Molecular change of hemagglutinin and neuraminidase of 2009 pandemic influenza virus H1N1 in Thailand, 2009-2011
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Published:
Jan 1, 2016
Keywords:
2009 pandemic influenza virus A (H1N1) epidemic wave HI titer genetic drift
Main Article Content
Abstract
Background: The 2009 pandemic influenza virus A (H1N1) caused the global pandemic disease since the first outbreak reported in April 2009. HA and NA genes of influenza virus have the frequent antigenic variation resulted from immune response and drug.
Objective: To analyze HA and NA genes from 34 viral isolates circulating during 2009-2011 in Thailand to elucidate the genetic drift of these genes.
Methods: A total of 34 samples of viruses were derived from individuals with influenza-like illness (ILI) in each epidemic wave from different regional areas of Thailand. Nucleotide sequences of HA and NA of viruses from each epidemic wave were analyzed and compared with the vaccine strain. Phylogenetic tree was constructed from the concatenated HA and NA nucleotide sequences of viruses isolated in this work. HI titer of the virus isolated from each epidemic wave was also determined with a reference human serum.
Result: Nucleotide and amino acid sequences analysis revealed that antigenic drift from vaccine strain of both genes has been occurred in the antigenic site since the first epidemic wave in Thailand. The increasing of mutation in the antigenic site could be observed in virus isolated from the 4th epidemic wave. However, no any amino acid differences could be found in receptor binding site and glycosylation site within HA of most virus isolates comparing to the vaccine strain according to HI titer. Additionally, change in amino acid sequence was not occurred in the drug binding site of NA. Phylogenetic tree analysis could classify viruses into closely related but distinct clusters.
Conclusion: Viruses were different between early pandemic and the 4th epidemic wave. Therefore, surveillance of the antigenic drift of 2009 pandemic influenza virus A (H1N1) should be continuously followed up for the consideration of vaccine update and drug treatment in Thailand.
Bull Chiang Mai Assoc Med Sci 2016; 49(1): 36-52. Doi: 10.14456/jams.2016.12
Article Details
How to Cite
Rattanarojpong, T., Wongprompitak, P., Pooruk, P., Lerdsamran, H., Phawong, C., Tassaneetrithep, B., Kongyu, S., Iamsirithaworn, S., & Puthavathana, P. (2016). Molecular change of hemagglutinin and neuraminidase of 2009 pandemic influenza virus H1N1 in Thailand, 2009-2011. Journal of Associated Medical Sciences, 49(1), 36. Retrieved from https://he01.tci-thaijo.org/index.php/bulletinAMS/article/view/59937
Section
Research Articles
Personal views expressed by the contributors in their articles are not necessarily those of the Journal of Associated Medical Sciences, Faculty of Associated Medical Sciences, Chiang Mai University.
References
1. Forrest HL, Webster RG. Perspectives on influenza evolution and the role of research. Anim Health Res Rev. 2010; 11: 3-18.
2. Nelson MI, Holmes EC. The evolution of epidemic influenza. Nat Rev Genet. 2007; 8: 196-205.
3. Drake JW. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U SA. 1993; 90: 4171-5.
4. Ortín J, Nájera R, López C, Dávila M, Domingo E. Genetic variability of Hong Kong (H3N2) influenza viruses: spontaneous mutations and their location in the viral genome. Gene. 1980; 11: 319-31.
5. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science. 2009; 325; 197-201.
6. Maurer-Stroh S, Ma J, Lee RT, Sirota FL, Eisenhaber F. Mapping the sequence mutations of the 2009 H1N1 influenza A virus neuraminidase relative to drug and antibody binding sites. Biol Direct. 2009; doi: 10.1186/1745-6150-4-18.
7. Xu L, Bao L, Lv Q, Deng W, Ma Y, Li F, et al. A single-amino-acid substitution in the HA protein changes the replication and pathogenicity of the 2009 pandemic A (H1N1) influenza viruses in vitro and in vivo. Virol J. 2010; doi: 10.1186/1743-422X-7-325.
