Annals of Laboratory Medicine

Korean Society for Laboratory Medicine (대한진단검사의학회)
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Erythrocyte Binding Preference of Human Pandemic Influenza Virus A and Its Effect on Antibody Response Detection

  • Makkoch, Jarika (Center of Excellence in Clinical Virology, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University) ;
  • Prachayangprecha, Slinporn (Center of Excellence in Clinical Virology, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University) ;
  • Payungporn, Sunchai (Center of Excellence in Clinical Virology, Department of Biochemistry, Faculty of Medicine, Chulalongkorn University) ;
  • Chieochansin, Thaweesak (Center of Excellence in Clinical Virology, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University) ;
  • Songserm, Thaweesak (Faculty of Veterinary Medicine, Kasetsart University) ;
  • Amonsin, Alongkorn (Faculty of Veterinary Science, Chulalongkorn University) ;
  • Poovorawan, Yong (Center of Excellence in Clinical Virology, Department of Pediatrics, Faculty of Medicine, Chulalongkorn University)
  • Published : 2012.07.01
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Abstract

Background: Validation of hemagglutination inhibition (HI) assays is important for evaluating antibody responses to influenza virus, and selection of erythrocytes for use in these assays is important. This study aimed to determine the correlation between receptor binding specificity and effectiveness of the HI assay for detecting antibody response to pandemic influenza H1N1 (pH1N1) virus. Methods: Hemagglutination (HA) tests were performed using erythrocytes from 6 species. Subsequently, 8 hemagglutinating units of pH1N1 from each species were titrated by realtime reverse transcription-PCR. To investigate the effect of erythrocyte binding preference on HI antibody titers, comparisons of HI with microneutralization (MN) assays were performed. Results: Goose erythrocytes showed most specific binding with pH1N1, while HA titers using human erythrocytes were comparable to those using turkey erythrocytes. The erythrocyte binding efficiency was shown to have an impact on antibody detection. Comparing MN titers, HI titers using turkey erythrocytes yielded the most accurate results, while those using goose erythrocytes produced the highest geometric mean titer. Human blood group O erythrocytes lacking a specific antibody yielded results most comparable to those obtained using turkey erythrocytes. Further, pre-existing antibody to pH1N1 and different erythrocyte species can distort HI assay results. Conclusions: HI assay, using turkey and human erythrocytes, yielded the most comparable and applicable results for pH1N1 than those by MN assay, and using goose erythrocytes may lead to overestimated titers. Selection of appropriate erythrocyte species for HI assay allows construction of a more reliable database, which is essential for further investigations and control of virus epidemics.

