650
Views
48
CrossRef citations to date
0
Altmetric
Research Article

Heterologous immunity: Immunopathology, autoimmunity and protection during viral infections

, , , , , & show all
Pages 328-347 | Published online: 20 Jan 2011

References

  • Posnett DN. Herpesviruses and autoimmunity. Curr Opin Investig Drugs. 2008; 9 5: 505–514.
  • Sips GJ, Chesik D, Glazenburg L, Wilschut J, De KJ, Wilczak N. Involvement of morbilliviruses in the pathogenesis of demyelinating disease. Rev Med Virol. 2007; 17 4: 223–244.
  • Libbey JE, McCoy LL, Fujinami RS. Molecular mimicry in multiple sclerosis. Int Rev Neurobiol. 2007; 79:127–147.
  • Welsh RM, Fujinami RS. Pathogenic epitopes, heterologous immunity and vaccine design. Nat Rev Microbiol. 2007; 5 7: 555–563.
  • Sotelo J, Martinez-Palomo A, Ordonez G, Pineda B. Varicella-zoster virus in cerebrospinal fluid at relapses of multiple sclerosis. Ann Neurol. 2008; 63 3: 303–311.
  • Giraudon P, Bernard A. Chronic viral infections of the central nervous system: Aspects specific to multiple sclerosis. Rev Neurol (Paris). 2009; 165 10: 789–795.
  • Requena L, Requena C. Erythema nodosum. Dermatol Online. 2002; 8:4.
  • Smoller BR, Weishar M, Gray MH. An unusual cutaneous manifestation in Crohn's disease. Arch Pathol Lab Med. 1990; 6:609–610.
  • Schlesinger C, Meyer CA, Veeraraghavan S, Koss MN. Constrictive (obliterative) bronchiolitis: Diagnosis, etiology, and a critical review of the literature. Ann Diagn Pathol. 1998; 2:321–334.
  • Jones JF, Ray CG, Minnich LL, Hicks MJ, Kibler R, Lucas DO. Evidence for active Epstein-Barr virus infection in patients with persistent, unexplained illnesses: Elevated anti-early antigen antibodies. Ann Intern Med. 1985; 102:1–7.
  • Ho-Yen DO, McNamara I. The epidemiology of post viral fatigue syndrome. Scott Med J. 1988; 33:368–369.
  • Evans AC. Brucellosis in the United States. Am J Public Health. 1947; 37:139–151.
  • Truss CO. The role of Candida albicans in human illness. J Orthomol Psych. 1981; 10:228–238.
  • Daugherty SA, Henry BE, Peterson DL, Swarts RL, Bastien S, Thomas RS. Chronic fatigue syndrome in northern Nevada. Rev Infect Dis. 1991; 13 suppl 1: S39–S44.
  • Buchwald D, Cheney PR, Peterson DL, Henry B, Wormsley SB, Geiger A, Ablashi DV, Salahuddin SZ, Saxinger C, Biddle R, Kikinis R, Jolesz FA, Folks T, Balachandran N, Peter JB, Gallo RC, Komaroff AL. A chronic illness characterized by fatigue, neurologic and immunologic disorders, and active herpesvirus type 6 infection. Ann Intern Med. 1992; 116:103–113.
  • Chia JK, Chia AY. Chronic fatigue syndrome is associated with chronic enterovirus infection of the stomach. J Clin Pathol. 2008; 61 1: 43–48.
  • Chia JK. The role of enterovirus in chronic fatigue syndrome. J Clin Pathol. 2005; 58 11: 1126–1132.
  • Lombardi VC, Ruscetti FW, Das GJ, Pfost MA, Hagen KS, Peterson DL, Ruscetti SK, Bagni RK, Petrow-Sadowski C, Gold B, Dean M, Silverman RH, Mikovits JA. Detection of an infectious retrovirus, XMRV, in blood cells of patients with chronic fatigue syndrome. Science. 2009; 326 5952: 585–589.
  • Jones JF. Serologic and immunologic responses in chronic fatigue syndrome with emphasis on the Epstein-Barr virus. Rev Infect Dis. 1991; 13 suppl 1: S26–S31.
  • Selin LK, Nahill SR, Welsh RM. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J Exp Med. 1994; 179:1933–1943.
  • Brehm MA, Pinto AK, Daniels KA, Schneck JP, Welsh RM, Selin LK. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat Immunol. 2002; 3 7: 627–634.
  • Selin LK, Vergilis K, Welsh RM, Nahill SR. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J Exp Med. 1996; 183:2489–2499.
