Advertisement

The Privacy of T Cell Memory to Viruses

  • R. M. Welsh
  • S. K. Kim
  • M. Cornberg
  • S. C. Clute
  • L. K. Selin
  • Y. N. Naumov
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 311)

Abstract

T cell responses to viral infections can mediate either protective immunity or damaging immunopathology. Viral infections induce the proliferation of T cells spe cific for viral antigens and cause a loss in the number of T cells with other specificities. In immunologically naïve hosts, viruses will induce T cell responses that, dependent on the MHC, recognize a distinct hierarchy of virus-encoded T cell epitopes. This hierarchy can change if the host has previously encountered another pathogen that elicited amemory pool of T cells specific to a cross-reactive epitope. This heterologous immunity can deviate the normal immune response and result in either beneficial or harmful effects on the host. Each host has a unique T cell repertoire caused by the random DNA rearrangement that created it, so the specific T cells that create the epitope hierarchy differ between individuals. This “private specificity” seems of little signifi-cance in the T cell responseof a naïvehost toinfection, but it is of profoundimportance under conditions of heterologous immunity, where a small subset of a cross-reactive memory pool may expand and dominate a response. Examples are given of how the private specificities of immune responses under conditions of heterologous immunity influence the pathogenesis of murine and human viral infections.

Keywords

Dengue Hemorrhagic Fever Cell Repertoire Memory Pool Heterologous Virus Heterologous Immunity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acierno PM, Newton DA, Brown EA, Maes LA, Baatz JE, Gattoni-Celli S (2003) Crossreactivity between HLA-A2-restricted FLU-M1:58–66 and HIV p17 GAG:77–85 epitopes in HIV-infected and uninfected individuals. J Transl Med 1:3PubMedGoogle Scholar
  2. Annels NE, Callan MF, Tan L, Rickinson AB (2000) Changing patterns of dominant TCR usage with maturation of an EBV-specific cytotoxic T cell response. J Immunol 165:4831–4841PubMedGoogle Scholar
  3. Arstila TP, Casrouge A, Baron V, Even J, Kanellopoulos J, Kourilsky P (1999) A direct estimate of the human alphabeta T cell receptor diversity. Science 286:958–961PubMedGoogle Scholar
  4. Bahl K, Kim S-K, Calcagno C, Ghersi D, Puzone R, Celada F, Selin LK, Welsh RM (2006) Interferon-induced attrition of T cells in the presence or absence of cognate antigen during the early stages of viral infection. J Immunol 176:4248–4295Google Scholar
  5. Battaglia M, Gorski J (2002) Evidence for preferred MHC class II-TCR recognition independent of the source of bound peptide. Eur J Immunol 32:2179–2187PubMedGoogle Scholar
  6. Becker TC, Wherry EJ, Boone D, Murali-Krishna K, Antia R, Ma A, Ahmed R (2002) Interleukin 15 is required for proliferative renewal of virus-specificmemory CD8 T cells. J Exp Med 195:1541–1548PubMedGoogle Scholar
  7. Becker TC, Coley SM, Wherry EJ, Ahmed R (2005) Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J Immunol 174:1269–1273PubMedGoogle Scholar
  8. Biron CA (1995) Cytokines in the generation of immune responses to, and resolution of virus infection. Curr Opin Immunol 6:530–538Google Scholar
  9. Biron CA, Sen GC (2001) Interferons and other cytokines. In: Knipe DM, Howley PM (eds) Fundamental virology. Lippincott, Williams and Wilkins, Philadelphia, pp 321–351Google Scholar
  10. Blattman JN, Sourdive DJ, Murali-Krishna K, Ahmed R, Altman JD (2000) Evolution of the T cell repertoire during primary, memory, and recall responses to viral infection. J Immunol 165:6081–6090PubMedGoogle Scholar
