Sequence diversity and associated pathogenicity of the hemagglutinin cleavage site of H5N2 avian influenza viruses isolated from chickens in Taiwan during 2013–2015
The sequence at the hemagglutinin (HA) cleavage site (CS) plays a key role in determining the pathogenicity of avian influenza viruses. Three types of HA CS sequences, QREKR/GL, QRKKR/GL and QRRKR/GL, were previously reported in Taiwanese H5N2 viruses that were isolated from chickens from 2003 to 20...
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| Published in | Journal of Veterinary Medical Science Vol. 79; no. 1; pp. 108 - 114 |
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| Main Authors | , , , , , , , , |
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Japan
JAPANESE SOCIETY OF VETERINARY SCIENCE
01.01.2017
Japan Science and Technology Agency The Japanese Society of Veterinary Science |
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| Abstract | The sequence at the hemagglutinin (HA) cleavage site (CS) plays a key role in determining the pathogenicity of avian influenza viruses. Three types of HA CS sequences, QREKR/GL, QRKKR/GL and QRRKR/GL, were previously reported in Taiwanese H5N2 viruses that were isolated from chickens from 2003 to 2013. However, no HA CS sequence was reported for viruses isolated after 2013. This article presents the HA CS sequences and pathogenicity of H5N2 viruses that were isolated from chickens in Taiwan during 2013–2015. Two novel HA CS sequences, QKEKR/GL and KREKREKR/GL, were found in the viruses isolated in 2013 and 2014, and pathogenicity tests showed that the viruses with these novel HA CS sequences are low and high pathogenic viruses, respectively. In contrast, the HA CS sequence QREKR/GL was found in all viruses that were isolated in 2015, and all of these viruses were low pathogenic viruses. After 10 passages in embryonated chicken eggs, a virus strain that was isolated in 2003 evolved into a viral quasispecies that contained at least four distinct types of HA CS sequences. These results highlight the potential of Taiwanese H5N2 viruses to change their pathogenicity and HA CS sequences via mutations. Furthermore, viruses with the HA CS sequence QREKR/GL were more prevalent than others in 2015. These findings are useful for understanding the mechanism of sequence changes at the HA CS and for refining H5N2 virus control measures in Taiwan. |
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| AbstractList | The sequence at the hemagglutinin (HA) cleavage site (CS) plays a key role in determining the pathogenicity of avian influenza viruses. Three types of HA CS sequences, QREKR/GL, QRKKR/GL and QRRKR/GL, were previously reported in Taiwanese H5N2 viruses that were isolated from chickens from 2003 to 2013. However, no HA CS sequence was reported for viruses isolated after 2013. This article presents the HA CS sequences and pathogenicity of H5N2 viruses that were isolated from chickens in Taiwan during 2013-2015. Two novel HA CS sequences, QKEKR/GL and KREKREKR/GL, were found in the viruses isolated in 2013 and 2014, and pathogenicity tests showed that the viruses with these novel HA CS sequences are low and high pathogenic viruses, respectively. In contrast, the HA CS sequence QREKR/GL was found in all viruses that were isolated in 2015, and all of these viruses were low pathogenic viruses. After 10 passages in embryonated chicken eggs, a virus strain that was isolated in 2003 evolved into a viral quasispecies that contained at least four distinct types of HA CS sequences. These results highlight the potential of Taiwanese H5N2 viruses to change their pathogenicity and HA CS sequences via mutations. Furthermore, viruses with the HA CS sequence QREKR/GL were more prevalent