Original antigenic sin: A comprehensive review

Journal of Autoimmunity

Volumn 83, Issue , 2017, Pages 12-21

  Vatti, Anup ^a   Monsalve, Diana M ^b   Pacheco, Yovana ^b   Chang, Christopher ^a   Anaya, Juan Manuel ^b   Gershwin, M Eric ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD DEL ROSARIO   (Colombia)

Author keywords

Antibody dependent enhancement; Bocavirus; Dengue; Influenza; Memory immune response; Vaccination; Zika virus

Indexed keywords

ANTIGEN; EPITOPE; VACCINE;

ANTIBODY DEPENDENT ENHANCEMENT; CHLAMYDIA TRACHOMATIS; DENGUE VIRUS; ENTEROVIRUS; HUMAN BOCAVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFLUENZA VIRUS; LEPTOSPIROSIS; NONHUMAN; PLASMODIUM; PRIORITY JOURNAL; REVIEW; SECONDARY IMMUNE RESPONSE; ZIKA VIRUS; ANIMAL; BIOLOGICAL MODEL; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFECTION;

ANIMALS; ANTIGENS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, HUMORAL; IMMUNODOMINANT EPITOPES; IMMUNOLOGIC MEMORY; INFECTION; MODELS, IMMUNOLOGICAL; VACCINES;

EID: 85018263565     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2017.04.008     Document Type: Review

References (70)