  11. Blattman JN, Antia R, Sourdive DJ, Wang X, Kaech SM, Murali-Krishna K, Altman JD, Ahmed R (2002) Estimating the precursor frequency of naive antigen-specific CD8 T cells. J Exp Med 195:657–664PubMedGoogle Scholar
  12. Bolognia J, Braverman IM (1992) Skin manifestations of internal disease. In: Isselbacher KJ, Braunwald E, Wilson J, Martin JB, Fauci AS, Kasper DL (eds) Harrison’s principles of internal medicine. McGraw-Hill, New York, pp 290–307Google Scholar
  13. Boniface JJ, Reich Z, Lyons DS, Davis MM (1999) Thermodynamics of T cell receptor binding to peptide-MHC: evidence for a general mechanism of molecular scanning. Proc Natl Acad Sci U S A 96:11446–11451PubMedGoogle Scholar
  14. Boon AC, de Mutsert G, van Baarle D, Smith DJ, Lapedes AS, Fouchier RA, Sintnicolaas K, Osterhaus AD, Rimmelzwaan GF (2004) Recognition of homo-and heterosubtypic variants of influenza A viruses by human CD8+ T lymphocytes. J Immunol 172:2453–2460PubMedGoogle Scholar
  15. Borg NA, Ely LK, Beddoe T, Macdonald WA, Reid HH, Clements CS, Purcell AW, Kjer-Nielsen L, Miles JJ, Burrows SR, McCluskey J, Rossjohn J (2005) The CDR3 regions of an immunodominant T cell receptor dictate the ‘energetic landscape’ of peptide-MHC recognition. Nat Immunol 6:171–180PubMedGoogle Scholar
  16. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, Meyers H, Nelson JA, Gairin JE, Hahn BH, Oldstone MB, Shaw GM (1997) Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 3:205–211PubMedGoogle Scholar
  17. Bradley LM, Haynes L, Swain SL (2005) IL-7: maintaining T-cellmemory and achieving homeostasis. Trends Immunol 26:172–176PubMedGoogle Scholar
  18. Brehm MA, Pinto AK, Daniels KA, Schneck JP, Welsh RM, Selin LK (2002) T cell immunodominance and maintenance of memory regulated by unexpectedly crossreactive pathogens. Nat Immunol 3:627–634PubMedGoogle Scholar
  19. Burgos JD (1996) Fractal representation of the immune B cell repertoire. Biosystems 39:19–24PubMedGoogle Scholar
  20. Butz EA, Bevan MJ (1998) Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 8:167–175PubMedGoogle Scholar
  21. Casrouge A, Beaudoing E, Dalle S, Pannetier C, Kanellopoulos J, Kourilsky P (2000) Size estimate of the alpha beta TCR repertoire of naive mouse splenocytes. J Immunol 164:5782–5787PubMedGoogle Scholar
  22. Chen HD, Fraire AE, Joris I, Brehm MA, Welsh RM, Selin LK (2001) Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat Immunol 2:1067–1076PubMedGoogle Scholar
  23. Chen HD, Fraire AE, Joris I, Welsh RM, Selin LK (2003) Specific history of heterologous virus infections determines antiviral immunity and immunopathology in the lung. Am J Pathol 163:1341–1355PubMedGoogle Scholar
  24. Cibotti R, Cabaniols JP, Pannetier C, Delarbre C, Vergnon I, Kanellopoulos JM, Kourilsky P (1994) Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice. J Exp Med 180:861–872PubMedGoogle Scholar
  25. Clarke SH, Staudt LM, Kavaler J, Schwartz D, Gerhard WU, Weigert MG (1990) Vregion gene usage and somatic mutation in the primary and secondary responses to influenza virus hemagglutinin. J Immunol 144:2795–2801PubMedGoogle Scholar
  26. Clute SC, Watkin LB, Cornberg M, Naumov YN, Sullivan JL, Luzuriaga K, Welsh RM, Selin LK (2005) Cross-reactive influenza virus-specific CD8+ T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis. J Clin Invest 115:3602–3612PubMedGoogle Scholar
  27. Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, Golenbock DT, Finberg RW (2003) Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 77:4588–4596PubMedGoogle Scholar
  28. Cornberg M, Chen AT, Wilkinson LA, Brehm MA, Kim S-K, Calcagno C, Ghersi D, Puzone R, Celada F, Welsh RM, Selin LK (2006) Narrowed T cell receptor repertoire and viral escape as a consequence of heterologous immunity. J Clin Invest 116:1143–1456Google Scholar
  29. Correia-Neves M, Waltzinger C, Mathis D, Benoist C (2001) The shaping of the T cell repertoire. Immunity 14:21–32PubMedGoogle Scholar
