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Original Antigenic Sin Response to RNA Viruses and Antiviral Immunity

  • Mee Sook Park (Department of Microbiology, The Institute of Viral Diseases, College of Medicine, Korea University) ;
  • Jin Il Kim (Department of Microbiology, The Institute of Viral Diseases, College of Medicine, Korea University) ;
  • Sehee Park (Department of Microbiology, The Institute of Viral Diseases, College of Medicine, Korea University) ;
  • Ilseob Lee (Department of Microbiology, The Institute of Viral Diseases, College of Medicine, Korea University) ;
  • Man-Seong Park (Department of Microbiology, The Institute of Viral Diseases, College of Medicine, Korea University)
  • Received : 2016.07.13
  • Accepted : 2016.08.15
  • Published : 2016.10.31

Abstract

The human immune system has evolved to fight against foreign pathogens. It plays a central role in the body's defense mechanism. However, the immune memory geared to fight off a previously recognized pathogen, tends to remember an original form of the pathogen when a variant form subsequently invades. This has been termed 'original antigenic sin'. This adverse immunological effect can alter vaccine effectiveness and sometimes cause enhanced pathogenicity or additional inflammatory responses, according to the type of pathogen and the circumstances of infection. Here we aim to give a simplified conceptual understanding of virus infection and original antigenic sin by comparing and contrasting the two examples of recurring infections such as influenza and dengue viruses in humans.

Keywords

Acknowledgement

This study was supported by a grant from the TEPIK (Transgovernmental Enterprise for Pandemic Influenza in Korea), which is part of the Korea Healthcare Technology R&D Project of the Ministry of Health & Welfare, Republic of Korea (Grant No.: A103001).

References

  1. Davenport, F. M., A. V. Hennessy, and T. Francis, Jr. 1953. Epidemiologic and immunologic significance of age distribution of antibody to antigenic variants of influenza virus. J. Exp. Med. 98: 641-656. https://doi.org/10.1084/jem.98.6.641
  2. Taylor, A., S. S. Foo, R. Bruzzone, L. V. Dinh, N. J. King, and S. Mahalingam. 2015. Fc receptors in antibody-dependent enhancement of viral infections. Immunol. Rev. 268: 340-364. https://doi.org/10.1111/imr.12367
  3. McHeyzer-Williams, M., S. Okitsu, N. Wang, and L. Heyzer- Williams. 2012. Molecular programming of B cell memory. Nat. Rev .Immunol. 12: 24-34. https://doi.org/10.1038/nri3128
  4. Netea, M. G., L. A. Joosten, E. Latz, K. H. Mills, G. Natoli, H. G. Stunnenberg, L. A. O'Neill, and R. J. Xavier. 2016. Trained immunity: A program of innate immune memory in health and disease. Science 352: aaf1098.
  5. Okhrimenko, A., J. R. Grun, K. Westendorf, Z. Fang, S. Reinke, R. P. von, G. Wassilew, A. A. Kuhl, R. Kudernatsch, S. Demski, C. Scheibenbogen, K. Tokoyoda, M. A. McGrath, M. J. Raftery, G. Schonrich, A. Serra, H. D. Chang, A. Radbruch, and J. Dong. 2014. Human memory T cells from the bone marrow are resting and maintain long-lasting systemic memory. Proc. Natl. Acad. Sci. U. S. A. 111: 9229-9234. https://doi.org/10.1073/pnas.1318731111
  6. Rothman, A. L. 2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11: 532-543. https://doi.org/10.1038/nri3014
  7. Beverley, P. C. 2002. Immunology of vaccination. Br. Med. Bull. 62: 15-28. https://doi.org/10.1093/bmb/62.1.15
  8. Tangye, S. G., D. T. Avery, E. K. Deenick, and P. D. Hodgkin. 2003. Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses. J. Immunol. 170: 686-694. https://doi.org/10.4049/jimmunol.170.2.686
  9. Michie, C. A., A. McLean, C. Alcock, and P. C. Beverley. 1992. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature 360: 264-265. https://doi.org/10.1038/360264a0
  10. Swain, S. L. 2000. CD4 T-cell memory can persist in the absence of class II. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355: 407-411. https://doi.org/10.1098/rstb.2000.0581
