiris, H. Chen, and Y. Guan. 2007. Establishment of influenza a virus (H6N1) in minor poultry species in southern China. J. Virol. 81:10402-10412.
9. de Jong, J. C., E. C. Claas, A. D. Osterhaus, R. G. Webster, and W. L. Lim. 1997. A pandemic warning? Nature 389:554.
10. de Wit, E., M. I. Spronken, T. M. Bestebroer, G. F. Rimmelzwaan, A. D. Osterhaus, and R. A. Fouchier. 2004. Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res. 103:155-161.
11. Duckert, P., S. Brunak, and N. Blom. 2004. Prediction of proprotein convertase cleavage sites. Protein Eng. Des Sel. 17:107-112.
12. Fouchier, R. A., V. Munster, A. Wallensten, T. M. Bestebroer, S. Herfst, D. Smith, G. F. Rimmelzwaan, B. Olsen, and A. D. Osterhaus. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79:2814-2822.
13. Garten, W., M. Vey, R. Ohuchi, M. Ohuchi, and H. D. Klenk. 1991. Modification of the cleavage activation of the influenza virus hemagglutinin by site-specific mutagenesis. Behring Inst. Mitt. 89:12-22.
14. Horimoto, T., and Y. Kawaoka. 1995. Molecular changes in virulent mutants arising from avirulent avian influenza viruses during replication in 14-day-old embryonated eggs. Virology 206:755-759.
15. Horimoto, T., and Y. Kawaoka. 1994. Reverse genetics provides direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian influenza A virus. J. Virol. 68:3120-3128.
16. Hossain, M. J., D. Hickman, and D. R. Perez. 2008. Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens. PLoS One 3:e3170.
17. Kawaoka, Y. 1991. Structural features influencing hemagglutinin cleavability in a human influenza A virus. J. Virol. 65:1195-1201.
18. Kawaoka, Y., C. W. Naeve, and R. G. Webster. 1984. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 139:303-316.
19. Khatchikian, D., M. Orlich, and R. Rott. 1989. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus. Nature 340:156-157.
20. Kido, H., Y. Okumura, E. Takahashi, H. Y. Pan, S. Wang, J. Chida, T. Q. Le, and M. Yano. 2008. Host envelope glycoprotein processing proteases are indispensable for entry into human cells by seasonal and highly pathogenic avian influenza viruses. J. Mol. Genet. Med. 3:167-175.
21. Lee, C. W., D. E. Swayne, J. A. Linares, D. A. Senne, and D. L. Suarez. 2005. H5N2 avian influenza outbreak in Texas in 2004: the first highly pathogenic strain in the United States in 20 years? J. Virol. 79:11412-11421.
22. Londt, B. Z., J. Banks, and D. J. Alexander. 2007. Highly pathogenic avian influenza viruses with low virulence for chickens in in vivo tests. Avian Pathol. 36:347-350.
23. Makarova, N. V., H. Ozaki, H. Kida, R. G. Webster, and D. R. Perez. 2003. Replication and transmission of influenza viruses in Japanese quail. Virology 310:8-15.
24. Munster, V. J., C. Baas, P. Lexmond, T. M. Bestebroer, J. Guldemeester, W. E. P. Beyer, E. de Wit, M. Schutten, G. F. Rimmelzwaan, A. D. M. E. Osterhaus, and R. A. M. Fouchier. 2009. Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J. Clin. Microbiol. 47:666-673.
25. Munster, V. J., C. Baas, P. Lexmond, J. Waldenstrom, A. Wallensten, T. Fransson, G. F. Rimmelzwaan, W. E. Beyer, M. Schutten, B. Olsen, A. D. Osterhaus, and R. A. Fouchier. 2007. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 3:e61.
26. Ohuchi, R., M. Ohuchi, W. Garten, and H. D. Klenk. 1991. Human influenza virus hemagglutinin with high sensitivity to proteolytic activation. J. Virol. 65:3530-3537.
27. OIE. 2009. Avian influenza. Manual of diagnostic tests and Vaccines for terrestrial animals 2009. OIE, Paris, France. http://www.oie.int/Eng./Normes/ Mmanual/2008/pdf/2.03.04-AI.pdf:1-20.
28. Perdue, M. L., J. Crawford, M. Garcia, J. Latimer, and D. Swayne. 2003. Occurrence and possible mechanisms of cleavage-site insertions in the avian influenza hemagglutinin gene. Avian Dis. 47:182-193.
29. Perdue, M. L., M. Garcia, D. Senne, and M. Fraire. 1997. Virulence-associated sequence duplication at the hemagglutinin cleavage site of avian influenza viruses. Virus Res. 49:173-186.