than others in 2015. These findings are useful for understanding the mechanism of sequence changes at the HA CS and for refining H5N2 virus control measures in Taiwan. The sequence at the hemagglutinin (HA) cleavage site (CS) plays a key role in determining the pathogenicity of avian influenza viruses. Three types of HA CS sequences, QREKR/GL, QRKKR/GL and QRRKR/GL, were previously reported in Taiwanese H5N2 viruses that were isolated from chickens from 2003 to 2013. However, no HA CS sequence was reported for viruses isolated after 2013. This article presents the HA CS sequences and pathogenicity of H5N2 viruses that were isolated from chickens in Taiwan during 2013–2015. Two novel HA CS sequences, QKEKR/GL and KREKREKR/GL, were found in the viruses isolated in 2013 and 2014, and pathogenicity tests showed that the viruses with these novel HA CS sequences are low and high pathogenic viruses, respectively. In contrast, the HA CS sequence QREKR/GL was found in all viruses that were isolated in 2015, and all of these viruses were low pathogenic viruses. After 10 passages in embryonated chicken eggs, a virus strain that was isolated in 2003 evolved into a viral quasispecies that contained at least four distinct types of HA CS sequences. These results highlight the potential of Taiwanese H5N2 viruses to change their pathogenicity and HA CS sequences via mutations. Furthermore, viruses with the HA CS sequence QREKR/GL were more prevalent than others in 2015. These findings are useful for understanding the mechanism of sequence changes at the HA CS and for refining H5N2 virus control measures in Taiwan. The sequence at the hemagglutinin (HA) cleavage site (CS) plays a key role in determining the pathogenicity of avian influenza viruses. Three types of HA CS sequences, QREKR/GL, QRKKR/GL and QRRKR/GL, were previously reported in Taiwanese H5N2 viruses that were isolated from chickens from 2003 to 2013. However, no HA CS sequence was reported for viruses isolated after 2013. This article presents the HA CS sequences and pathogenicity of H5N2 viruses that were isolated from chickens in Taiwan during 2013-2015. Two novel HA CS sequences, QKEKR/GL and KREKREKR/GL, were found in the viruses isolated in 2013 and 2014, and pathogenicity tests showed that the viruses with these novel HA CS sequences are low and high pathogenic viruses, respectively. In contrast, the HA CS sequence QREKR/GL was found in all viruses that were isolated in 2015, and all of these viruses were low pathogenic viruses. After 10 passages in embryonated chicken eggs, a virus strain that was isolated in 2003 evolved into a viral quasispecies that contained at least four distinct types of HA CS sequences. These results highlight the potential of Taiwanese H5N2 viruses to change their pathogenicity and HA CS sequences via mutations. Furthermore, viruses with the HA CS sequence QREKR/GL were more prevalent than others in 2015. These findings are useful for understanding the mechanism of sequence changes at the HA CS and for refining H5N2 virus control measures in Taiwan.The sequence at the hemagglutinin (HA) cleavage site (CS) plays a key role in determining the pathogenicity of avian influenza viruses. Three types of HA CS sequences, QREKR/GL, QRKKR/GL and QRRKR/GL, were previously reported in Taiwanese H5N2 viruses that were isolated from chickens from 2003 to 2013. However, no HA CS sequence was reported for viruses isolated after 2013. This article presents the HA CS sequences and pathogenicity of H5N2 viruses that were isolated from chickens in Taiwan during 2013-2015. Two novel HA CS sequences, QKEKR/GL and KREKREKR/GL, were found in the viruses isolated in 2013 and 2014, and pathogenicity tests showed that the viruses with these novel