1. ORIGINAL antigenic sin, N Engl J Med 258 (1958), 1016–1017.
2. Fazekas de St, G., Webster, R.G., Disquisitions on original antigenic sin. II. Proof in lower creatures. J. Exp. Med. 124 (1966), 347–361.
3. Fazekas de St, G., Webster, R.G., Disquisitions of original antigenic sin. I. Evidence in man. J. Exp. Med. 124 (1966), 331–345.
4. Inouye, S., Matsuno, S., Tsurukubo, Y., “Original antigenic sin” phenomenon in experimental flavivirus infections of Guinea pigs: studies by enzyme-linked immunosorbent assay. Microbiol. Immunol. 28:5 (1984), 569–574.
5. East, I.J., Todd, P.E., Leach, S.J., Original antigenic sin: experiments with a defined antigen. Mol. Immunol. 17:12 (1980), 1539–1544.
6. Li, X., Kantola, K., Hedman, L., Arku, B., Hedman, K., Söderlund-Venermo, M., Original antigenic sin with human bocaviruses 1-4. J. general Virol. 96:10 (2015), 3099–3108.
7. Lambert, P.H., Liu, M., Siegrist, C.A., Can successful vaccines teach us how to induce efficient protective immune responses?. Nat. Med. 11:4 Suppl (2005), S54–S62.
8. Francis, T., On the doctrine of original antigenic sin. Proc. Am. Philos. Soc. 104 (1960), 572–578.
9. Angelova, L.A., Shvartsman Ya, S., Original antigenic sin to influenza in rats. Immunology 46:1 (1982), 183–188.
10. Park, M.S., Kim, J.I., Park, S., Lee, I., Park, M.S., Original antigenic sin response to RNA viruses and antiviral immunity. Immune Netw. 16:5 (2016), 261–270.
11. Deutsch, Sylvia, Bussard, A.E., Original antigenic sin at the cellular level I. Antibodies produced by individual cells against cross-reacting haptens. Eur. J. Immunol. 2:4 (1972), 374–378.
12. Deutsch, S., Vinit, M.A., Bussard, A.E., Original antigenic sin at the cellular level. II. Specificity of the antibodies produced by individual cells. Eur. J. Immunol. 3:4 (1973), 235–240.
13. Deutsch, S., Vinit, M.A., Bussard, A.E., Original antigenic sin at the cellular level-III. Importance of protein carrier in the stimulation process. Immunochemistry 12:3 (1975), 191–197.
14. Midgley, C.M., Bajwa-Joseph, M., Vasanawathana, S., Limpitikul, W., Wills, B., Flanagan, A., Waiyaiya, E., Tran, H.B., Cowper, A.E., Chotiyarnwong, P., Chotiyarnwon, P., Grimes, J.M., Yoksan, S., Malasit, P., Simmons, C.P., Mongkolsapaya, J., Screaton, G.R., An in-depth analysis of original antigenic sin in dengue virus infection. J. Virol. 85:1 (2011), 410–421.
15. Taylor, A., Foo, S.S., Bruzzone, R., Dinh, L.V., King, N.J., Mahalingam, S., Fc receptors in antibody-dependent enhancement of viral infections. Immunol. Rev. 268:1 (2015), 340–364.
16. Rothman, A.L., Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11:8 (2011), 532–543.
17. Singh, R.A., Rodgers, J.R., Barry, M.A., The role of T cell antagonism and original antigenic sin in genetic immunization. J. Immunol. Baltim. Md. 1950) 169:12 (2002), 6779–6786.
18. Weiskopf, D., Angelo, M.A., de Azeredo, E.L., Sidney, J., Greenbaum, J.A., Fernando, A.N., Broadwater, A., Kolla, R.V., De Silva, A.D., de Silva, A.M., Mattia, K.A., Doranz, B.J., Grey, H.M., Shresta, S., Peters, B., Sette, A., Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. Proc. Natl. Acad. Sci. U. S. A. 110:22 (2013), E2046–E2053.
19. Klenerman, P., Zinkernagel, R.M., Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature 394:6692 (1998), 482–485.
20. Kantola, K., Hedman, L., Arthur, J., Alibeto, A., Delwart, E., Jartti, T., Ruuskanen, O., Hedman, K., Söderlund-Venermo, M., Seroepidemiology of human bocaviruses 1-4. J. Infect. Dis. 204:9 (2011), 1403–1412.
21. Linderman, S.L., Hensley, S.E., Antibodies with 'original antigenic sin' properties are valuable components of secondary immune responses to influenza viruses. PLoS Pathog., 12, 2016, e1005806.