8. Treanor J. Influenza vaccine--outmaneuvering antigenic shift and drift. N Engl J Med. 2004; 350: 218-20.
9. Boni MF. Vaccination and antigenic drift in influenza. Vaccine. 2008; 26: C8-14.
10. Boni MF, Gog JR, Andreasen V, Feldman MW. Epidemic dynamics and antigenic evolution in a single season of influenza A. Proc Biol Sci. 2006; 273:1307-16.
11. Lee CW, Senne DA, Suarez DL. Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. J Virol. 2004; 78; 8372-81.
12. Stevens J1, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science. 2004; 303: 1866-70.
13. Yang H, Carney P, Stevens J. Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr. 2010; 2: RRN1152.
14. Breschkin AM, Ahern J, White DO. Antigenic determinants of influenza virus hemagglutinin. VIII. Topography of the antigenic regions of influenza virus hemagglutinin determined by competitive radioimmunoassay with monoclonal antibodies. Virology. 1981; 113: 130-40.
15. Caton AJ, Raymond FL, Brownlee GG, Yewdell JW, Gerhard W. Antigenic variation in influenza virus. Biochem Soc Trans. 1983; 11: 435-41.
16. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE Jr, Wilson IA. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science. 2010; 328: 357-60.
17. Laver WG. Crystallization and peptide maps of neuraminidase “heads” from H2N2 and H3N2 influenza virus strains. Virology. 1978; 86: 78-87.
18. Steinhauer DA, Skehel JJ. Genetics of influenza viruses. Annu Rev Genet. 2002; 36: 305-32.
19. Zambon MC. The pathogenesis of influenza in humans. Rev Med Virol. 2001; 11: 227-41.
20. de Wit E, Munster VJ, van Riel D, Beyer WE, Rimmelzwaan GF, Kuiken T, et al. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol. 2010; 84: 1597-606.
21. Kobasa D, Wells K, Kawaoka Y. Amino acids responsible for the absolute sialidase activity of the influenza A virus neuraminidase: relationship to growth in the duck intestine. J Virol. 2001; 75; 11773-80.
22. Hughes MT1, McGregor M, Suzuki T, Suzuki Y, Kawaoka Y. Adaptation of influenza A viruses to cells expressing low levels of sialic acid leads to loss of neuraminidase activity. J Virol. 2001; 75: 3766-70.
23. Zhou JJ, Tian J, Fang DY, Liang Y, Yan HJ, Zhou JM, et al. Analysis of antigen epitopes and molecular pathogenic characteristics of the 2009 H1N1 pandemic influenza A virus in China. Acta Virol. 2011; 55, 195-202.
24. Knossow M, Skehel JJ. Variation and infectivity neutralization in influenza. Immunology. 2006; 119: 1-7.
25. Wiley DC, Skehel JJ. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem. 1987; 56: 365-94.
26. Wei CJ, Boyington JC, Dai K, Houser KV, Pearce MB, Kong WP, et al. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci Transl Med. 2010; 2; 24ra21.
27. Sun S, Wang Q, Zhao F, Chen W, Li Z. Glycosylation site alteration in the evolution of influenza A (H1N1) viruses. PLoS One. 2011; 6; e22844.
28. Goñi N, Fajardo A, Moratorio G, Colina R, Cristina J. Modeling gene sequences over time in 2009 H1N1 influenza A virus populations. Virol J. 2009; 6: 215.
29. Furuse Y, Shimabukuro K, Odagiri T, Sawayama R, Okada T, Khandaker I, Suzuki A, Oshitani H. Comparison of selection pressures on the HA gene of pandemic (2009) and seasonal human and swine influenza A H1 subtype viruses. Virology. 2010; 405: 314-21.
30. Fereidouni SR, Beer M, Vahlenkamp T, Starick E. Differentiation of two distinct clusters among currently circulating influenza A (H1N1)v viruses, March-September 2009. Euro Surveill. 2009; 14: pii: 19409.
31. Zepeda HM, Perea-Araujo L, Zarate-Segura PB, Vázquez-Pérez JA, Miliar-García A, Garibay-Orijel C, et al. Identification of influenza A pandemic (H1N1) 2009 variants during the first 2009 influenza outbreak in Mexico City. J Clin Virol. 2010; 48: 36-9.