  • Selin LK, Lin MY, Kraemer KA, Schneck JP, Pardoll D, Varga SM, Santolucito PA, Pinto AK, Welsh RM. Attrition of T cell memory: Selective loss of lymphocytic choriomeningitis virus (LCMV) epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity. 1999; 11:733–742.
  • Selin LK, Varga SM, Wong IC, Welsh RM. Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations. J Exp Med. 1998; 188:1705–1715.
  • Welsh RM, Selin LK. No one is naïve: The significance of heterologous T-cell immunity. Nat Rev Immunol. 2002; 2 6: 417–426.
  • Rock KL, York IA, Saric T, Goldberg AL. Protein degradation and the generation of MHC class I-presented peptides. Adv Immunol. 1903; 80:1–70 JID 0370425.
  • Doherty PC, Zinkernagel RM. T-cell-mediated immunopathology in viral infections. Transplant Rev. 1974; 19:89–120.
  • Marshall DR, Turner SJ, Belz GT, Wingo S, Andreansky S, Sangster MY, Riberdy JM, Liu T, Tan M, Doherty PC. Measuring the diaspora for virus-specific CD8+ T cells. Proc Natl Acad Sci USA. 2001; 98:6313–6318.
  • Kaech SM, Ahmed R. Memory CD8+ T cell differentiation: Initial antigen encounter triggers a developmental program in naïve cells. Nat Immunol. 2001; 2:415–422.
  • Mercado R, Vijh S, Allen SE, Kerksiek K, Pilip IM, Pamer EG. Early programming of T cell populations responding to bacterial infection. J Immunol. 2000; 165:6833–6839.
  • van Stipdonk MJ, Lemmens EE, Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol. 2001; 2:423–429.
  • Borrow P, Tishon A, Lee S, Xu J, Grewal IS, Oldstone MB, Flavell RA. CD40L-deficient mice show deficits in antiviral immunity and have an impaired memory CD8+ CTL response. J Exp Med. 1996; 183:2129–2142.
  • Williams MA, Tyznik AJ, Bevan MJ. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature. 2006; 441 7095: 890–893.
  • York IA, Brehm MA, Zendzian S, Towne CF, Rock KL. Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivo and plays an important role in immunodominance. Proc Natl Acad Sci USA. 2006; 103 24: 9202–9207.
  • Razvi ES, Welsh RM, McFarland HI. In vivo state of antiviral CTL precursors: Characterization of a cycling population containing CTL precursors in immune mice. J Immunol. 1995; 154:620–632.
  • Selin LK, Welsh RM. Cytolytically active memory CTL present in lymphocytic choriomeningitis virus (LCMV)-immune mice after clearance of virus infection. J Immunol. 1997; 158:5366–5373.
  • Zimmermann C, Brduscha-Riem K, Blaser C, Zinkernagel RM, Pircher H. Visualization, characterization, and turnover of CD8+ memory T cells in virus-infected hosts. J Exp Med. 1996; 183:1367–1375.
  • McNally JM, Zarozinski CC, Lin MY, Brehm MA, Chen HD, Welsh RM. Attrition of bystander CD8 T cells during virus-induced T cell and interferon responses. J Virol. 2001; 75:5965–5976.
  • Tumpey TM, Lu X, Morken T, Zaki SR, Katz JM. Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (H5N1) virus isolated from humans. J Virol. 2000; 74 13: 6105–6116 JID 0113724.
  • Geisbert TW, Hensley LE, Gibb TR, Steele KE, Jaax NK, Jahrling PB. Apoptosis induced in vitro and in vivo during infection by Ebola and Marburg viruses. Lab Invest. 2000; 80 2: 171–186 JID 0376617.
  • Dietz WHJ, Peralta PH, Johnson KM. Ten clinical cases of human infection with venezuelan equine encephalomyelitis virus, subtype I-D. Am J Trop Med Hyg. 1979; 28 2: 329–334 JID 0370507.
  • Bahl K, Kim SK, Calcagno C, Ghersi D, Puzone R, Celada F, Selin LK, Welsh RM. IFN-induced attrition of CD8 T cells in the presence or absence of cognate antigen during the early stages of viral infections. J Immunol. 2006; 176 7: 4284–4295.
  • Jiang J, Gross D, Nogusa S, Elbaum P, Murasko DM. Depletion of T cells by type I interferon: Differences between young and aged mice. J Immunol. 2005; 175 3: 1820–1826.
  • Jiang J, Lau LL, Shen H. Selective depletion of nonspecific T cells during the early stage of immune responses to infection. J Immunol. 2003; 171 8: 4352–4358.
  • Selin LK, Cornberg M, Brehm MA, Kim SK, Calcagno C, Ghersi D, Puzone R, Celada F, Welsh RM. CD8 memory T cells: Cross-reactivity and heterologous immunity. Semin Immunol. 2004; 16 5: 335–347.