  11. Hale, J. S., and R. Ahmed. 2015. Memory T follicular helper CD4 T cells. Front. Immunol. 6: 16.
  12. Schmidlin, H., S. A. Diehl, and B. Blom. 2009. New insights into the regulation of human B-cell differentiation. Trends Immunol. 30: 277-285. https://doi.org/10.1016/j.it.2009.03.008
  13. Benson, M. J., L. D. Erickson, M. W. Gleeson, and R. J. Noelle. 2007. Affinity of antigen encounter and other early B-cell signals determine B-cell fate. Curr. Opin. Immunol. 19: 275-280. https://doi.org/10.1016/j.coi.2007.04.009
  14. Lees, J. R., and D. L. Farber. 2010. Generation, persistence and plasticity of CD4 T-cell memories. Immunology 130: 463-470. https://doi.org/10.1111/j.1365-2567.2010.03288.x
  15. Ma, C. S., E. K. Deenick, M. Batten, and S. G. Tangye. 2012. The origins, function, and regulation of T follicular helper cells. J. Exp. Med. 209: 1241-1253. https://doi.org/10.1084/jem.20120994
  16. Eisen, H. N. 2014. Affinity enhancement of antibodies: how low-affinity antibodies produced early in immune responses are followed by high-affinity antibodies later and in memory B-cell responses. Cancer Immunol. Res. 2: 381-392. https://doi.org/10.1158/2326-6066.CIR-14-0029
  17. Farrington, L. A., T. A. Smith, F. Grey, A. B. Hill, and C. M. Snyder. 2013. Competition for antigen at the level of the APC is a major determinant of immunodominance during memory inflation in murine cytomegalovirus infection. J. Immunol. 190: 3410-3416. https://doi.org/10.4049/jimmunol.1203151
  18. Johansson, B. E., and E. D. Kilbourne. 1996. Immunization with dissociated neuraminidase, matrix, and nucleoproteins from influenza A virus eliminates cognate help and antigenic competition. Virology 225: 136-144. https://doi.org/10.1006/viro.1996.0581
  19. Pham, G. H., B. V. Iglesias, and E. J. Gosselin. 2014. Fc receptor-targeting of immunogen as a strategy for enhanced antigen loading, vaccination, and protection using intranasally administered antigen-pulsed dendritic cells. Vaccine 32: 5212-5220. https://doi.org/10.1016/j.vaccine.2014.07.050
  20. Krammer, F., P. Palese, and J. Steel. 2015. Advances in universal influenza virus vaccine design and antibody mediated therapies based on conserved regions of the hemagglutinin. Curr. Top. Microbiol. Immunol. 386: 301-321. https://doi.org/10.1007/82_2014_408
  21. Nachbagauer, R., T. J. Wohlbold, A. Hirsh, R. Hai, H. Sjursen, P. Palese, R. J. Cox, and F. Krammer. 2014. Induction of broadly reactive anti-hemagglutinin stalk antibodies by an H5N1 vaccine in humans. J. Virol. 88: 13260-13268. https://doi.org/10.1128/JVI.02133-14
  22. Adar, Y., Y. Singer, R. Levi, E. Tzehoval, S. Perk, C. Banet- Noach, S. Nagar, R. Arnon, and T. Ben-Yedidia. 2009. A universal epitope-based influenza vaccine and its efficacy against H5N1. Vaccine 27: 2099-2107. https://doi.org/10.1016/j.vaccine.2009.02.011
  23. Hemann, E. A., S. M. Kang, and K. L. Legge. 2013. Protective CD8 T cell-mediated immunity against influenza A virus infection following influenza virus-like particle vaccination. J. Immunol. 191: 2486-2494. https://doi.org/10.4049/jimmunol.1300954
  24. Zeng, W., A. C. Tan, K. Horrocks, and D. C. Jackson. 2015. A lipidated form of the extracellular domain of influenza M2 protein as a self-adjuvanting vaccine candidate. Vaccine 33: 3526-3532. https://doi.org/10.1016/j.vaccine.2015.05.053
  25. Gibbons, R. V. 2010. Dengue conundrums. Int. J. Antimicrob. Agents 36 Suppl 1: S36-S39. https://doi.org/10.1016/j.ijantimicag.2010.06.019