22. Halstead, S.B., Rojanasuphot, S., Sangkawibha, N., Original antigenic sin in dengue. Am. J. Trop. Med. Hyg. 32:1 (1983), 154–156.
23. Rothman, A.L., Medin, C.L., Friberg, H., Currier, J.R., Immunopathogenesis versus protection in dengue virus infections. Curr. Trop. Med. Rep. 1:1 (2014), 13–20.
24. Friberg, H., Bashyam, H., Toyosaki-Maeda, T., Potts, J.A., Greenough, T., Kalayanarooj, S., Gibbons, R.V., Nisalak, A., Srikiatkhachorn, A., Green, S., Stephens, H.A., Rothman, A.L., Mathew, A., Cross-reactivity and expansion of dengue-specific T cells during acute primary and secondary infections in humans. Sci. Rep., 1, 2011, 51.
25. Mongkolsapaya, J., Dejnirattisai, W., Xu, X.N., Vasanawathana, S., Tangthawornchaikul, N., Chairunsri, A., Sawasdivorn, S., Duangchinda, T., Dong, T., Rowland-Jones, S., Yenchitsomanus, P.T., McMichael, A., Malasit, P., Screaton, G., Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat. Med. 9:7 (2003), 921–927.
26. Duangchinda, T., Dejnirattisai, W., Vasanawathana, S., Limpitikul, W., Tangthawornchaikul, N., Malasit, P., Mongkolsapaya, J., Screaton, G., Immunodominant T-cell responses to dengue virus NS3 are associated with DHF. Proc. Natl. Acad. Sci. U. S. A. 107:39 (2010), 16922–16927.
27. Mangada, M.M., Endy, T.P., Nisalak, A., Chunsuttiwat, S., Vaughn, D.W., Libraty, D.H., Green, S., Ennis, F.A., Rothman, A.L., Dengue-specific T cell responses in peripheral blood mononuclear cells obtained prior to secondary dengue virus infections in Thai schoolchildren. J. Infect. Dis. 185:12 (2002), 1697–1703.
28. Gunther, V.J., Putnak, R., Eckels, K.H., Mammen, M.P., Scherer, J.M., Lyons, A., Sztein, M.B., Sun, W., A human challenge model for dengue infection reveals a possible protective role for sustained interferon gamma levels during the acute phase of illness. Vaccine 29:22 (2011), 3895–3904.
29. Chang, C., Ortiz, K., Ansari, A., Gershwin, M.E., The Zika outbreak of the 21st century. J. Autoimmun. 68 (2016), 1–13.
30. Rasmussen, S.A., Jamieson, D.J., Honein, M.A., Petersen, L.R., Zika Virus and Birth Defects–Reviewing The evidence for causality. N. Engl. J. Med. 374 (2016), 1981–1987.
31. Anaya, J.M., Rodriguez, Y., Monsalve, D.M., Vega, D., Ojeda, E., Gonzalez-Bravo, D., et al. A comprehensive analysis and immunobiology of autoimmune neurological syndromes during the Zika virus outbreak in Cucuta. Colomb. J. Autoimmun. 77 (2017), 123–138.
32. Priyamvada, L., Quicke, K.M., Hudson, W.H., Onlamoon, N., Sewatanon, J., Edupuganti, S., Pattanapanyasat, K., Chokephaibulkit, K., Mulligan, M.J., Wilson, P.C., Ahmed, R., Suthar, M.S., Wrammert, J., Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc. Natl. Acad. Sci. U. S. A. 113:28 (2016), 7852–7857.
33. Dejnirattisai, W., Supasa, P., Wongwiwat, W., Rouvinski, A., Barba-Spaeth, G., Duangchinda, T., Sakuntabhai, A., Cao-Lormeau, V.M., Malasit, P., Rey, F.A., Mongkolsapaya, J., Screaton, G.R., Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat. Immunol. 17:9 (2016), 1102–1108.
34. Bardina, S.V., Bunduc, P., Tripathi, S., Duehr, J., Frere, J.J., Brown, J.A., Nachbagauer, R., Foster, G.A., Krysztof, D., Tortorella, D., Stramer, S.L., García-Sastre, A., Krammer, F., Lim, J.K., Enhancement of Zika virus pathogenesis by preexisting antiflavivirus immunity. Sci. (New York, N.Y.) 356:6334 (2017), 175–180.
35. Adalja, A.A., Henderson, D.A., Original antigenic sin and pandemic (H1N1) 2009. Emerg. Infect. Dis. 16:6 (2010), 1028–1029.
36. Kim, J.H., Skountzou, I., Compans, R., Jacob, J., Original antigenic sin responses to influenza viruses. J. Immunol. Baltim. Md. 1950) 183:5 (2009), 3294–3301.