  • Selin LK, Welsh RM. Plasticity of T cell memory responses to viruses. Immunity. 2004; 20 1: 5–16.
  • Kim SK, Welsh RM. Comprehensive early and lasting loss of memory CD8 T cells and functional memory during acute and persistent viral infections. J Immunol. 2004; 172 5: 3139–3150.
  • Yewdell JW, Bennink JR. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol. 1999; 17:51–88.
  • Clute SC, Watkin LB, Cornberg M, Naumov YN, Sullivan JL, Luzuriaga K, Welsh RM, Selin LK. Cross-reactive influenza virus-specific CD8+ T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis. J Clin Invest. 2005; 115 12: 3602–3612.
  • Mason D. A very high level of crossreactivity is an essential feature of the T cell repertoire. Immunol Today. 1998; 19:395–404.
  • Wilson DB, Wilson DH, Schroder K, Pinilla C, Blondelle S, Houghten RA, Garcia KC. Specificity and degeneracy of T cells. Mol Immunol. 2004; 40 14-15: 1047–1055.
  • Selin LK, Brehm MA. Frontiers in nephrology: Heterologous immunity, T cell cross-reactivity, and alloreactivity. J Am Soc Nephrol. 2007; 18 8: 2268–2277.
  • Welsh RM, Che JW, Brehm MA, Selin LK. Heterologous immunity between viruses. Immunol Rev. 2010; 235 1: 244–266.
  • Welsh RM, Selin LK, Szomolanyi-Tsuda E. Immunological memory to viral infections. Annu Rev Immunol. 2004; 22:711–743.
  • Acierno PM, Newton DA, Brown EA, Maes LA, Baatz JE, Gattoni-Celli S. Cross-reactivity between HLA-A2-restricted FLU-M1:58-66 and HIV p17 GAG:77-85 epitopes in HIV-infected and uninfected individuals. J Transl Med. 2003; 1:3–7.
  • Nilges K, Hohn H, Pilch H, Neukirch C, Freitag K, Talbot PJ, Maeurer MJ. Human papillomavirus type 16 E7 peptide-directed CD8+ T cells from patients with cervical cancer are cross-reactive with the coronavirus NS2 protein. J Virol. 2003; 77 9: 5464–5474.
  • Frankild S, De Boer RJ, Lund O, Nielsen M, Kesmir C. Amino acid similarity accounts for T cell cross-reactivity and for ‘holes’ in the T cell repertoire. PLoS ONE. 2008; 3 3: e1831.
  • Bahl K, Huebner A, Davis RJ, Welsh RM. Analysis of apoptosis of memory T cells and dendritic cells during the early stages of viral infection or exposure to toll-like receptor agonists. J Virol. 2010; 84 10: 4866–4877.
  • van der Most RG, Sette A, Oseroff C, Alexander J, Murali-Krishna K, Lau LL, Southwood S, Sidney J, Chesnut RW, Matloubian M, Ahmed R. Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J Immunol. 1996; 157 12: 5543–5554.
  • Whitton JL, Southern PJ, Oldstone MBA. Analyses of the cytotoxic T lymphocyte responses to glycoprotein and nucleoprotein components of lymphocytic choriomeningitis virus. Virol. 1988; 162:321–327.
  • Chen W, Anton LC, Bennink JR, Yewdell JW. Dissecting the multifactorial causes of immunodominace in class I-restricted T cell responses to viruses. Immunity. 2000; 12:83–93.
  • Vitiello A, Yuan L, Chesnut RW, Sidney J, Southwood S, Farness P, Jackson MR, Peterson PA, Sette A. Immunodominance analysis of CTL responses to influenza PR8 virus reveals two dominant and subdominant Kb-restricted epitopes. J Immunol. 1996; 157:5555–5562.
  • Maryanski JL, Attuil V, Hamrouni A, Mutin M, Rossi M, Aublin A, Bucher P. Individuality of Ag-selected and preimmune TCR repertoires. Immunol Res. 2001; 23 1: 75–84.
  • Lin MY, Welsh RM. Stability and diversity of T cell receptor (TCR) repertoire usage during lymphocytic choriomeningitis virus infection of mice. J Exp Med. 1998; 188:1993–2005.
  • Blattman JN, Sourdive DJ, Murali-Krishna K, Ahmed R, Altman JD. Evolution of the T cell repertoire during primary, memory, and recall responses to viral infection. J Immunol. 2000; 165:6081–6090.
  • Turner SJ, Kedzierska K, Komodromou H, La Gruta NL, Dunstone MA, Webb AI, Webby R, Walden H, Xie W, McCluskey J, Purcell AW, Rossjohn J, Doherty PC. Lack of prominent peptide-major histocompatibility complex features limits repertoire diversity in virus-specific CD8+ T cell populations. Nat Immunol. 2005; 6 4: 382–389.