HA CS sequences are low and high pathogenic viruses, respectively. In contrast, the HA CS sequence QREKR/GL was found in all viruses that were isolated in 2015, and all of these viruses were low pathogenic viruses. After 10 passages in embryonated chicken eggs, a virus strain that was isolated in 2003 evolved into a viral quasispecies that contained at least four distinct types of HA CS sequences. These results highlight the potential of Taiwanese H5N2 viruses to change their pathogenicity and HA CS sequences via mutations. Furthermore, viruses with the HA CS sequence QREKR/GL were more prevalent than others in 2015. These findings are useful for understanding the mechanism of sequence changes at the HA CS and for refining H5N2 virus control measures in Taiwan. |
| Author | LIU, Yu-Pin LIN, Yu-Ju SHIEN, Jui-Hung CHEN, Li-Hsuan TAN, Duen-Huey LI, Kuang-Po CHANG, Poa-Chun CHENG, Ming-Chu TSAI, Hsiang-Jung |
| Author_xml | – sequence: 1 fullname: LI, Kuang-Po organization: Department of Veterinary Medicine, National Chung Hsing University, Taichung 40227, Taiwan – sequence: 2 fullname: CHANG, Poa-Chun organization: Graduate Institute of Microbiology and Public Health, National Chung Hsing University, Taichung 40227, Taiwan – sequence: 3 fullname: CHENG, Ming-Chu organization: Animal Health Research Institute, New Taipei City 25158, Taiwan – sequence: 4 fullname: TAN, Duen-Huey organization: Graduate Institute of Microbiology and Public Health, National Chung Hsing University, Taichung 40227, Taiwan – sequence: 5 fullname: CHEN, Li-Hsuan organization: Animal Health Research Institute, New Taipei City 25158, Taiwan – sequence: 6 fullname: LIU, Yu-Pin organization: Animal Health Research Institute, New Taipei City 25158, Taiwan – sequence: 7 fullname: LIN, Yu-Ju organization: Animal Health Research Institute, New Taipei City 25158, Taiwan – sequence: 8 fullname: TSAI, Hsiang-Jung organization: Animal Health Research Institute, New Taipei City 25158, Taiwan – sequence: 9 fullname: SHIEN, Jui-Hung organization: Department of Veterinary Medicine, National Chung Hsing University, Taichung 40227, Taiwan |
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| References | 6. Fouchier, R. A., Munster, V., Wallensten, A., Bestebroer, T. M., Herfst, S., Smith, D., Rimmelzwaan, G. F., Olsen, B. and Osterhaus, A. D. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79: 2814–2822. 15. Van den Hoecke, S., Verhelst, J., Vuylsteke, M. and Saelens, X. 2015. Analysis of the genetic diversity of influenza A viruses using next-generation DNA sequencing. BMC Genomics 16: 79. 1. Alexander, D. J. 1995. The epidemiology and control of avian influenza and Newcastle disease. J. Comp. Pathol. 112: 105–126. 5. Duffy, S., Shackelton, L. A. and Holmes, E. C. 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9: 267–276. 16. WHO. 2014. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/. [accessed 16 August, 2016]. 13. Senne, D. A., Panigrahy, B., Kawaoka, Y., Pearson, J. E., Süss, J., Lipkind, M., Kida, H. and Webster, R. G. 1996. 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. Avian Dis. 40: 425–437. 14. Soda, K., Cheng, M. C., Yoshida, H., Endo, M., Lee, S. H., Okamatsu, M., Sakoda, Y., Wang, C. H. and Kida, H. 2011. A low pathogenic H5N2 influenza virus isolated in Taiwan acquired high pathogenicity by consecutive passages in chickens. J. Vet. Med. Sci. 73: 767–772. 10. Londt, B. Z., Banks, J. and Alexander, D. J. 2007. Highly pathogenic avian influenza viruses with low virulence for chickens in in vivo tests. Avian Pathol. 36: 347–350. 11. OIE 2008. Avian influenza, pp. 465–481. In: Manual of Diagnostic Tests and Vaccines For Terrestrial Animals (Mammals, Birds and Bees), 6th ed., vol. 1. Office Intl Des Epizooties, Paris. 