32. Glinsky GV. Genomic analysis of pandemic (H1N1) 2009 reveals association of increasing disease severity with emergence of novel hemagglutinin mutations. Cell Cycle. 2010; 9: 958-70.
33. van der Vries E, Stelma FF, Boucher CA. Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. N Engl J Med. 2010; 363: 1381-2.
34. Melidou A, Gioula G, Exindari M, Chatzidimitriou D, Diza E, Malisiovas N. Molecular and phylogenetic analysis of the haemagglutinin gene of pandemic influenza H1N1 2009 viruses associated with severe and fatal infections. Virus Res. 2010; 151: 192-9.
35. Puzelli S, Facchini M, Spagnolo D, De Marco MA, Calzoletti L, Zanetti A, et al. Transmission of hemagglutinin D222G mutant strain of pandemic (H1N1) 2009 virus. Emerg Infect Dis. 2010; 16: 863-5.
36. Maurer-Stroh S, Lee RT, Eisenhaber F, Cui L, Phuah SP, Lin RT. A new common mutation in the hemagglutinin of the 2009 (H1N1) influenza A virus. PLoS Curr. 2010; 2: RRN1162.
37. World Health Organization (2010): H1N1 now in the post-pandemic period. Online at http://www/who.int/csr/disease/swineflu/en/>. Retrieved October 14, 2013
38. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792-7.
39. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17: 754-5.
40. Makkoch J, Suwannakarn K, Payungporn S, Prachayangprecha S, Cheiocharnsin T, Linsuwanon P, et al. Whole genome characterization, phylogenetic and genome signature analysis of human pandemic H1N1 virus in Thailand, 2009-2012. PLoS One. 2012; 7: e51275.
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28: 2731-9.
42. Lerdsamran H, Pittayawonganon C, Pooruk P, Mungaomklang A, Iamsirithaworn S, Thongcharoen P, et al. Serological response to the 2009 pandemic influenza A (H1N1) virus for disease diagnosis and estimating the infection rate in Thai population. PLoS One. 2011; 6: e16164.
43. Igarashi M, Ito K, Yoshida R, Tomabechi D, Kida H, Takada A. Predicting the antigenic structure of the pandemic (H1N1) 2009 influenza virus hemagglutinin. PLoS One. 2010; 5: e8553.
44. Payungporn S, Panjaworayan N, Makkoch J, Poovorawan Y. Molecular characteristics of the human pandemic influenza A virus (H1N1). Acta Virol. 2010; 54: 155-63.
45. Sung JC, Van Wynsberghe AW, Amaro RE, Li WW, McCammon JA. Role of secondary sialic acid binding sites in influenza N1 neuraminidase. J Am Chem Soc. 2010; 132: 2883-5.
46. WHO: Pandemic (H1N1). 2009 [http://www.wpro.who.int/media_centre/press_releases/pr_20091206.htm]. Retrieved October 14, 2013
47. Reinheimer C1, Doerr HW, Friedrichs I, Stürmer M, Allwinn R. H1N1v at a seroepidemiological glance: is the nightmare over? Eur J Clin Microbiol Infect Dis. 2012; 31: 1467-71.
48. Zhang H, Huang YW, Liu YZ, Li FC, Chen Z, Li WC, et al. Virological surveillance of pandemic (H1N1) 2009 virus and its genetic characteristics in Hunan Province, 2009-2011. Bing Du Xue Bao. 2013; 29: 148-53.
2. Nelson MI, Holmes EC. The evolution of epidemic influenza. Nat Rev Genet. 2007; 8: 196-205.
3. Drake JW. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U SA. 1993; 90: 4171-5.
4. Ortín J, Nájera R, López C, Dávila M, Domingo E. Genetic variability of Hong Kong (H3N2) influenza viruses: spontaneous mutations and their location in the viral genome. Gene. 1980; 11: 319-31.
5. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science. 2009; 325; 197-201.
6. Maurer-Stroh S, Ma J, Lee RT, Sirota FL, Eisenhaber F. Mapping the sequence mutations of the 2009 H1N1 influenza A virus neuraminidase relative to drug and antibody binding sites. Biol Direct. 2009; doi: 10.1186/1745-6150-4-18.