30. Perez, D. R., W. Lim, J. P. Seiler, G. Yi, M. Peiris, K. F. Shortridge, and R. G. Webster. 2003. Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. J. Virol. 77:3148-3156.
31. Perkins, L. E. L., and D. E. Swayne. 2001. Pathobiology of A/Chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Vet. Pathol. 38:149-164.
32. Remacle, A. G., S. A. Shiryaev, E. S. Oh, P. Cieplak, A. Srinivasan, G. Wei, R. C. Liddington, B. I. Ratnikov, A. Parent, R. Desjardins, R. Day, J. W. Smith, M. Lebl, and A. Y. Strongin. 2008. Substrate cleavage analysis of furin and related proprotein convertases. A comparative study. J. Biol. Chem. 283:20897-20906.
33. Senne, D. A. 2003. Avian influenza in the Western Hemisphere including the Pacific Islands and Australia. Avian Dis. 47:798-805.
34. Sorrell, E. M., and D. R. Perez. 2007. Adaptation of influenza A/Mallard/Potsdam/178-4/83 H2N2 virus in Japanese quail leads to infection and transmission in chickens. Avian Dis. 51:264-268.
35. Stech, O., J. Veits, S. Weber, D. Deckers, D. Schroer, T. W. Vahlenkamp, A. Breithaupt, J. Teifke, T. C. Mettenleiter, and J. Stech. 2009. Acquisition of a polybasic hemagglutinin cleavage site by a low-pathogenic avian influenza virus is not sufficient for immediate transformation into a highly pathogenic strain. J. Virol. 83:5864-5868.
36. Steensels, M., S. Van Borm, M. Boschmans, and T. van den Berg. 2007. Lethality and molecular characterization of an HPAI H5N1 virus isolated from eagles smuggled from Thailand into Europe. Avian Dis. 51:401-407.
37. Suarez, D. L., D. A. Senne, J. Banks, I. H. Brown, S. C. Essen, C. W. Lee, R. J. Manvell, C. Mathieu-Benson, V. Moreno, J. C. Pedersen, B. Panigrahy, H. Rojas, E. Spackman, and D. J. Alexander. 2004. Recombination resulting in virulence shift in avian influenza outbreak, Chile. Emerg. Infect. Dis. 10:693-699.
38. Swayne, D. E. 2007. Understanding the complex pathobiology of high pathogenicity avian influenza viruses in birds. Avian Dis. 51:242-249.
39. Swayne, D. E., and R. D. Slemons. 2008. Using mean infectious dose of high-and low-pathogenicity avian influenza viruses originating from wild duck and poultry as one measure of infectivity and adaptation to poultry. Avian Dis. 52:455-460.
40. van Riel, D., J. M. van den Brand, V. J. Munster, T. M. Besteboer, R. A. Fouchier, A. D. Osterhaus, and T. Kuiken. 2009. Pathology and virus distribution in chickens naturally infected with highly pathogenic avian influenza A virus (H7N7) during the 2003 outbreak in The Netherlands. Vet. Pathol. 46:971-976.
41. Vey, M., M. Orlich, S. Adler, H. D. Klenk, R. Rott, and W. Garten. 1992. Hemagglutinin activation of pathogenic avian influenza viruses of serotype H7 requires the protease recognition motif R-X-K/R-R. Virology 188:408-413.
42. Webby, R. J., D. R. Perez, J. S. Coleman, Y. Guan, J. H. Knight, E. A. Govorkova, L. R. McClain-Moss, J. S. Peiris, J. E. Rehg, E. I. Tuomanen, and R. G. Webster. 2004. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 363:1099-1103.
43. Webster, R. G., W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179.
44. Webster, R. G., and R. Rott. 1987. Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell 50:665-666.
45. Wood, G. W., J. W. McCauley, J. B. Bashiruddin, and D. J. Alexander. 1993. Deduced amino acid sequences at the haemagglutinin cleavage site of avian influenza A viruses of H5 and H7 subtypes. Arch. Virol. 130:209-217.
46. Wood, G. W., G. Parsons, and D. J. Alexander. 1995. Replication of influenza A viruses of high and low pathogenicity for chickens at different sites in chickens and ducks following intranasal inoculation. Avian Pathol. 24:545-551.
47. Woolcock, P. R., D. L. Suarez, and D. Kuney. 2003. Low-pathogenicity avian influenza virus (H6N2) in chickens in California, 2000-02. Avian Dis. 47:872-881.