37. Nachbagauer, R., Choi, A., Hirsh, A., Margine, I., Iida, S., Barrera, A., Ferres, M., Albrecht, R.A., García-Sastre, A., Bouvier, N.M., Ito, K., Medina, R.A., Palese, P., Krammer, F., Defining the antibody cross-reactome directed against the influenza virus surface glycoproteins. Nat. Immunol. 18:4 (2017), 464–473.
38. Reichert, T., Chowell, G., Nishiura, H., Christensen, R.A., McCullers, J.A., Does Glycosylation as a modifier of Original Antigenic Sin explain the case age distribution and unusual toxicity in pandemic novel H1N1 influenza?. BMC Infect. Dis., 10, 2010, 5.
39. O'Donnell, C.D., Wright, A., Vogel, L., Boonnak, K., Treanor, J.J., Subbarao, K., Humans and ferrets with prior H1N1 influenza virus infections do not exhibit evidence of original antigenic sin after infection or vaccination with the 2009 pandemic H1N1 influenza virus. Clin. Vacc. Immunol. CVI 21:5 (2014), 737–746.
40. Zehn, D., Turner, M.J., Lefrançois, L., Bevan, M.J., Lack of original antigenic sin in recall CD8(+) T cell responses. J. Immunol. Baltim. Md. 1950) 184:11 (2010), 6320–6326.
41. Tsuchiya, H., Furukawa, M., Matsui, M., Katsuki, K., Inouye, S., 'Original antigenic sin' phenomenon in neutralizing antibody responses in children with enterovirus meningitis. J. Clin. Virol. Off. Publ. Pan Am. Soc. Clin. Virol. 19:3 (2000), 205–207.
42. Elmastour, F., Jaidane, H., Aguech-Oueslati, L., Benkahla, M.A., Aouni, M., Gharbi, J., Sane, F., Hober, D., Immunoglobulin G-dependent enhancement of the infection with Coxsackievirus B4 in a murine system. Virulence 7:5 (2016), 527–535.
43. Bopegamage, S., Enterovirus infections: pivoting role of the adaptive immune response. Virulence 7:5 (2016), 495–497.
44. Berry, J.D., Peeling, R.W., Brunham, R.C., Analysis of the original antigenic sin antibody response to the major outer membrane protein of Chlamydia trachomatis. J. Infect. Dis. 179:1 (1999), 180–186.
45. Craig, S.B., Graham, G.C., Burns, M.A., Dohnt, M.F., Smythe, L.D., McKay, D.B., A case of 'original antigenic sin' or just a paradoxical reaction in leptospirosis?. Ann. Trop. Med. Parasitol. 103:5 (2009), 467–470.
46. Currier, J., Sattabongkot, J., Good, M.F., 'Natural' T cells responsive to malaria: evidence implicating immunological cross-reactivity in the maintenance of TCR alpha beta+ malaria-specific responses from non-exposed donors. Int. Immunol. 4:9 (1992), 985–994.
47. Beyer, W.E., Van der Logt, J.T., van Beek, R., Masurel, N., Immunoglobulin, G., A and M response to influenza vaccination in different age groups: effects of priming and boosting. J. Hyg. (Lond) 96 (1986), 513–522.
48. Ma, J., Dushoff, J., Earn, D.J., Age-specific mortality risk from pandemic influenza. J. Theor. Biol. 288 (2011), 29–34.
49. Masurel, N., Drescher, J., Production of highly cross-reactive hemagglutination-inhibiting influenza antibodies in ferrets. Infect. Immun. 13:4 (1976), 1023–1029.
50. McElhaney, J.E., Meneilly, G.S., Lechelt, K.E., Beattie, B.L., Bleackley, R.C., Antibody response to whole-virus and split-virus influenza vaccines in successful ageing. Vaccine 11:10 (1993), 1055–1060.
51. Thompson, M.A., Raychaudhuri, S., Cancro, M.P., Restricted adult clonal profiles induced by neonatal immunization. Influence of suppressor T cells. J. Exp. Med. 158:1 (1983), 112–125.
52. Virelizier, J.L., Allison, A.C., Schild, G.C., Antibody responses to antigenic determinants of influenza virus hemagglutinin. II. Original antigenic sin: a bone marrow-derived lymphocyte memory phenomenon modulated by thymus-derived lymphocytes. J. Exp. Med. 140 (1974), 1571–1578.