  26. Weiskopf, D., and A. Sette. 2014. T-cell immunity to infection with dengue virus in humans. Front. Immunol. 5: 93.
  27. McKittrick, N., I. Frank, J. M. Jacobson, C. J.W hite, D. Kim, R. Kappes, C. DiGiorgio, T. Kenney, J. Boyer, and P. Tebas. 2013. Improved immunogenicity with high-dose seasonal influenza vaccine in HIV-infected persons: a single-center, parallel, randomized trial. Ann. Intern. Med. 158: 19-26. https://doi.org/10.7326/0003-4819-158-1-201301010-00005
  28. Berger, C. T., V. Greiff, M. Mehling, S. Fritz, M. A. Meier, G. Hoenger, A. Conen, M. Recher, M. Battegay, S. T. Reddy, and C. Hess. 2015. Influenza vaccine response profiles are affected by vaccine preparation and preexisting immunity, but not HIV infection. Hum. Vaccin. Immunother. 11: 391-396. https://doi.org/10.1080/21645515.2015.1008930
  29. Sallusto, F., A. Lanzavecchia, K. Araki, and R. Ahmed. 2010. From vaccines to memory and back. Immunity 33: 451-463. https://doi.org/10.1016/j.immuni.2010.10.008
  30. Tricco, A. C., A. Chit, C. Soobiah, D. Hallett, G. Meier, M. H. Chen, M. Tashkandi, C. T. Bauch, and M. Loeb. 2013. Comparing influenza vaccine efficacy against mismatched and matched strains: a systematic review and meta-analysis. BMC Med. 11: 153.
  31. Johns, M. C., A. A. Eick, D. L. Blazes, S. E. Lee, C. L. Perdue, R. Lipnick, K. G. Vest, K. L. Russell, R. F. DeFraites, and J. L. Sanchez. 2010. Seasonal influenza vaccine and protection against pandemic (H1N1) 2009-associated illness among US military personnel. PLoS One 5: e10722.
  32. Eick-Cost, A. A., K. J. Tastad, A. C. Guerrero, M. C. Johns, S. E. Lee, V. H. Macintosh, R. L. Burke, D. L. Blazes, K. L. Russell, and J. L. Sanchez. 2012. Effectiveness of seasonal influenza vaccines against influenza-associated illnesses among US military personnel in 2010-11: a case-control approach. PLoS One 7: e41435.
  33. Bergtold, A., D. D. Desai, A. Gavhane, and R. Clynes. 2005. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23: 503-514. https://doi.org/10.1016/j.immuni.2005.09.013
  34. Batista, F. D., and M. S. Neuberger. 2000. B cells extract and present immobilized antigen: implications for affinity discrimination. EMBO J. 19: 513-520. https://doi.org/10.1093/emboj/19.4.513
  35. Faix, D. J., A. W. Hawksworth, C. A. Myers, C. J. Hansen, R. G. Ortiguerra, R. Halpin, D. Wentworth, L. A. Pacha, E. G. Schwartz, S. M. Garcia, A. A. Eick-Cost, C. D. Clagett, S. Khurana, H. Golding, and P. J. Blair. 2012. Decreased serologic response in vaccinated military recruits during 2011 correspond to genetic drift in concurrent circulating pandemic A/H1N1 viruses. PLoS One 7: e34581.
  36. Skowronski, D. M., N. Z. Janjua, S. G. De, S. Sabaiduc, A. Eshaghi, J. A. Dickinson, K. Fonseca, A. L. Winter, J. B. Gubbay, M. Krajden, M. Petric, H. Charest, N. Bastien, T. L. Kwindt, S. M. Mahmud, C. P. Van, and Y. Li. 2014. Low 2012- 13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLoS One 9: e92153.
