H9N2 influenza virus acquires intravenous pathogenicity on the introduction of a pair of di-basic amino acid residues at the cleavage site of the hemagglutinin and consecutive passages in chickens

Virology Journal

Volumn 8, Issue , 2011, Pages

  Soda, Kosuke ^a   Asakura, Shingo ^a   Okamatsu, Masatoshi ^a   Sakoda, Yoshihiro ^a   Kida, Hiroshi ^a,b,c  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HEMAGGLUTININ; TRYPSIN; INFLUENZA VIRUS HEMAGGLUTININ;

AIR SAC; ARTICLE; AVIAN INFLUENZA VIRUS; CELL STRAIN; CHICKEN; INFLUENZA VIRUS A H9N2; INOCULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; VIRUS VIRULENCE; AMINO ACID SEQUENCE; ANIMAL; AVIAN INFLUENZA; BIRD DISEASE; CELL LINE; CHEMISTRY; DOG; GENE EXPRESSION REGULATION; GENETICS; INFLUENZA VIRUS A H5N1; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; PROTEIN PROCESSING; VIROLOGY; VIRUS CULTURE;

ANIMALIA; AVES; AVIAN INFLUENZA VIRUS; GALLUS GALLUS; ORTHOMYXOVIRIDAE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL LINE; CHICKENS; DOGS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; POULTRY DISEASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERIAL PASSAGE;

EID: 79751528740     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-8-64     Document Type: Article

References (44)

1. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. RA Fouchier V Munster A Wallensten TM Bestebroer S Herfst D Smith GF Rimmelzwaan B Olsen AD Osterhaus, J Virol 2005 79 2814 2822 10.1128/JVI.79.5.2814-2822.2005 15709000 (Pubitemid 40270559)
2. The evolution of H5N1 influenza viruses in ducks in southern China. H Chen G Deng Z Li G Tian Y Li P Jiao L Zhang Z Liu RG Webster K Yu, Proc Natl Acad Sci USA 2004 101 10452 10457 10.1073/pnas.0403212101 15235128 (Pubitemid 38924946)
3. Generation of a highly pathogenic avian influenza A virus from an avirulent field isolate by passaging in chickens. T Ito H Goto E Yamamoto H Tanaka M Takeuchi M Kuwayama Y Kawaoka K Otsuki, J Virol 2001 75 4439 4443 10.1128/JVI.75.9.4439-4443.2001 11287597 (Pubitemid 32410160)
4. Replication and transmission of influenza viruses in Japanese quail. NV Makarova H Ozaki H Kida RG Webster DR Perez, Virology 2003 310 8 15 10.1016/S0042-6822(03)00094-1 12788625 (Pubitemid 38352576)
5. Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. DR Perez W Lim JP Seiler G Yi M Peiris KF Shortridge RG Webster, J Virol 2003 77 3148 3156 10.1128/JVI.77.5.3148-3156.2003 12584339 (Pubitemid 36228099)
6. Comparative susceptibility of chickens and turkeys to avian influenza A H7N2 virus infection and protective efficacy of a commercial avian influenza H7N2 virus vaccine. TM Tumpey DR Kapczynski DE Swayne, Avian Dis 2004 48 167 176 10.1637/7103 15077811 (Pubitemid 38448588)
7. Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. DA Senne B Panigrahy Y Kawaoka JE Pearson J Suss M Lipkind H Kida RG Webster, Avian Dis 1996 40 425 437 10.2307/1592241 8790895 (Pubitemid 26310993)
8. Avian influenza. T Ito Y Kawaoka, Textbook of Influenza Blackwell Science Ltd, Oxford, Nicholson KG, Webster RG, Hay AJ, 1998 126 136
9. Source of high pathogenicity of an avian influenza virus H5N1: why H5 is better cleaved by furin. P Decha T Rungrotmongkol P Intharathep M Malaisree O Aruksakunwong C Laohpongspaisan V Parasuk P Sompornpisut S Pianwanit S Kokpol S Hannongbua, Biophys J 2008 95 128 134 10.1529/biophysj.107.127456 18375507
10. Cleavage mechanism of the H5N1 hemagglutinin by trypsin and furin. XL Guo L Li DQ Wei YS Zhu KC Chou, Amino Acids 2008 35 375 382 10.1007/s00726-007- 0611-3 18235997
11. Characterization of H9 subtype influenza viruses from the ducks of southern China: a candidate for the next influenza pandemic in humans? KS Li KM Xu JS Peiris LL Poon KZ Yu KY Yuen KF Shortridge RG Webster Y Guan, J Virol 2003 77 6988 6994 10.1128/JVI.77.12.6988-6994.2003 12768017 (Pubitemid 36666891)
12. Genetic conservation of hemagglutinin gene of H9 influenza virus in chicken population in Mainland China. JH Liu K Okazaki A Mweene WM Shi QM Wu JL Su GZ Zhang GR Bai H Kida, Virus Genes 2004 29 329 334 10.1007/s11262-004-7436-x 15550773 (Pubitemid 40941266)
13. Continuing evolution of H9 influenza viruses in Korean poultry. YJ Lee JY Shin MS Song YM Lee JG Choi EK Lee OM Jeong HW Sung JH Kim YK Kwon JH Kwon CJ Kim RJ Webby RG Webster YK Choi, Virology 2007 359 313 323 10.1016/j.virol.2006. 09.025 17056087 (Pubitemid 46274868)
14. Evolution and molecular epidemiology of H9N2 influenza A viruses from quail in southern China, 2000 to 2005. KM Xu KS Li GJ Smith JW Li H Tai JX Zhang RG Webster JS Peiris H Chen Y Guan, J Virol 2007 81 2635 2645 10.1128/JVI.02316-06 17192315 (Pubitemid 46447029)
15. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. YJ Guo S Krauss DA Senne IP Mo KS Lo XP Xiong M Norwood KF Shortridge RG Webster Y Guan, Virology 2000 267 279 288 10.1006/viro.1999.0115 10662623 (Pubitemid 30123610)
16. Sequence analysis of the hemagglutinin gene of H9N2 Korean avian influenza viruses and assessment of the pathogenic potential of isolate MS96. CW Lee CS Song YJ Lee IP Mo M Garcia DL Suarez SJ Kim, Avian Dis 2000 44 527 535 10.2307/1593091 11006999
17. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Y Guan KF Shortridge S Krauss RG Webster, Proc Natl Acad Sci USA 1999 96 9363 9367 10.1073/pnas.96.16.9363 10430948 (Pubitemid 29374760)
18. H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. Y Guan KF Shortridge S Krauss PS Chin KC Dyrting TM Ellis RG Webster M Peiris, J Virol 2000 74 9372 9380 10.1128/JVI.74.20.9372-9380.2000 11000205
19. Role of infectious bronchitis live vaccine on pathogenicity of H9N2 avian influenza virus. M Haghighat-Jahromi K Asasi H Nili H Dadras, Int J Poult Sci 2007 6 838 841 10.3923/ijps.2007.838.841 (Pubitemid 350164228)
20. An occurrence of non-highly pathogenic avian influenza in Korea. IP Mo CS Song KS Kim JC Rhee, Proc 4th International Symposium on Avian Influenza, Athens, GA 1998 379 383
21. Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens. N Kishida Y Sakoda M Eto Y Sunaga H Kida, Arch Virol 2004 149 2095 2104 10.1007/s00705-004-0372-1 15503199 (Pubitemid 39508952)
22. Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens. S Bano K Naeem SA Malik, Avian Dis 2003 47 817 822 10.1637/0005-2086-47.s3.817 14575070 (Pubitemid 37143842)