  • Cornberg M, Chen AT, Wilkinson LA, Brehm MA, Kim SK, Calcagno C, Ghersi D, Puzone R, Celada F, Welsh RM, Selin LK. Narrowed TCR repertoire and viral escape as a consequence of heterologous immunity. J Clin Invest. 2006; 116 5: 1443–1456.
  • Kim SK, Cornberg M, Wang XZ, Chen HD, Selin LK, Welsh RM. Private specificities of CD8 T cell responses control patterns of heterologous immunity. J Exp Med. 2005; 201 4: 523–533.
  • Nie S, Lin SJ, Kim SK, Welsh RM, Selin LK. Pathological features of heterologous immunity are regulated by the private specificities of the immune repertoire. Am J Pathol. 2010; 176 5: 2107–2112.
  • Urbani S, Amadei B, Fisicaro P, Pilli M, Missale G, Bertoletti A, Ferrari C. Heterologous T cell immunity in severe hepatitis C virus infection. J Exp Med. 2005; 201:675–680.
  • Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N, Chairunsri A, Sawasdivorn S, Duangchinda T, Dong T, Rowland-Jones S, Yenchitsomanus PT, McMichael A, Malasit P, Screaton G. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med. 2003; 9 7: 921–927.
  • Kasprowicz V, Ward SM, Turner A, Grammatikos A, Nolan BE, Lewis-Ximines L, Sharp C, Woodfruff J, Fleming VM, Sims S, Walker BD, Sewell AK, Lauer GM, Klenerman P. Defining the directionality and quality of influenza virus-specific CD8 T cell cross-reactivity in individuals infected with hepatitis C virus. J Clin Invest. 2008; 118 3: 1143–1153.
  • Page KR, Scott AL, Manabe YC. The expanding realm of heterologous immunity: Friend or foe?. Cell Microbiol. 2006; 8 2: 185–196.
  • Chen HD, Fraire AE, Joris I, Welsh RM, Selin LK. Specific history of heterologous virus infections determines anti-viral immunity and immunopathology in the lung. Am J Pathol. 2003; 163 4: 1341–1355.
  • Cornberg M, Clute SC, Watkin LB, Saccoccio FM, Kim SK, Naumov YN, Brehm MA, Aslan N, Welsh RM, Selin LK. CD8 T cell cross-reactivity networks mediate heterologous immunity in human EBV and murine vaccinia virus infections. J Immunol. 2010; 184 6: 2825–2838.
  • Chen HD, Fraire AE, Joris I, Brehm MA, Welsh RM, Selin LK. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat Immunol. 2001; 2:1067–1076.
  • Nie S, Cornberg M, Selin LK. Resistance to vaccinia virus is less dependent on TNF under conditions of heterologous immunity. J Immunol. 2009; 183 10: 6554–6560.
  • Kim SK, Brehm MA, Welsh RM, Selin LK. Dynamics of memory T cell proliferation under conditions of heterologous immunity and bystander stimulation. J Immunol. 2002; 169 1: 90–98.
  • Brehm MA, Pinto AK, Daniels KA, Schneck JP, Welsh RM, Selin LK. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat Immunol. 2002; 3:627–634.
  • Cornberg M, Sheridan BS, Saccoccio FM, Brehm MA, Selin LK. Protection against vaccinia virus challenge by CD8 memory T cells resolved by molecular mimicry. J Virol. 2007; 81 2: 934–944.
  • Cole GA, Nathanson N, Prendergast RA. Requirement for q-bearing cells in lymphocytic choriomeningitis virus-induced central nervous system disease. Nature. 1972; 238:335–337.
  • Kapikian AZ, Mitchell RH, Chanock RM, Shvedoff RA, Stewart CE. An epidemiological study of altered clinical reactivity to respiratory syncitial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine. Am J Epidemiol. 1969; 89:405–421.
  • Cannon MJ, Openshaw PJM, Askonas BA. Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J Exp Med. 1988; 168:1163–1168.
  • Graham BS, Bunton LA, Wright PF, Karzon DT. Role of T lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J Clin Invest. 1991; 88:1026–1033.
  • Moskophidis D, Kioussis D. Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J Exp Med. 1998; 188:223–232.
  • Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: Molecular mechanisms and role in T cell biology. Annu Rev Immunol. 1996; 14:1–27.
  • Kersh GJ, Kersh EN, Fremont DH, Allen PM. High- and low-potency ligands with similar affinities for the TCR: The importance of kinetics in TCR signaling. Immunity. 1998; 9:817–826.