  37. Chambers, B. S., K. Parkhouse, T. M. Ross, K. Alby, and S. E. Hensley. 2015. Identification of hemagglutinin residues responsible for H3N2 antigenic drift during the 2014-2015 influenza season. Cell Rep. 12: 1-6. https://doi.org/10.1016/j.celrep.2015.06.005
  38. Hancock, K., V. Veguilla, X. Lu, W. Zhong, E. N. Butler, H. Sun, F. Liu, L. Dong, J. R. DeVos, P. M. Gargiullo, T. L. Brammer, N. J. Cox, T. M. Tumpey, and J. M. Katz. 2009. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N. Engl. J. Med. 361: 1945-1952. https://doi.org/10.1056/NEJMoa0906453
  39. Dormitzer, P. R., G. Galli, F. Castellino, H. Golding, S. Khurana, G. G. Del, and R. Rappuoli. 2011. Influenza vaccine immunology. Immunol. Rev. 239: 167-177. https://doi.org/10.1111/j.1600-065X.2010.00974.x
  40. Neumann, G., and Y. Kawaoka. 2011. The first influenza pandemic of the new millennium. Influenza Other Respir. Viruses 5: 157-166. https://doi.org/10.1111/j.1750-2659.2011.00231.x
  41. Tan, G. S., P. E. Leon, R. A. Albrecht, I. Margine, A. Hirsh, J. Bahl, and F. Krammer. 2016. Broadly-reactive neutralizing and non-neutralizing antibodies directed against the H7 influenza virus hemagglutinin reveal divergent mechanisms of protection. PLoS Pathog. 12: e1005578.
  42. Viboud, C., J. Eisenstein, A. H. Reid, T. A. Janczewski, D. M. Morens, and J. K. Taubenberger. 2013. Age- and sex-specific mortality associated with the 1918-1919 influenza pandemic in Kentucky. J. Infect. Dis. 207: 721-729. https://doi.org/10.1093/infdis/jis745
  43. Reed, C., S. S. Chaves, A. Perez, T. D'Mello, K. P. Daily, D. Aragon, J. I. Meek, M. M. Farley, P. Ryan, R. Lynfield, C. A. Morin, E. B. Hancock, N. M. Bennett, S. M. Zansky, A. Thomas, M. L. Lindegren, W. Schaffner, and L. Finelli. 2014. Complications among adults hospitalized with influenza: a comparison of seasonal influenza and the 2009 H1N1 pandemic. Clin. Infect. Dis. 59: 166-174. https://doi.org/10.1093/cid/ciu285
  44. Morens, D. M., J. K. Taubenberger, G. K. Folkers, and A. S. Fauci. 2010. Pandemic influenza's 500th anniversary. Clin. Infect. Dis. 51: 1442-1444. https://doi.org/10.1086/657429
  45. Tumpey, T. M., C. F. Basler, P. V. Aguilar, H. Zeng, A. Solorzano, D. E. Swayne, N. J. Cox, J. M. Katz, J. K. Taubenberger, P. Palese, and A. Garcia-Sastre. 2005. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310: 77-80. https://doi.org/10.1126/science.1119392
  46. Epstein, S. L., C. Y. Lo, J. A. Misplon, and J. R. Bennink. 1998. Mechanism of protective immunity against influenza virus infection in mice without antibodies. J. Immunol. 160: 322-327. https://doi.org/10.4049/jimmunol.160.1.322
  47. Zaiss, D. M., C. J. Boog, E. W. van, and A. J. Sijts. 2010. Considerations in the design of vaccines that induce CD8 T cell mediated immunity. Vaccine 28: 7716-7722. https://doi.org/10.1016/j.vaccine.2010.08.101
  48. Murali-Krishna, K., L. L. Lau, S. Sambhara, F. Lemonnier, J. Altman, and R. Ahmed. 1999. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 286: 1377-1381. https://doi.org/10.1126/science.286.5443.1377
  49. Shane, H. L., and K. D. Klonowski. 2014. Every breath you take: the impact of environment on resident memory CD8 T cells in the lung. Front. Immunol. 5: 320.