3. Cheng, M. C., Lee, M. S., Lee, S. H. and Wang, C. H. 2011. The Virulence Variation in a H5N2 Low Pathogenic Avian Influenza Virus after Passage in 14-day-old Chicken Embryonic Eggs. Taiwan V. J. 37: 221–226. (in Chinese) 4. Cheng, M. C., Soda, K., Lee, M. S., Lee, S. H., Sakoda, Y., Kida, H. and Wang, C. H. 2010. Isolation and characterization of potentially pathogenic H5N2 influenza virus from a chicken in Taiwan in 2008. Avian Dis. 54: 885–893. 12. Rott, R. 1992. The pathogenic determinant of influenza virus. Vet. Microbiol. 33: 303–310. 9. Lee, C. C., Zhu, H., Huang, P. Y., Peng, L., Chang, Y. C., Yip, C. H., Li, Y. T., Cheung, C. L., Compans, R., Yang, C., Smith, D. K., Lam, T. T., King, C. C. and Guan, Y. 2014. Emergence and evolution of avian H5N2 influenza viruses in chickens in Taiwan. J. Virol. 88: 5677–5686. 2. Banks, J., Speidel, E. S., Moore, E., Plowright, L., Piccirillo, A., Capua, I., Cordioli, P., Fioretti, A. and Alexander, D. J. 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. 8. Iqbal, M., Reddy, K. B., Brookes, S. M., Essen, S. C., Brown, I. H. and McCauley, J. W. 2014. Virus pathotype and deep sequencing of the HA gene of a low pathogenicity H7N1 avian influenza virus causing mortality in Turkeys. PLOS ONE 9: e87076. 7. Horimoto, T., Rivera, E., Pearson, J., Senne, D., Krauss, S., Kawaoka, Y. and Webster, R. G. 1995. Origin and molecular changes associated with emergence of a highly pathogenic H5N2 influenza virus in Mexico. Virology 213: 223–230. 11 12 13 14 15 16 1 2 3 4 5 6 7 8 9 10 24489838 - PLoS One. 2014 Jan 28;9(1):e87076 25758772 - BMC Genomics. 2015 Feb 14;16:79 8790895 - Avian Dis. 1996 Apr-Jun;40(2):425-37 7483266 - Virology. 1995 Oct 20;213(1):223-30 21301183 - J Vet Med Sci. 2011 Jun;73(6):767-72 17899457 - Avian Pathol. 2007 Oct;36(5):347-50 24623422 - J Virol. 2014 May;88(10):5677-86 1481363 - Vet Microbiol. 1992 Nov;33(1-4):303-10 11448033 - Arch Virol. 2001;146(5):963-73 15709000 - J Virol. 2005 Mar;79(5):2814-22 18319742 - Nat Rev Genet. 2008 Apr;9(4):267-76 7769142 - J Comp Pathol. 1995 Feb;112(2):105-26 20608534 - Avian Dis. 2010 Jun;54(2):885-93 |
| References_xml | – reference: 11. OIE 2008. Avian influenza, pp. 465–481. In: Manual of Diagnostic Tests and Vaccines For Terrestrial Animals (Mammals, Birds and Bees), 6th ed., vol. 1. Office Intl Des Epizooties, Paris. – reference: 13. Senne, D. A., Panigrahy, B., Kawaoka, Y., Pearson, J. E., Süss, J., Lipkind, M., Kida, H. and Webster, R. G. 1996. 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. Avian Dis. 40: 425–437. – reference: 10. Londt, B. Z., Banks, J. and Alexander, D. J. 2007. Highly pathogenic avian influenza viruses with low virulence for chickens in in vivo tests. Avian Pathol. 36: 347–350. – reference: 1. Alexander, D. J. 1995. The epidemiology and control of avian influenza and Newcastle disease. J. Comp. Pathol. 112: 105–126. – reference: 4. Cheng, M. C., Soda, K., Lee, M. S., Lee, S. H., Sakoda, Y., Kida, H. and Wang, C. H. 2010. Isolation and characterization of potentially pathogenic H5N2 influenza virus from a chicken in Taiwan in 2008. Avian Dis. 54: 885–893. – reference: 3. Cheng, M. C., Lee, M. S., Lee, S. H. and Wang, C. H. 2011. The Virulence Variation in a H5N2 Low Pathogenic Avian Influenza Virus after Passage in 14-day-old Chicken Embryonic Eggs. Taiwan V. J. 37: 221–226. (in Chinese) – reference: 8. Iqbal, M., Reddy, K. B., Brookes, S. M., Essen, S. C., Brown, I. H. and McCauley, J. W. 2014. Virus pathotype and deep sequencing of the HA gene of a low pathogenicity H7N1 avian influenza virus causing mortality in Turkeys. PLOS ONE 9: e87076. – reference: 14. Soda, K., Cheng, M. C., Yoshida, H., Endo, M., Lee, S. H., Okamatsu, M., Sakoda, Y., Wang, C. H. and Kida, H. 2011. A low pathogenic H5N2 influenza virus isolated in Taiwan acquired high pathogenicity by consecutive passages in chickens. J. Vet. Med. Sci. 73: 767–772. – reference: 6. Fouchier, R. A., Munster, V., Wallensten, A., Bestebroer, T. M., Herfst, S., Smith, D., Rimmelzwaan, G. F., Olsen, B. and Osterhaus, A. D. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79: 2814–2822. – reference: 7. Horimoto, T., Rivera, E., Pearson, J., Senne, D., Krauss, S., Kawaoka, Y. and Webster, R. G. 1995. Origin and molecular changes associated with emergence of a highly pathogenic H5N2 influenza virus in Mexico. Virology 213: 223–230. – reference: 2. Banks, J., Speidel, E. S., Moore, E., Plowright, L., Piccirillo, A., Capua, I., Cordioli, P., Fioretti, A. and Alexander, D. J. 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. – reference: 16. WHO. 2014. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/. [accessed 16 August, 2016]. – reference: 5. Duffy, S., Shackelton, L. A. and Holmes, E. C. 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9: 267–276. – reference: 9. Lee, C. C., Zhu, H., Huang, P. Y., Peng, L., Chang, Y. C., Yip, C. H., Li, Y. T., Cheung, C. L., Compans, R., Yang, C., Smith, D. K., Lam, T. T., King, C. C. and Guan, Y. 2014. Emergence and evolution of avian H5N2 influenza viruses in chickens in Taiwan. J. Virol. 88: 5677–5686. – reference: 15. Van den Hoecke, S., Verhelst, J., Vuylsteke, M. and Saelens, X. 2015. Analysis of the genetic diversity of influenza A viruses using next-generation DNA sequencing. BMC Genomics 16: 79. – reference: 12. Rott, R. 1992. The pathogenic determinant of influenza virus. Vet. Microbiol. 33: 303–310. – ident: 3 – ident: 15 doi: 10.1186/s12864-015-1284-z – ident: 11 – ident: 5 doi: 10.1038/nrg2323 – ident: 16 – ident: 9 doi: 10.1128/JVI.00139-14 – ident: 7 doi: 10.1006/viro.1995.1562 – ident: 2 doi: 10.1007/s007050170128 – ident: 10 doi: 10.1080/03079450701589134 – ident: 13 doi: 10.2307/1592241 – ident: 4 doi: 10.1637/9208-120609-Reg.1 – ident: 8 doi: 10.1371/journal.pone.0087076 – ident: 12 doi: 10.1016/0378-1135(92)90058-2 – ident: 1 doi: 10.1016/S0021-9975(05)80054-4 – ident: 14 doi: 10.1292/jvms.10-0532 – ident: 6 doi: 10.1128/JVI.79.5.2814-2822.2005 – reference: 18319742 - Nat Rev Genet. 2008 Apr;9(4):267-76 – reference: 24623422 - J Virol. 2014 May;88(10):5677-86 – reference: 8790895 - Avian Dis. 1996 Apr-Jun;40(2):425-37 – reference: 11448033 - Arch Virol. 2001;146(5):963-73 – reference: 21301183 - J Vet Med Sci. 2011 Jun;73(6):767-72 – reference: 25758772 - BMC Genomics. 2015 Feb 14;16:79 – reference: 7769142 - J Comp Pathol. 1995 Feb;112(2):105-26 – reference: 24489838 - PLoS One. 2014 Jan 28;9(1):e87076 – reference: 15709000 - J Virol. 2005 Mar;79(5):2814-22 – reference: 20608534 - Avian Dis. 2010 Jun;54(2):885-93 – reference: 7483266 - Virology. 1995 Oct 20;213(1):223-30 – reference: 17899457 - Avian Pathol. 2007 Oct;36(5):347-50 – reference: 1481363 - Vet Microbiol. 1992 Nov;33(1-4):303-10 |
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| SubjectTerms | Animals Avian flu avian influenza virus Base Sequence Chickens Eggs H5N2 hemagglutinin cleavage site Hemagglutinin Glycoproteins, Influenza Virus - genetics Hemagglutinin Glycoproteins, Influenza Virus - metabolism Hemagglutinins Influenza Influenza A Virus, H5N2 Subtype - genetics Influenza A Virus, H5N2 Subtype - pathogenicity Influenza in Birds - virology Pandemics Pathogenicity RNA, Viral - genetics Taiwan Taiwan - epidemiology Virology Virulence |
| Title | Sequence diversity and associated pathogenicity of the hemagglutinin cleavage site of H5N2 avian influenza viruses isolated from chickens in Taiwan during 2013–2015 |
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