  30. Di Giusto CA, Bernhard JD (1986) Erythema nodosum provoked by hepatitis B vaccine. Lancet 2:1042PubMedGoogle Scholar
  31. Ding YH, Baker BM, Garboczi DN, Biddison WE, Wiley DC (1999) Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 11:45–56PubMedGoogle Scholar
  32. Dong T, Stewart-Jones G, Chen N, Easterbrook P, Xu X, Papagno L, Appay V, Weekes M, Conlon C, Spina C, Little S, Screaton G, van der MA, Richman DD, McMichael AJ, Jones EY, Rowland-Jones SL (2004) HIV-specific cytotoxic T cells fromlong-term survivors select a unique T cell receptor. J Exp Med 200:1547–1557PubMedGoogle Scholar
  33. Effros RB, Doherty PC, Gerhard W, Bennink J (1977) Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses. J Exp Med 145:557–568PubMedGoogle Scholar
  34. Farci P, Alter HJ, Shimoda A, Govindarajan S, Cheung LC, Melpolder JC, Sacher RA, Shih JW, Purcell RH (1996) Hepatitis C virus-associated fulminant hepatic failure. N Engl J Med 335:631–634PubMedGoogle Scholar
  35. Fazekas de St Groth S, Webster RG (1966) Disquisitions on original antigenic sin. II. Proof in lower creatures. J Exp Med 124:347–361PubMedGoogle Scholar
  36. Fuller MJ, Khanolkar A, Tebo AE, Zajac AJ (2004) Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J Immunol 172:4204–4214PubMedGoogle Scholar
  37. Gorski J, Yassai M, Zhu X, Kissela B, Kissella B, Keever C, Flomenberg N (1994) Circulating T cell repertoire complexity in normal individuals and bone marrow recipients analyzed by CDR3 size spectratyping. Correlation with immune status. J Immunol 152:5109–5119PubMedGoogle Scholar
  38. Grayson JM, Zajac AJ, Altman JD, Ahmed R (2000) Cutting edge: increased expression of Bcl-2 in antigen-specific memory CD8+ T cells. J Immunol 164:3950–3954PubMedGoogle Scholar
  39. Grayson JM, Harrington LE, Lanier JG, Wherry EJ, Ahmed R (2002) Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo. J Immunol 169:3760–3770PubMedGoogle Scholar
  40. Grayson JM, Laniewski NG, Lanier JG, Ahmed R (2003) Mitochondrial potential and reactive oxygen intermediates in antigen-specific CD8+ T cells during viral infection. J Immunol 170:4745–4751PubMedGoogle Scholar
  41. Gulwani-Akolkar B, Posnett DN, Janson CH, Grunewald J, Wigzell H, Akolkar P, Gregersen PK, Silver J (1991) T cell receptor V-segment frequencies in peripheral blood T cells correlate with human leukocyte antigen type. J Exp Med 174:1139–1146PubMedGoogle Scholar
  42. Haanan JB, Wolkers MC, Kruisbeek AM, Schumacher TN (1999) Selective expansion of cross-reactive CD8(+) memory T cells by viral variants. J Exp Med 190:1319–1328Google Scholar
  43. Hahm B, Trifilo MJ, Zuniga EI, Oldstone MB (2005) Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 22:247–257PubMedGoogle Scholar
  44. Han S, Zheng B, Takahashi Y, Kelsoe G (1997) Distinctive characteristics of germinal center B cells. Semin Immunol 9:255–260PubMedGoogle Scholar
  45. Harris NL, Ronchese F (1999) The role of B7 costimulation in T-cell immunity. Immunol Cell Biol 77:304–311PubMedGoogle Scholar
  46. Haynes LM, Moore DD, Kurt-Jones EA, Finberg RW, Anderson LJ, Tripp RA (2001) Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J Virol 75:10730–10737PubMedGoogle Scholar
  47. Huang AY, Qi H, Germain RN (2004) Illuminating the landscape of in vivo immunity: insights from dynamic in situ imaging of secondary lymphoid tissues. Immunity 21:331–339PubMedGoogle Scholar
  48. Jiang J, Anaraki F, Blank KJ, Murasko DM (2003a) Cutting edge: T cells fromagedmice are resistant to depletion early during virus infection. J Immunol 171:3353–3357PubMedGoogle Scholar
  49. Jiang J, Lau LL, Shen H (2003b) Selective depletion of nonspecific T cells during the early stage of immune responses to infection. J Immunol 171:4352–4358PubMedGoogle Scholar