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References

  1. Centers for Disease Control and Prevention. Swine influenza A (H1N1) infection in two children - Southern California, March-April 2009. MMWR Morb Mortal Wkly Rep 2009;58:400-2.
  2. World Health Organization. Clinical management of adult patients with complications of pandemic influenza A (H1N1) 2009: emergency guidelines for the management of patients with severe respiratory distress and shock in district hospitals in limited-resource settings. Geneva, Switzerland: World Health Organization, 2010.
  3. World Health Organization. Pandemic (H1N1) 2009 - update 111. http://www.who.int/csr/don/2010_07_30/ en/ (Updated on Jul 2010).
  4. Boonsuk P, Payungporn S, ChieochansinT, Samransamruajkit R, Amonsin A, Songserm T, et al. Detection of influenza virus types A and B and type A subtypes (H1, H3, and H5) by multiplex polymerase chain reaction. Tohuku J Exp Med 2008;3:247-55.
  5. Chieochansin T, Makkoch J, Suwannakarn K, Payungporn S, PoovorawanY. Novel H1N1 2009 influenza virus infection in Bangkok, Thailand: effects of school closures. Asian Biomed 2009;3:469-75.
  6. World Health Organization. WHO manual on animal influenza diagnosis and surveillance. Department of communicable disease, World Health Organization, Geneva, Switzerland: World Health Organization, 2002.
  7. Klenk E and Uhlenbruck G. A neuraminic acid containing mucoprotein from cattle erythrocyte stroma. Hoppe Seyler Z Physiol Chem 1958;311:227-33. https://doi.org/10.1515/bchm2.1958.311.1.227
  8. Rogers GN and 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;127:361-73. https://doi.org/10.1016/0042-6822(83)90150-2
  9. Yamakawa T and Nagai Y. Glycolipid at the cell surface and their biological functions. Trends Biochem Sci 1978;3:128-31. https://doi.org/10.1016/S0968-0004(78)80031-0
  10. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, Wiley DC. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 1983;304:76-8. https://doi.org/10.1038/304076a0
  11. Stephenson I, Wood JM, Nicholson KG, Zambon MC. Sialic acid receptor specificity on erythrocytes affects detection of antibody to avian influenza haemagglutinin. J Med Virol 2003;70:391-8. https://doi.org/10.1002/jmv.10408
  12. Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, Kawaoka Y. Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 1997;227:493-9. https://doi.org/10.1006/viro.1996.8323
  13. Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, Kiso M, et al. Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 2000;74:11825-31. https://doi.org/10.1128/JVI.74.24.11825-11831.2000
  14. Chutinimitkul S, Chieochansin T, Payungporn S, Samransamruajkit R, Hiranras T, Theamboonlert A, et al. Molecular characterization and phylogenetic analysis of H1N1 and H3N2 human influenza A viruses among infants and children in Thailand. Virus Res 2008;132:122-31. https://doi.org/10.1016/j.virusres.2007.11.007
  15. Makkoch J, Payungporn S, Prachayangprecha S, Tantilertcharoen R, Poovorawan Y. Determination of antibody response to the human pandemic influenza H1N1 2009 among patients with influenza-like illness and high risk group. Asian Pac J Allergy Immunol 2010;28:67-75.
  16. World Health Organization. CDC protocol of realtime RT-PCR for influenza A (H1N1). http://www.who.int/csr/resources/publications/swineflu/realtimeptpcr/en/index.html (Updated on Apr 2009).
  17. Prachayangprecha S, Makkoch J, Payungporn S, Chieochansin T, Vuthitanachot C, Vuthitanachot V, et al. Serological analysis of human pandemic influenza (H1N1) in Thailand. J Health Popul Nutr 2010;28:537-44.
  18. Kendal AP, PereiraMS, Skehel JJ. Concepts and procedures for laboratory- based influenza surveillance. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control, 1982.
  19. Martensson E, Raal A, Svennerholm L. Sialic acid in blood serum. Biochim BiophysActa 1958;30:124-9. https://doi.org/10.1016/0006-3002(58)90248-8
  20. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, et al. Crossreactive antibody response to the 2009 pandemic H1N1 influenza virus. N Eng J Med 2009;361:1945-52. https://doi.org/10.1056/NEJMoa0906453
  21. Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, Lim W, et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 1999;37:937-43.
  22. Reed LJ and Muench H. A simple method of estimating fifty percent endpoint. Am J Hyg 1938;27:493-7.
  23. Hara S, Takemori Y, Yamaguchi M, Nakamura M, Ohkura Y. Fluorometric high-performance liquid chromatography of N-acetyl-and N-glycolylneuraminic acids and its application to their microdetermination in human and animal sera, glycoproteins, and glycolipids. Anal Biochem 1987;164:138-45. https://doi.org/10.1016/0003-2697(87)90377-0
  24. Naiki M. Chemical and immunochemical properties of two classes of globoside from equine organs. Jpn J Exp Med 1971;41:67-81.
  25. Pettersson S, Sivertsson OR, Sjogren S, Svennerholm L. The sialic acids of hog pancreas. Biochim BiophysActa 1958;28:444-5. https://doi.org/10.1016/0006-3002(58)90498-0
  26. Schauer R, ed. Sialic acids, chemistry, metabolism, and function. New York: Springer-Verlag, 1982.
  27. Varki A. Diversity in the sialic acids. Glycobiology 1992;2:25-40. https://doi.org/10.1093/glycob/2.1.25
  28. Higa HH, Rogers GN, Paulson JC. Influenza virus hemagglutinins differentiate between receptor determinants bearing N-acetyl-, N-glycollyland N,O-diacetylneuraminic acids. Virology 1985;144:279-82. https://doi.org/10.1016/0042-6822(85)90325-3
  29. 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. https://doi.org/10.1006/viro.1994.1615
  30. Ilyulshina NA, Kim JK, Negovetich NJ, Choi YK, Lang V, Bovin NV, et al. Extensive mammalian ancestry of pandemic (H1N1) 2009 virus. Emerg Infect Dis 2010;16:314-7. https://doi.org/10.3201/eid1602.091141
  31. Suzuki Y, Matsunaga M, Matsumoto M. N-Acetylneuraminyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. Binding specificity of influenza virus A/Aichi/2/68 (H3N2) to membrane-associated GM3 with different molecular species of sialic acid. J Biol Chem 1985;260:1362-5.
  32. Wiriyarat W, Lerdsamran H, Pooruk P, Webster RG, Louisirirotchanakul S, Ratanakorn P, et al. Erythrocyte binding preference of 16 subtypes of low pathogenic avian influenza and 2009 pandemic influenza A (H1N1) viruses. Vet Microbiol 2010;15:346-9.
  33. Carboneras C. Family Anatidae (ducks, geese, and swans). In: del Hoyo J, Elliot A, Sargatal J, eds. Handbook of the birds of the world. Barcelona: Lynx Edicions, 1992:536-628.
  34. Dulyachai W, Makkoch J, Rianthavorn P, Changpinyo M, Prayangprecha S, Payungporn S, et al. Perinatal pandemic (H1N1) 2009 infection, Thailand. Emerg Infect Dis 2010;16:343-4. https://doi.org/10.3201/eid1602.091733

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