7. Xu L, Bao L, Lv Q, Deng W, Ma Y, Li F, et al. A single-amino-acid substitution in the HA protein changes the replication and pathogenicity of the 2009 pandemic A (H1N1) influenza viruses in vitro and in vivo. Virol J. 2010; doi: 10.1186/1743-422X-7-325.
8. Treanor J. Influenza vaccine--outmaneuvering antigenic shift and drift. N Engl J Med. 2004; 350: 218-20.
9. Boni MF. Vaccination and antigenic drift in influenza. Vaccine. 2008; 26: C8-14.
10. Boni MF, Gog JR, Andreasen V, Feldman MW. Epidemic dynamics and antigenic evolution in a single season of influenza A. Proc Biol Sci. 2006; 273:1307-16.
11. Lee CW, Senne DA, Suarez DL. Effect of vaccine use in the evolution of Mexican lineage H5N2 avian influenza virus. J Virol. 2004; 78; 8372-81.
12. Stevens J1, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science. 2004; 303: 1866-70.
13. Yang H, Carney P, Stevens J. Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr. 2010; 2: RRN1152.
14. Breschkin AM, Ahern J, White DO. Antigenic determinants of influenza virus hemagglutinin. VIII. Topography of the antigenic regions of influenza virus hemagglutinin determined by competitive radioimmunoassay with monoclonal antibodies. Virology. 1981; 113: 130-40.
15. Caton AJ, Raymond FL, Brownlee GG, Yewdell JW, Gerhard W. Antigenic variation in influenza virus. Biochem Soc Trans. 1983; 11: 435-41.
16. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE Jr, Wilson IA. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science. 2010; 328: 357-60.
17. Laver WG. Crystallization and peptide maps of neuraminidase “heads” from H2N2 and H3N2 influenza virus strains. Virology. 1978; 86: 78-87.
18. Steinhauer DA, Skehel JJ. Genetics of influenza viruses. Annu Rev Genet. 2002; 36: 305-32.
19. Zambon MC. The pathogenesis of influenza in humans. Rev Med Virol. 2001; 11: 227-41.
20. de Wit E, Munster VJ, van Riel D, Beyer WE, Rimmelzwaan GF, Kuiken T, et al. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol. 2010; 84: 1597-606.
21. Kobasa D, Wells K, Kawaoka Y. Amino acids responsible for the absolute sialidase activity of the influenza A virus neuraminidase: relationship to growth in the duck intestine. J Virol. 2001; 75; 11773-80.
22. Hughes MT1, McGregor M, Suzuki T, Suzuki Y, Kawaoka Y. Adaptation of influenza A viruses to cells expressing low levels of sialic acid leads to loss of neuraminidase activity. J Virol. 2001; 75: 3766-70.
23. Zhou JJ, Tian J, Fang DY, Liang Y, Yan HJ, Zhou JM, et al. Analysis of antigen epitopes and molecular pathogenic characteristics of the 2009 H1N1 pandemic influenza A virus in China. Acta Virol. 2011; 55, 195-202.
24. Knossow M, Skehel JJ. Variation and infectivity neutralization in influenza. Immunology. 2006; 119: 1-7.
25. Wiley DC, Skehel JJ. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem. 1987; 56: 365-94.
26. Wei CJ, Boyington JC, Dai K, Houser KV, Pearce MB, Kong WP, et al. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci Transl Med. 2010; 2; 24ra21.
27. Sun S, Wang Q, Zhao F, Chen W, Li Z. Glycosylation site alteration in the evolution of influenza A (H1N1) viruses. PLoS One. 2011; 6; e22844.
28. Goñi N, Fajardo A, Moratorio G, Colina R, Cristina J. Modeling gene sequences over time in 2009 H1N1 influenza A virus populations. Virol J. 2009; 6: 215.
29. Furuse Y, Shimabukuro K, Odagiri T, Sawayama R, Okada T, Khandaker I, Suzuki A, Oshitani H. Comparison of selection pressures on the HA gene of pandemic (2009) and seasonal human and swine influenza A H1 subtype viruses. Virology. 2010; 405: 314-21.