  50. Jiang Z, Mak TW, Sen G, Li X (2004) Toll-like receptor 3-mediated activation of NFkappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc Natl Acad Sci U S A 101:3533–3538PubMedGoogle Scholar
  51. Kaech SM, Ahmed R (2001) Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2:415–422PubMedGoogle Scholar
  52. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4:1191–1198PubMedGoogle Scholar
  53. Kapasi ZF, Murali-Krishna K, McRae ML, Ahmed R (2002) Defective generation but normal maintenance of memory T cells in old mice. Eur J Immunol 32:1567–1573PubMedGoogle Scholar
  54. Kapikian AZ, Mitchell RH, Chanock RM, Shvedoff RA, Stewart CE (1969) An epidemiological study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine. Am J Epidemiol 89:405–421PubMedGoogle Scholar
  55. Khan N, Shariff N, Cobbold M, Bruton R, Ainsworth JA, Sinclair AJ, Nayak L, Moss PA (2002) Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J Immunol 169:1984–1992PubMedGoogle Scholar
  56. Kieper WC, Jameson SC (1999) Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc Natl Acad Sci U S A 96:13306–13311PubMedGoogle Scholar
  57. Kieper WC, Tan JT, Bondi-Boyd B, Gapin L, Sprent J, Ceredig R, Surh CD (2002) Overexpression of interleukin (IL)-7 leads to IL-15-independent generation of memory phenotype CD8+ T cells. J Exp Med 195:1533–1539PubMedGoogle Scholar
  58. Kim SK, Welsh RM (2004) Comprehensive early and lasting loss of memory CD8 T cells and functional memory during acute and persistent viral infections. J Immunol 172:3139–3150PubMedGoogle Scholar
  59. Kim SK, Brehm MA, Welsh RM, Selin LK (2002) Dynamics of memory T cell proliferation under conditions of heterologous immunity and bystander stimulation. J Immunol 169:90–98PubMedGoogle Scholar
  60. Kim SK, Cornberg M, Wang XZ, Chen HD, Selin LK, Welsh RM (2005) Private speci-ficities of CD8 T cell responses control patterns of heterologous immunity. J Exp Med 201:523–533PubMedGoogle Scholar
  61. Kjer-Nielsen L, Clements CS, Purcell AW, Brooks AG, Whisstock JC, Burrows SR, McCluskey J, Rossjohn J (2003) A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 18:53–64PubMedGoogle Scholar
  62. Klenerman P, Zinkernagel RM (1998) Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature 394:421–422Google Scholar
  63. Lawson TM, Man S, Wang EC, Williams S, Amos N, Gillespie GM, Moss PA, Borysiewicz LK (2001a) Functional differences between influenza A-specific cytotoxic T lymphocyte clones expressing dominant and subdominant TCR. Int Immunol 13:1383–1390PubMedGoogle Scholar
  64. Lawson TM, Man S, Williams S, Boon AC, Zambon M, Borysiewicz LK (2001b) In-fluenza A antigen exposure selects dominant Vbeta17+ TCR in human CD8+ cytotoxic T cell responses. Int Immunol 13:1373–1381PubMedGoogle Scholar
  65. Lehner PJ, Wang ECY, Moss PAH, Williams S, Platt K, Friedman SM, Bell JI, Borysiewicz LK (1995) Human HLA-A0201-restricted cytotoxic T lymphocyte recognition of influenza A is dominated by T cells bearing the Vb17 gene segment. J Exp Med 181:79–91PubMedGoogle Scholar
  66. Lim A, Trautmann L, Peyrat MA, Couedel C, Davodeau F, Romagne F, Kourilsky P, Bonneville M (2000a) Frequent contribution of T cell clonotypes with public TCR features to the chronic response against a dominant EBV-derived epitope: application to direct detection of theirmolecular imprint on the humanperipheral T cell repertoire. J Immunol 165:2001–2011PubMedGoogle Scholar
  67. Lim DG, Bieganowska BK, Freeman GJ, Hafler DA (2000b) Examination of CD8+ T cell function in humans using MHC class I tetramers: similar cytotoxicity but variable proliferation and cytokine production among different clonal CD8+ T cells specific to a single viral epitope. J Immunol 165:6214–6220PubMedGoogle Scholar