53. Webster, R.G., Kasel, J.A., Couch, R.B., Laver, W.G., Influenza virus subunit vaccines. II. Immunogenicity and original antigenic sin in humans. J. Infect. Dis. 134:1 (1976), 48–58.
54. Yarchoan, R., Nelson, D.L., Specificity of in vitro anti-influenza virus antibody production by human lymphocytes: analysis of original antigenic sin by limiting dilution cultures. J. Immunol. 132 (1984), 928–935.
55. Good, M.F., Zevering, Y., Currier, J., Bilsborough, J., 'Original antigenic sin', T cell memory, and malaria sporozoite immunity: an hypothesis for immune evasion. Parasite Immunol. 15:4 (1993), 187–193.
56. Kuno, G., Gubler, D.J., Oliver, A., Use of 'original antigenic sin' theory to determine the serotypes of previous dengue infections. Trans. R. Soc. Trop. Med. Hyg. 87:1 (1993 Jan-Feb), 103–105.
57. Zompi, S., Harris, E., Original antigenic sin in dengue revisited. Proc. Natl. Acad. Sci. U. S. A. 110:22 (2013), 8761–8762.
58. Kantola, K., Hedman, L., Tanner, L., Simell, V., Makinen, M., Partanen, J., et al. B-cell responses to human bocaviruses 1-4: new insights from a childhood follow-up study. PLoS One, 10, 2015, e0139096.
59. Choi, Y.S., Baek, Y.H., Kang, W., Nam, S.J., Lee, J., You, S., Chang, D.Y., Youn, J.C., Choi, Y.K., Shin, E.C., Reduced antibody responses to the pandemic (H1N1) 2009 vaccine after recent seasonal influenza vaccination. Clin. Vacc. Immunol. CVI 18:9 (2011), 1519–1523.
60. Chakradhar, S., Updated, augmented vaccines compete with original antigenic sin. Nat. Med. 21:6 (2015), 540–541.
61. Ndifon, Wilfred, A simple mechanistic explanation for original antigenic sin and its alleviation by adjuvants. J. R. Soc. Interface, 12(112), 2015, 20150627.
62. Kim, J.H., Davis, W.G., Sambhara, S., Jacob, J., Strategies to alleviate original antigenic sin responses to influenza viruses. Proc. Natl. Acad. Sci. U. S. A. 109:34 (2012), 13751–13756.
63. Villar, L., Dayan, G.H., Arredondo-García, J.L., Rivera, D.M., Cunha, R., Deseda, C., Reynales, H., Costa, M.S., Morales-Ramírez, J.O., Carrasquilla, G., Rey, L.C., Dietze, R., Luz, K., Rivas, E., Miranda Montoya, M.C., Cortés Supelano, M., Zambrano, B., Langevin, E., Boaz, M., Tornieporth, N., Saville, M., Noriega, F., CYD15 Study Group, Efficacy of a tetravalent dengue vaccine in children in Latin America. N. Engl. J. Med. 372:2 (2015), 113–123.
64. Anderson, D.E., Carlos, M.P., Nguyen, L., Torres, J.V., Overcoming original (antigenic) sin. Clin. Immunol. Orl. Fla.) 101:2 (2001), 152–157.
65. Haaheim, L.R., Original antigenic sin. A confounding issue?. Dev. Biol. 115 (2003), 49–53.
66. Kucharski, A.J., Gog, J.R., Age profile of immunity to influenza: effect of original antigenic sin. Theor. Popul. Biol. 81:2 (2012), 102–112.
67. Webster, R.G., Original antigenic sin in ferrets: the response to sequential infections with influenza viruses. J. Immunol. Baltim. Md. 1950) 97:2 (1966), 177–183.
68. Frias-Staheli, N., Dorner, M., Marukian, S., Billerbeck, E., Labitt, R.N., Rice, C.M., Ploss, A., Utility of humanized BLT mice for analysis of dengue virus infection and antiviral drug testing. J. Virol. 88:4 (2014), 2205–2218.
69. Whitehead, R.H., Chaicumpa, V., Olson, L.C., Russell, P.K., Sequential dengue virus infections in the white-handed gibbon (Hylobates lar). Am. J. Trop. Med. Hyg. 19:1 (1970), 94–102.
70. Koraka, P., Benton, S., van Amerongen, G., Stittelaar, K.J., Osterhaus, A.D., Characterization of humoral and cellular immune responses in cynomolgus macaques upon primary and subsequent heterologous infections with dengue viruses. Microb. Infect. 9:8 (2007), 940–946.