  • Ding Y-H, Baker BM, Garboczi DN, Biddison WE, Wiley DC. Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity. 1999; 11:45–56.
  • Hemmer B, Stefanova I, Vergelli M, Germain RN, Martin R. Relationships among TCR ligand potency, thresholds for effector function elicitation, and the quality of early signalling events in human T cells. J Immunol. 1998; 160:5807–5814.
  • Zehn D, Lee SY, Bevan MJ. Complete but curtailed T-cell response to very low-affinity antigen. Nature. 2009; 458 7235: 211–214.
  • Guy CS, Vignali DA. Organization of proximal signal initiation at the TCR:CD3 complex. Immunol Rev. 2009; 232 1: 7–21.
  • Wedemeyer H, Mizukoshi E, Davis AR, Bennink JR, Rehermann B. Cross-reactivity between hepatitis C virus and influenza A virus determinant-specific cytotoxic T cells. J Virol. 2001; 75:11392–11400.
  • Rehermann B, Shin EC. Private aspects of heterologous immunity. J Exp Med. 2005; 201 5: 667–670.
  • Zivny J, DeFronzo M, Jarry W, Jameson J, Cruz J, Ennis FA, Rothman AL. Partial agonist effect influences the CTL response to a heterologous dengue virus serotype. J Immunol. 1999; 163 5: 2754–2760.
  • Yang H, Joris I, Majno G, Welsh RM. Necrosis of adipose tissue induced by sequential infections with unrelated viruses. Am J Pathol. 1985; 120:173–177.
  • Yang H, Dundon PL, Nahill SR, Welsh RM. Virus-induced polyclonal cytotoxic T lymphocyte stimulation. J Immunol. 1989; 142:1710–1718.
  • Moutaftsi M, Salek-Ardakani S, Croft M, Peters B, Sidney J, Grey H, Sette A. Correlates of protection efficacy induced by vaccinia virus-specific CD8+ T-cell epitopes in the murine intranasal challenge model. Eur J Immunol. 2009; 39 3: 717–722.
  • Mathurin KS, Martens GW, Kornfeld H, Welsh RM. CD4 T-cell-mediated heterologous immunity between mycobacteria and poxviruses. J Virol. 2009; 83 8: 3528–3539.
  • Ploegh HL. Viral strategies of immune evasion. Science. 1998; 280:248–253.
  • Xiao Z, Casey KA, Jameson SC, Curtsinger JM, Mescher MF. Programming for CD8 T cell memory development requires IL-12 or type I IFN. J Immunol. 2009; 182 5: 2786–2794.
  • Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med. 2005; 202 5: 637–650.
  • Gilbertson B, Germano S, Steele P, Turner S, Fazekas de St GB, Cheers C. Bystander activation of CD8+ T lymphocytes during experimental mycobacterial infection. Infect Immun. 2004; 72 12: 6884–6891.
  • Berg RE, Crossley E, Murray S, Forman J. Memory CD8+ T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J Exp Med. 2003; 198 10: 1583–1593.
  • Bangs SC, Baban D, Cattan HJ, Li CK, McMichael AJ, Xu XN. Human CD4+ memory T cells are preferential targets for bystander activation and apoptosis. J Immunol. 2009; 182 4: 1962–1971.
  • Polley R, Sanos SL, Prickett S, Haque A, Kaye PM. Chronic Leishmania donovani infection promotes bystander CD8+-T-cell expansion and heterologous immunity. Infect Immun. 2005; 73 12: 7996–8001.
  • Raue HP, Brien JD, Hammarlund E, Slifka MK. Activation of virus-specific CD8+ T cells by lipopolysaccharide-induced IL-12 and IL-18. J Immunol. 2004; 173 11: 6873–6881.
  • Bukowski JF, Welsh RM. Enhanced susceptibility to cytotoxic T lymphocytes of target cells isolated from virus-infected or interferon-treated mice. J Virol. 1986; 59:735–739.
  • Bukowski JF, Welsh RM. Interferon enhances the susceptibility of virus-infected fibroblasts to cytotoxic T cells. J Exp Med. 1985; 161:257–262.
  • Liu F, Whitton JL. Cutting edge: Re-evaluating the in vivo cytokine responses of CD8+ T cells during primary and secondary viral infections. J Immunol. 2005; 174 10: 5936–5940.
  • Haanen JB, Wolkers MC, Kruisbeek AM, Schumacher TN. Selective expansion of cross-reactive CD8(+) memory T cells by viral variants. J Exp Med. 1999; 190 9: 1319–1328.
  • Nettesheim P, Szakal AK. Morphogenesis of alveolar bronchiolization. Lab Invest. 1972; 26:210–219.