  68. Lin KI, Tunyaplin C, Calame K (2003) Transcriptional regulatory cascades controlling plasma cell differentiation. Immunol Rev 194:19–28PubMedGoogle Scholar
  69. Lin MY, Welsh RM (1998) Stability and diversity of T cell receptor (TCR) repertoire usage during lymphocytic choriomeningitis virus infection of mice. J Exp Med 188:1993–2005PubMedGoogle Scholar
  70. Liu Y, deBoutellier O, Fujii H (1997) Mechanisms of selection and differentiation in germinal centers. Curr Opin Immunol 9:256–262PubMedGoogle Scholar
  71. Maeda K, West K, Toyosaki-Maeda T, Rothman AL, Ennis FA, Terajima M (2004) Identification and analysis for cross-reactivity among hantaviruses of H-2b-restricted cytotoxic T-lymphocyte epitopes in Sin Nombre virus nucleocapsid protein. JGen Virol 85:1909–1919Google Scholar
  72. Manfras BJ, Weidenbach H, Beckh KH, Kern P, Moller P, Adler G, Mertens T, Boehm BO (2004) Oligoclonal CD8+ T-cell expansion in patients with chronic hepatitis C is associated with liver pathology and poor response to interferon-alpha therapy. J Clin Immunol 24:258–271PubMedGoogle Scholar
  73. Marshall DR, Turner SJ, Belz GT, Wingo S, Andreansky S, Sangster MY, Riberdy JM, Liu T, Tan M, Doherty PC (2001) Measuring the diaspora for virus-specific CD8+ T cells. Proc Natl Acad Sci USA 98:6313–6318PubMedGoogle Scholar
  74. Marshall DR, Olivas E, Andreansky S, LaGruta NL, Neale GA, Gutierrez A, Wichlan DG, Wingo S, Cheng C, Doherty PC, Turner SJ (2005) Effector CD8+ T cells recovered from an influenza pneumonia differentiate to a state of focused gene expression. Proc Natl Acad Sci U S A 102:6074–6079PubMedGoogle Scholar
  75. Maryanski JL, Attuil V, Hamrouni A, Mutin M, Rossi M, Aublin A, Bucher P (2001) Individuality of Ag-selected and preimmune TCR repertoires. Immunol Res 23:75–84PubMedGoogle Scholar
  76. Masopust D, Vezys V, Marzo AL, Lefrancois L (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291:2413–2417PubMedGoogle Scholar
  77. McNally JM, Zarozinski CC, Lin MY, Brehm MA, Chen HD, Welsh RM (2001) Attrition of bystander CD8 T cells during virus-induced T cell and interferon responses. J Virol 75:5965–5976PubMedGoogle Scholar
  78. Mercado R, Vijh S, Allen SE, Kerksiek K, Pilip IM, Pamer EG (2000) Early programming of T cell populations responding to bacterial infection. J Immunol 165:6833–6839PubMedGoogle Scholar
  79. Meyer-Olson D, Shoukry NH, Brady KW, Kim H, Olson DP, Hartman K, Shintani AK, Walker CM, Kalams SA (2004) Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J Exp Med 200:307–319PubMedGoogle Scholar
  80. 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 (2003) Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9:921–927PubMedGoogle Scholar
  81. Morens DM (1994) Antibody-dependent enhancement of infection and the pathogenesis of viral disease. Clin Infect Dis 19:500–512PubMedGoogle Scholar
  82. Moss PAH, Moots RJ, Rosenberg WMC, Rowland-Jones SJ, Bodmer HC, McMichael AJ, Bell JI (1991) Extensive conservation of a and b chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza Amatrix peptide. Proc Natl Acad Sci U S A 88:8987–8990PubMedGoogle Scholar
  83. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–563PubMedGoogle Scholar
  84. Naumov YN, Hogan KT, Naumova EN, Pagel JT, Gorski J (1998) A class I MHC-restricted recall response to a viral peptide is highly polyclonal despite stringent CDR3 selection: implications for establishing memory T cell repertoires in “realworld” conditions. J Immunol 160:2842–2852PubMedGoogle Scholar
  85. Naumov YN, Naumova EN, Clute SC, Watkin LB, Kota K, Gorski J, Selin LK (2006) Complex T cell memory repertoires participate in recall responses at extremes of antigen load. J Immunol 177 (in press)Google Scholar
  86. Naumov YN, Naumova EN, Hogan KT, Selin LK, Gorski J (2003) A fractal clonotype distribution in the CD8+ memory T cell repertoire could optimize potential for immune responses. J Immunol 170:3994-4001Google Scholar