  50. Liang, S., K. Mozdzanowska, G. Palladino, and W. Gerhard. 1994. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 152: 1653-1661. https://doi.org/10.4049/jimmunol.152.4.1653
  51. Wu, T., Y. Hu, Y. T. Lee, K. R. Bouchard, A. Benechet, K. Khanna, and L. S. Cauley. 2014. Lung-resident memory CD8 T cells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection. J. Leukoc. Biol. 95: 215-224. https://doi.org/10.1189/jlb.0313180
  52. Kash, J. C., T. M. Tumpey, S. C. Proll, V. Carter, O. Perwitasari, M. J. Thomas, C. F. Basler, P. Palese, J. K. Taubenberger, A. Garcia-Sastre, D. E. Swayne, and M. G. Katze. 2006. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443: 578-581. https://doi.org/10.1038/nature05181
  53. Taubenberger, J. K., and D. M. Morens. 2008. The pathology of influenza virus infections. Annu. Rev. Pathol. 3: 499-522. https://doi.org/10.1146/annurev.pathmechdis.3.121806.154316
  54. Schmid, M. A., M. S. Diamond, and E. Harris. 2014. Dendritic cells in dengue virus infection: targets of virus replication and mediators of immunity. Front. Immunol. 5: 647.
  55. Avirutnan, P., P. Malasit, B. Seliger, S. Bhakdi, and M. Husmann. 1998. Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J. Immunol. 161: 6338-6346. https://doi.org/10.4049/jimmunol.161.11.6338
  56. Dalrymple, N., and E. R. Mackow. 2011. Productive dengue virus infection of human endothelial cells is directed by heparan sulfate-containing proteoglycan receptors. J. Virol. 85: 9478-9485. https://doi.org/10.1128/JVI.05008-11
  57. Ghebrehiwet, B., and E. I. Peerschke. 2004. cC1q-R (calreticulin) and gC1q-R/p33: ubiquitously expressed multiligand binding cellular proteins involved in inflammation and infection. Mol. Immunol. 41: 173-183. https://doi.org/10.1016/j.molimm.2004.03.014
  58. Dalrymple, N. A., and E. R. Mackow. 2014. Virus interactions with endothelial cell receptors: implications for viral pathogenesis. Curr. Opin. Virol. 7: 134-140. https://doi.org/10.1016/j.coviro.2014.06.006
  59. Thomas, K. A., N. M. Valenzuela, and E. F. Reed. 2015. The perfect storm: HLA antibodies, complement, FcgammaRs, and endothelium in transplant rejection. Trends Mol. Med. 21: 319-329. https://doi.org/10.1016/j.molmed.2015.02.004
  60. Beltramello, M., K. L. Williams, C. P. Simmons, A. Macagno, L. Simonelli, N. T. Quyen, S. Sukupolvi-Petty, E. Navarro-Sanchez, P. R. Young, A. M. de Silva, F. A. Rey, L. Varani, S. S. Whitehead, M. S. Diamond, E. Harris, A. Lanzavecchia, and F. Sallusto. 2010. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8: 271-283. https://doi.org/10.1016/j.chom.2010.08.007
  61. Short, K. R., E. J. Veldhuis Kroeze, L. A. Reperant, M. Richard, and T. Kuiken. 2014. Influenza virus and endothelial cells: a species specific relationship. Front. Microbiol. 5: 653.
  62. Monsalvo, A. C., J. P. Batalle, M. F. Lopez, J. C. Krause, J. Klemenc, J. Z. Hernandez, B. Maskin, J. Bugna, C. Rubinstein, L. Aguilar, L. Dalurzo, R. Libster, V. Savy, E. Baumeister, L. Aguilar, G. Cabral, J. Font, L. Solari, K. P. Weller, J. Johnson, M. Echavarria, K. M. Edwards, J. D. Chappell, J. E. Crowe, Jr., J. V. Williams, G. A. Melendi, and F. P. Polack. 2011. Severe pandemic 2009 H1N1 influenza disease due to pathogenic immune complexes. Nat. Med. 17: 195-199. https://doi.org/10.1038/nm.2262