  • Wlodarczyk MF, Kraft AR, Chen HD, Kenney LL, Selin LK. Pathological consequences of heterologous immunity prevented by inhibition of cross-reactive influenza A specific memory CD8 T-cells, 2010; submitted for publication.
  • Varga SM, Wang X, Welsh RM, Braciale TJ. Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4+ T cells. Immunity. 2001; 15:637–646.
  • Johnson TR, Graham BS. Secreted respiratory syncytial virus G glcoprotein induces interleukin-5 (IL-5), IL-13, and eosinophilia by an IL-4-dependent mechanism. J Virol. 1999; 73:8485–8495.
  • Walzl G, Tafuro S, Moss P, Openshaw PJ, Hussell T. Influenza virus lung infection protects from respiratory syncitial virus-induced immunopathology. J Exp Med. 2000; 192:1317–1326.
  • Aaby P, Samb B, Simondon F, Seck AM, Knudsen K, Whittle H. Non-specific beneficial effect of measles immunisation: Analysis of mortality studies from developing countries. Br Med J. 1995; 311:481–485.
  • Flanagan KL, Klein S, Skakkebaek NE, Marriott I, Marcha A, Selin LK, Fish E, Prentice A, Whittle H, Benn C, Aaby P. On behalf of the optimize immunization network (optimmunize). Sex-specific and non-specific effects of vaccines: Do they exist and what should be done?, 2010; submitted for publication.
  • Stensballe LG, Nante E, Jensen IP, Kofoed PE, Poulsen A, Jensen H, Newport M, Marchant A, Aaby P. Acute lower respiratory tract infections and respiratory syncytial virus in infants in Guinea-Bissau: A beneficial effect of BCG vaccination for girls community based case-control study. Vaccine. 2005; 23 10: 1251–1257.
  • Farrington CP, Firth MJ, Moulton LH, Ravn H, Andersen PK, Evans S. Epidemiological studies of the non-specific effects of vaccines: II-methodological issues in the design and analysis of cohort studies. Trop Med Int Health. 2009; 14 9: 977–985.
  • Benn CS, Rodrigues A, Yazdanbakhsh M, Fisker AB, Ravn H, Whittle H, Aaby P. The effect of high-dose vitamin A supplementation administered with BCG vaccine at birth may be modified by subsequent DTP vaccination. Vaccine. 2009; 27 21: 2891–2898.
  • Aaby P, Biai S, Veirum JE, Sodemann M, Lisse I, Garly ML, Ravn H, Benn CS, Rodrigues A. DTP with or after measles vaccination is associated with increased in-hospital mortality in Guinea-Bissau. Vaccine. 2007; 25 7: 1265–1269.
  • Jennes W, Verheyden S, Demanet C, Adje-Toure CA, Vuylsteke B, Nkengasong JN, Kestens L. Cutting edge: Resistance to HIV-1 infection among African female sex workers is associated with inhibitory KIR in the absence of their HLA ligands. J Immunol. 2006; 177 10: 658–692.
  • Tillmann HL, Heiken H, Knapik-Botor A, Heringlake S, Ockenga J, Wilber JC, Goergen B, Detmer J, McMorrow M, Stoll M, Schmidt RE, Manns MP. Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med. 2001; 345:715–724.
  • Clute SC, Naumov YN, Watkin LB, Aslan N, Sullivan JL, Luzuriaga K, Welsh RM, Puzone R, Celada F, Selin LK. Broad cross-reactive T cell receptor repertoires recognizing dissimilar Epstein-Barr and influenza A virus epitopes. J Immunol. 2010.
  • Borja-Hart NL, Benavides S, Christensen C. Human papillomavirus vaccine safety in pediatric patients: An evaluation of the vaccine adverse event reporting system. Ann Pharmacother. 2009; 43 2: 356–359.
  • Debeer P, De MP, Bruyninckx F, Devlieger R. Brachial plexus neuritis following HPV vaccination. Vaccine. 2008; 26 35: 4417–4419.
  • Debold V, Hurwitz E. Adverse events and quadrivalent human papillomavirus recombinant vaccine. J Am Med Assoc. 2009; 302 24: 2657–2658.
  • Ojaimi S, Buttery JP, Korman TM. Quadrivalent human papillomavirus recombinant vaccine associated lipoatrophy. Vaccine. 2009; 27 36: 4876–4878.
  • Khalifa YM, Monahan PM, Acharya NR. Ampiginous choroiditis following quadrivalent human papilloma virus vaccine. Br J Ophthalmol. 2010; 94 1: 137–139.