  87. Nikolich-Zugich J, Slifka MK, Messaoudi I (2004) The many important facets of T-cell repertoire diversity. Nat Rev Immunol 4:123–132PubMedGoogle Scholar
  88. Nilges K, Hohn H, Pilch H, Neukirch C, Freitag K, Talbot PJ, Maeurer MJ (2003) 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 77:5464–5474PubMedGoogle Scholar
  89. Norbury CC, Malide D, Gibbs JS, Bennink JR, Yewdell JW (2002) Visualizing priming of virus-specific CD8+ T cells by infected dendritic cells in vivo. Nat Immunol 3:265–271PubMedGoogle Scholar
  90. Oehen S, Brduscha-Riem K (1999) Naive cytotoxic T lymphocytes spontaneously acquire effector function in lymphocytopenic recipients: a pitfall for T cell memory studies? Eur J Immunol 29:608–614PubMedGoogle Scholar
  91. Oldstone MBA (1991) Molecular anatomy of viral persistence. J Virol 65:6381–6386PubMedGoogle Scholar
  92. Ostler T, Pircher H, Ehl S (2003) “Bystander” recruitment of systemic memory T cells delays the immune response to respiratory virus infection. Eur J Immunol 33:1839–1848PubMedGoogle Scholar
  93. Pannetier C, Cochet M, Darche S, Casrouge A, Zoller M, Kourilisky P (1993) The sizes of the CDR3 hypervariable regions of the murine T-cell receptor b chains vary as a function of the recombined germ-line segments. Proc Natl Acad Sci USA 90:4319–4323PubMedGoogle Scholar
  94. Pantaleo G, Demarest JF, Soudeyns H, Graziosi C, Denis F, Adelsberger JW, Borrow P, Saag MS, Shaw GM, Sekaly RP (1994) Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV. Nature 370:463–467PubMedGoogle Scholar
  95. Park KY, Lee MG, Ryu JC, Park YK (1997) Evolutionary stasis of M1 gene of human influenza A viruses and the possibility of their subtyping by restriction analysis of M1 gene polymerase chain reaction product. Acta Virol 41:231–239PubMedGoogle Scholar
  96. Peacock CD, Kim S-K, Welsh RM (2003) Attrition of virus-specific memory CD8(+) T cells during reconstitution of lymphopenic environments. J Immunol 171:655–663PubMedGoogle Scholar
  97. Pewe LL, Netland JM, Heard SB, Perlman S (2004) Very diverse CD8 T cell clonotypic responses after virus infections. J Immunol 172:3151–3156PubMedGoogle Scholar
  98. Pfizenmaier K, Jung H, Starzinski-Powitz A, Rollinghoff M, Wagner H (1977) The role of T cells in anti-herpes simplex virus immunity. I. Induction of antigen-specific cytotoxic T lymphocytes. J Immunol 119:939–944PubMedGoogle Scholar
  99. Ploegh HL (1998) Viral strategies of immune evasion. Science 280:248–253PubMedGoogle Scholar
  100. Po JL, Gardner EM, Anaraki F, Katsikis PD, Murasko DM (2002) Age-associated decrease in virus-specific CD8+ T lymphocytes during primary influenza infection. Mech Ageing Dev 123:1167–1181PubMedGoogle Scholar
  101. Prlic M, Lefrancois L, Jameson SC (2002) Multiple choices: regulation of memory CD8 T cell generation and homeostasis by interleukin (IL)-7 and IL-15. J Exp Med 195:F49–F52PubMedGoogle Scholar
  102. Ray SJ, Franki SN, Pierce RH, Dimitrova S, Koteliansky V, Sprague AG, Doherty PC, de Fougerolles AR, Topham DJ (2004) The collagen binding alpha1 beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity 20:167–179PubMedGoogle Scholar
  103. Razvi ES, Jiang Z, Woda BA, Welsh RM (1995a) Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr and Bcl-2-transgenic mice. Am J Pathol 147:79–91PubMedGoogle Scholar
  104. Razvi ES, Welsh RM, McFarland HI (1995b) In vivo state of antiviral CTL precursors: characterization of a cycling population containing CTL precursors in immune mice. J Immunol 154:620–632PubMedGoogle Scholar
  105. Rehermann B, Shin EC (2005) Private aspects of heterologous immunity. J Exp Med 201:667–670PubMedGoogle Scholar