23. Coinfection of avian influenza virus (H9N2 subtype) with infectious bronchitis live vaccine. M Haghighat-Jahromi K Asasi H Nili H Dadras AH Shooshtari, Arch Virol 2008 153 651 655 10.1007/s00705-008-0033-x 18247102
24. Human infection with influenza H9N2. M Peiris KY Yuen CW Leung KH Chan PL Ip RW Lai WK Orr KF Shortridge, Lancet 1999 354 916 917 10.1016/S0140-6736(99) 03311-5 10489954 (Pubitemid 29424025)
25. Cocirculation of avian H9N2 and contemporary "human" H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? JS Peiris Y Guan D Markwell P Ghose RG Webster KF Shortridge, J Virol 2001 75 9679 9686 10.1128/JVI.75.20.9679-9686.2001 11559800 (Pubitemid 32900102)
26. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. TR Maines KJ Szretter L Perrone JA Belser RA Bright H Zeng TM Tumpey JM Katz, Immunol Rev 2008 225 68 84 10.1111/j.1600-065X.2008. 00690.x 18837776
27. Characterization of a human H9N2 influenza virus isolated in Hong Kong. T Saito W Lim T Suzuki Y Suzuki H Kida SI Nishimura M Tashiro, Vaccine 2001 20 125 133 10.1016/S0264-410X(01)00279-1 11567756 (Pubitemid 32905324)
28. Avian influenza, Manual of Diagnostic Tests and Vaccines For Terrestrial Animals (mammals, birds and bees). OIE, Sixth 2008 1 465 481
29. An avian influenza virus of H10 subtype that is highly pathogenic for chickens, but lacks multiple basic amino acids at the haemagglutinin cleavage site. GW Wood J Banks I Strong G Parsons DJ Alexander, Avian Pathol 1996 25 799 806 10.1080/03079459608419182 18645899 (Pubitemid 27052448)
30. Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. H Wan DR Perez, J Virol 2007 81 5181 5191 10.1128/JVI.02827-06 17344280 (Pubitemid 46744428)
31. Molecular changes in A/Chicken/Pennsylvania/83 (H5N2) influenza virus associated with acquisition of virulence. RG Webster Y Kawaoka WJ Bean Jr, Virology 1986 149 165 173 10.1016/0042-6822(86)90118-2 3946082 (Pubitemid 16127814)
32. Insertion of a multibasic cleavage motif into the hemagglutinin of a low-pathogenic avian influenza H6N1 virus induces a highly pathogenic phenotype. VJ Munster EJ Schrauwen E de Wit JM van den Brand TM Bestebroer S Herfst GF Rimmelzwaan AD Osterhaus RA Fouchier, J Virol 2010 84 7953 7960 10.1128/JVI.00449-10 20519405
33. 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. O Stech J Veits S Weber D Deckers D Schroer TW Vahlenkamp A Breithaupt J Teifke TC Mettenleiter J Stech, J Virol 2009 83 5864 5868 10.1128/JVI.02649-08 19297482
34. Pathology and Virus Distribution in Chickens Naturally Infected with Highly Pathogenic Avian Influenza a Virus (H7N7) During the 2003 Outbreak in the Netherlands. D van Riel J van den Brand VJ Munster TM Besteboer RA Fouchier A Osterhaus T Kuiken, Vet Pathol 2009 46 971 976 10.1354/vp.08-VP-0215-K-BC 19429981
35. Targeted infection of endothelial cells by avian influenza virus A/FPV/Rostock/34 (H7N1) in chicken embryos. A Feldmann MK Schafer W Garten HD Klenk, J Virol 2000 74 8018 8027 10.1128/JVI.74.17.8018-8027.2000 10933711 (Pubitemid 30641647)
36. Characterization of H9N2 influenza A viruses isolated from chicken products imported into Japan from China. M Mase M Eto K Imai K Tsukamoto S Yamaguchi, Epidemiol Infect 2007 135 386 391 10.1017/S0950268806006728 16824249 (Pubitemid 46443423)
37. Development of vaccine strains of H5 and H7 influenza viruses. K Soda Y Sakoda N Isoda M Kajihara Y Haraguchi H Shibuya H Yoshida T Sasaki R Sakamoto K Saijo J Hagiwara H Kida, Jpn J Vet Res 2008 55 93 98 18318111 (Pubitemid 351325956)
38. Antigenic and genetic analysis of H5 influenza viruses isolated from water birds for the purpose of vaccine use. K Soda H Ozaki Y Sakoda N Isoda Y Haraguchi S Sakabe N Kuboki N Kishida A Takada H Kida, Arch Virol 2008 153 2041 2048 10.1007/s00705-008-0226-3 18932020
39. Potency of an inactivated avian influenza vaccine prepared from a non-pathogenic H5N1 reassortant virus generated between isolates from migratory ducks in Asia. N Isoda Y Sakoda N Kishida K Soda S Sakabe R Sakamoto T Imamura M Sakaguchi T Sasaki N Kokumai T Ohgitani K Saijo A Sawata J Hagiwara Z Lin H Kida, Arch Virol 2008 153 1685 1692 10.1007/s00705-008-0171-1 18651092
40. The 3' and 5'-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. U Desselberger VR Racaniello JJ Zazra P Palese, Gene 1980 8 315 328 10.1016/0378-1119(80)90007-4 7358274 (Pubitemid 10099893)
41. Universal primer set for the full-length amplification of all influenza A viruses. E Hoffmann J Stech Y Guan RG Webster DR Perez, Arch Virol 2001 146 2275 2289 10.1007/s007050170002 11811679 (Pubitemid 34682391)
42. A DNA transfection system for generation of influenza A virus from eight plasmids. E Hoffmann G Neumann Y Kawaoka G Hobom RG Webster, Proc Natl Acad Sci USA 2000 97 6108 6113 10.1073/pnas.100133697 10801978 (Pubitemid 30367531)
43. Biological activity of monoclonal antibodies to operationally defined antigenic regions on the hemagglutinin molecule of A/Seal/Massachusetts/1/80 (H7N7) influenza virus. H Kida LE Brown RG Webster, Virology 1982 122 38 47 10.1016/0042-6822(82)90375-0 6182687 (Pubitemid 12004497)
44. A simple method for estimating fifty percent endpoints. M Reed H Muench, Am J Hyg 1938 37 493 497