  • Slade BA, Leidel L, Vellozzi C, Woo EJ, Hua W, Sutherland A, Izurieta HS, Ball R, Miller N, Braun MM, Markowitz LE, Iskander J. Postlicensure safety surveillance for quadrivalent human papillomavirus recombinant vaccine. J Am Med Assoc. 2009; 302 7: 750–757.
  • Effros RB, Doherty PC, Gerhard W, Bennink J. Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses. J Exp Med. 1977; 145 3: 557–568.
  • Lee LY, Ha do LA, Simmons C, de Jong MD, Chau NV, Schumacher R, Peng YC, McMichael AJ, Farrar JJ, Smith GL, Townsend AR, Askonas BA, Rowland-Jones S, Dong T. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest. 2008; 118 10: 3478–3490.
  • Epstein SL. Prior H1N1 influenza infection and susceptibility of Cleveland family study participants during the H2N2 pandemic of 1957: An experiment of nature. J Infect Dis. 2006; 193 1: 49–53.
  • Slepushkin AN. The effect of a previous attack of A1 influenza on susceptibility to A2 virus during the 1957 outbreak. Bull World Health Organ. 1959; 20 2-3: 297–301.
  • Moss PAH, Moots RJ, Rosenberg WMC, Rowland-Jones SJ, Bodmer HC, McMichael AJ, Bell JI. Extensive conservation of a and b chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc Natl Acad Sci USA. 1991; 88:8987–8990.
  • Naumov YN, Naumova EN, Yassai MB, Kota K, Welsh RM, Selin LK. Multiple glycines in TCR alpha-chains determine clonally diverse nature of human T cell memory to influenza A virus. J Immunol. 2008; 181 10: 7407–7419.
  • Weinstein L, Meade RH. Respiratory manifestations of chickenpox. Arch Intern Med. 1956; 98:91–99.
  • Rickinson AB, Kieff E. 1996. Epstein-Barr virus. In: Fields BN, Knipe DM, Howley PM, Chanock RM, Melnick JL, Monath TP, Roizman B, Straus SS. editors. Virology. Philadelphia, PA: Lippincott-Raven Publishers. Vol. 2 p 2397–2446.
  • Silins SL, Sherritt MA, Silleri JM, Cross SM, Elliott SL, Bharadwaj M, Le TT, Morrison LE, Khanna R, Moss DJ, Suhrbier A, Misko IS. Asymptomatic primary Epstein-Barr virus infection occurs in the absence of blood T-cell repertoire perturbations despite high levels of systemic viral load. Blood. 2001; 98 13: 3739–3744.
  • Morens DM. Antibody-dependent enhancement of infection and the pathogenesis of viral disease. Clin Infect Dis. 1994; 19 3: 500–512.
  • Halstead SB. Antibody, macrophages, dengue virus infection, shock and hemorrhage: A pathogenetic cascade. Rev Infect Dis. 1989; 11:S830–S839.
  • Matthew A, Kurane I, Green S, Stephens HAF, Vaughn DW, Kalayanarooj S, Suntayakorn S, Chandanayingyong D, Ennis FA, Rothman AL. Predominance of HLA-restricted cytotoxic T-lymphocyte responses to serotype-cross-reactive epitopes on nonstructural proteins following natural secondary dengue virus infection. J Virol. 1998; 72:3999–4004.
  • Suri-Payer E, Fritzsching B. Regulatory T cells in experimental autoimmune disease. Springer Semin Immunopathol. 2006; 28 1: 3–16.
  • Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, Shimizu J, Takahashi T, Nomura T. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev. 2006; 212:8–27.
  • Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008; 133 5: 775–787.
  • Izcue A, Coombes JL, Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol. 2009; 27:313–338.
  • Mottet C, Uhlig HH, Powrie F. Cutting edge: Cure of colitis by CD4+ CD25+ regulatory T cells. J Immunol. 2003; 170 8: 3939–3943.
  • Morgan ME, Sutmuller RP, Witteveen HJ, van Duivenvoorde LM, Zanelli E, Melief CJ, Snijders A, Offringa R, de Vries RR, Toes RE. CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum. 2003; 48 5: 1452–1460.
  • Lindley S, Dayan CM, Bishop A, Roep BO, Peakman M, Tree TI. Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes. Diabetes. 2005; 54 1: 92–99.
  • Mittrucker HW, Kaufmann SH. Mini-review. Regulatory T cells and infection: Suppression revisited. Eur J Immunol. 2004; 34 2: 306–312.
  • Rouse BT, Sarangi PP, Suvas S. Regulatory T cells in virus infections. Immunol Rev. 2006; 212:272–286.
  • Belkaid Y, Tarbell K. Regulatory T cells in the control of host-microorganism interactions (*). Annu Rev Immunol. 2009; 27:551–589.