30. Fereidouni SR, Beer M, Vahlenkamp T, Starick E. Differentiation of two distinct clusters among currently circulating influenza A (H1N1)v viruses, March-September 2009. Euro Surveill. 2009; 14: pii: 19409.
31. Zepeda HM, Perea-Araujo L, Zarate-Segura PB, Vázquez-Pérez JA, Miliar-García A, Garibay-Orijel C, et al. Identification of influenza A pandemic (H1N1) 2009 variants during the first 2009 influenza outbreak in Mexico City. J Clin Virol. 2010; 48: 36-9.
32. Glinsky GV. Genomic analysis of pandemic (H1N1) 2009 reveals association of increasing disease severity with emergence of novel hemagglutinin mutations. Cell Cycle. 2010; 9: 958-70.
33. van der Vries E, Stelma FF, Boucher CA. Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. N Engl J Med. 2010; 363: 1381-2.
34. Melidou A, Gioula G, Exindari M, Chatzidimitriou D, Diza E, Malisiovas N. Molecular and phylogenetic analysis of the haemagglutinin gene of pandemic influenza H1N1 2009 viruses associated with severe and fatal infections. Virus Res. 2010; 151: 192-9.
35. Puzelli S, Facchini M, Spagnolo D, De Marco MA, Calzoletti L, Zanetti A, et al. Transmission of hemagglutinin D222G mutant strain of pandemic (H1N1) 2009 virus. Emerg Infect Dis. 2010; 16: 863-5.
36. Maurer-Stroh S, Lee RT, Eisenhaber F, Cui L, Phuah SP, Lin RT. A new common mutation in the hemagglutinin of the 2009 (H1N1) influenza A virus. PLoS Curr. 2010; 2: RRN1162.
37. World Health Organization (2010): H1N1 now in the post-pandemic period. Online at http://www/who.int/csr/disease/swineflu/en/>. Retrieved October 14, 2013
38. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792-7.
39. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17: 754-5.
40. Makkoch J, Suwannakarn K, Payungporn S, Prachayangprecha S, Cheiocharnsin T, Linsuwanon P, et al. Whole genome characterization, phylogenetic and genome signature analysis of human pandemic H1N1 virus in Thailand, 2009-2012. PLoS One. 2012; 7: e51275.
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28: 2731-9.
42. Lerdsamran H, Pittayawonganon C, Pooruk P, Mungaomklang A, Iamsirithaworn S, Thongcharoen P, et al. Serological response to the 2009 pandemic influenza A (H1N1) virus for disease diagnosis and estimating the infection rate in Thai population. PLoS One. 2011; 6: e16164.
43. Igarashi M, Ito K, Yoshida R, Tomabechi D, Kida H, Takada A. Predicting the antigenic structure of the pandemic (H1N1) 2009 influenza virus hemagglutinin. PLoS One. 2010; 5: e8553.
44. Payungporn S, Panjaworayan N, Makkoch J, Poovorawan Y. Molecular characteristics of the human pandemic influenza A virus (H1N1). Acta Virol. 2010; 54: 155-63.
45. Sung JC, Van Wynsberghe AW, Amaro RE, Li WW, McCammon JA. Role of secondary sialic acid binding sites in influenza N1 neuraminidase. J Am Chem Soc. 2010; 132: 2883-5.
46. WHO: Pandemic (H1N1). 2009 [http://www.wpro.who.int/media_centre/press_releases/pr_20091206.htm]. Retrieved October 14, 2013
47. Reinheimer C1, Doerr HW, Friedrichs I, Stürmer M, Allwinn R. H1N1v at a seroepidemiological glance: is the nightmare over? Eur J Clin Microbiol Infect Dis. 2012; 31: 1467-71.
48. Zhang H, Huang YW, Liu YZ, Li FC, Chen Z, Li WC, et al. Virological surveillance of pandemic (H1N1) 2009 virus and its genetic characteristics in Hunan Province, 2009-2011. Bing Du Xue Bao. 2013; 29: 148-53.