  • Zelinskyy G, Dietze KK, Husecken YP, Schimmer S, Nair S, Werner T, Gibbert K, Kershaw O, Gruber AD, Sparwasser T, Dittmer U. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood. 2009; 114 15: 3199–3207.
  • Zelinskyy G, Kraft AR, Schimmer S, Arndt T, Dittmer U. Kinetics of CD8+ effector T cell responses and induced CD4+ regulatory T cell responses during Friend retrovirus infection. Eur J Immunol. 2006; 36 10: 2658–2670.
  • Suvas S, Kumaraguru U, Pack CD, Lee S, Rouse BT. CD4+ CD25+ T cells regulate virus-specific primary and memory CD8+ T cell responses. J Exp Med. 2003; 198 6: 889–901.
  • Suvas S, Azkur AK, Kim BS, Kumaraguru U, Rouse BT. CD4+ CD25+ regulatory T cells control the severity of viral immunoinflammatory lesions. J Immunol. 2004; 172 7: 4123–4132.
  • Zhao Z-S, Granucci F, Yeh L, Schaffer PA, Cantor H. Molecular mimicry by herpes simplex virus-type 1: Autoimmune disease after viral infection. Science. 1998; 279:1344–1347.
  • Hiemstra HS, Schloot NC, van Veelen PA, Willemen SJ, Franken KL, van Rood JJ, de Vries RR, Chaudhuri A, Behan PO, Drijfhout JW, Roep BO. Cytomegalovirus in autoimmunity: T cell crossreactivity to viral antigen and autoantigen glutamic acid decarboxylase. Proc Natl Acad Sci USA. 2001; 98 7: 3988–3991.
  • Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: Role of anti-self (virus) immune response. Cell. 1991; 65 2: 319–331.
  • Evans CF, Horwitz MS, Hobbs MV, Oldstone MBA. Viral infection of transgenic mice expressing a viral protein in oligodendrocytes leads to chronic central nervous system autoimmune disease. J Exp Med. 1996; 184:2371–2384.
  • Kagi D, Odermatt B, Ohashi PS, Zinkernagel RM, Hengartner H. Development of insulitis without diabetes in transgenic mice lacking perforin-dependent cytotoxicity. J Exp Med. 1996; 183 5: 2143–2152.
  • Christen U, Edelmann KH, McGavern DB, Wolfe T, Coon B, Teague MK, Miller SD, Oldstone MB, von Herrath MG. A viral epitope that mimics a self antigen can accelerate but not initiate autoimmune diabetes. J Clin Invest. 2004; 114:1290–1298.
  • McCoy L, Tsunoda I, Fujinami RS. Multiple sclerosis and virus induced immune responses: Autoimmunity can be primed by molecular mimicry and augmented by bystander activation. Autoimmunity. 2006; 39 1: 9–19.
  • Theil DJ, Tsunoda I, Rodriguez F, Whitton JL, Fujinami RS. Viruses can silently prime for and trigger central nervous system autoimmune disease. J Neurovirol. 2001; 7 3: 220–227.
  • Sospedra M, Zhao Y, zur HH, Muraro PA, Hamashin C, de Villiers EM, Pinilla C, Martin R. Recognition of conserved amino acid motifs of common viruses and its role in autoimmunity. PLoS Pathog. 2005; 1 4: e41.
  • Welsh RM, Rothman AL. Dengue immune response: Low affinity, high febrility. Nature Med. 2003; 9:820–822.
  • Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M, Diamond MS, Miller VL, Virgin HW. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature. 2007; 447 7142: 326–329.
  • Di Giusto CA, Bernhard JD. Erythema nodosum provoked by hepatitis B vaccine. Lancet. 1986; 2 8514: 1042.
  • Cheng C, Gall JG, Nason M, King CR, Koup RA, Roederer M, McElrath MJ, Morgan CA, Churchyard G, Baden LR, Duerr AC, Keefer MC, Graham BS, Nabel GJ. Differential specificity and immunogenicity of adenovirus type 5 neutralizing antibodies elicited by natural infection or immunization. J Virol. 2010; 84 1: 630–638.
  • DiMario FJJr, Hajjar M, Ciesielski T. A 16-year-old girl with bilateral visual loss and left hemiparesis following an immunization against human papilloma virus. J Child Neurol. 2010; 25 3: 321–327.
  • Williams OM, Hart KW, Wang EC, Gelder CM. Analysis of CD4(+) T-cell responses to human papillomavirus (HPV) type 11 L1 in healthy adults reveals a high degree of responsiveness and cross-reactivity with other HPV types. J Virol. 2002; 76 15: 7418–7429.
  • Ahmed R, Gray D. Immunological memory and protective immunity: Understanding their relation. Science. 1996; 272:54–60.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.