  106. Reinhardt RL, Khoruts A, Merica R, Zell T, Jenkins MK (2001) Visualizing the generation of memory CD4 T cells in the whole body. Nature 410:101–105PubMedGoogle Scholar
  107. Reiser JB, Gregoire C, Darnault C, Mosser T, Guimezanes A, Schmitt-Verhulst AM, Fontecilla-Camps JC, Mazza G, Malissen B, Housset D (2002) A T cell receptor CDR3beta loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. Immunity 16:345–354PubMedGoogle Scholar
  108. Reiser JB, Darnault C, Gregoire C, Mosser T, Mazza G, Kearney A, van der Merwe PA, Fontecilla-Camps JC, Housset D, Malissen B (2003) CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat Immunol 4:241–247PubMedGoogle Scholar
  109. Roost H-P, Bachmann MF, Haag A, Kalinke U, Pliska V, Hengartner H, Zinkernagel RM (1995) Early high-affinity neutralizing anti-viral lgG responses without further improvements of affinity. Proc Natl Acad Sci U S A 92:1257–1261PubMedGoogle Scholar
  110. Rudolph MG, Wilson IA (2002) The specificity of TCR/pMHC interaction. Curr Opin Immunol 14:52–65PubMedGoogle Scholar
  111. Sallusto F, Mackay CR, Lanzavecchia A (2000) The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 18:593–620PubMedGoogle Scholar
  112. Schlesinger C, Meyer CA, Veeraraghavan S, Koss MN (1998) Constrictive (obliterative) bronchiolitis: diagnosis, etiology, and a critical review of the literature. Ann Diagn Pathol 2:321–334PubMedGoogle Scholar
  113. Selin LK, Welsh RM (1997) Cytolytically active memory CTL present in lymphocytic choriomeningitis virus (LCMV)-immune mice after clearance of virus infection. J Immunol 158:5366–5373PubMedGoogle Scholar
  114. Selin LK, Welsh RM (2004) Plasticity of T cell memory responses to viruses. Immunity 20:5–16PubMedGoogle Scholar
  115. Selin LK, Nahill SR, Welsh RM (1994) Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J Exp Med 179:1933–1943PubMedGoogle Scholar
  116. Selin LK, Vergilis K, Welsh RM, Nahill SR (1996) Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J Exp Med 183:2489–2499PubMedGoogle Scholar
  117. Selin LK, Varga SM, Wong IC, Welsh RM (1998) Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations. J Exp Med 188:1705–1715PubMedGoogle Scholar
  118. Selin LK, Lin MY, Kraemer KA, Schneck JP, Pardoll D, Varga SM, Santolucito PA, Pinto AK, Welsh RM (1999) Attrition of T cell memory: selective loss of lymphocytic choriomeningitis virus (LCMV) epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity 11:733–742PubMedGoogle Scholar
  119. Sigal LJ, Crotty S, Andino R, Rock KL (1999) Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398:77–80PubMedGoogle Scholar
  120. Silins SL, Sherritt MA, Silleri JM, Cross SM, Elliott SL, Bharadwaj M, Le TT, Morrison LE, Khanna R, Moss DJ, Suhrbier A, Misko IS (2001) Asymptomatic primary Epstein-Barr virus infection occurs in the absence of blood T-cell repertoire perturbations despite high levels of systemic viral load. Blood 98:3739–3744PubMedGoogle Scholar
  121. Spaulding AC, Kurane I, Ennis FA, Rothman AL (1999) Analysis of murine CD8(+) T-cell clones specific for the Dengue virus NS3 protein: flavivirus cross-reactivity and influence of infecting serotype. J Virol 73:398–403PubMedGoogle Scholar
  122. Tan JT, Ernst B, Kieper WC, LeRoy E, Sprent J, Surh CD (2002) Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells. J Exp Med 195:1523–1532PubMedGoogle Scholar
  123. Tough DF, Sprent J (1994) Turnover of naive-and memory-phenotype T cells. J Exp Med 179:1127–1135PubMedGoogle Scholar
  124. Townsend ARM, Rothband J, Gotch F, Bahadur G, Wraith DC, McMichael AJ (1986) The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44:959–968PubMedGoogle Scholar
  125. Turner SJ, Diaz G, Cross R, Doherty PC (2003) Analysis of clonotype distribution and persistence for an influenza virus-specific CD8+ T cell response. Immunity 18:549–559PubMedGoogle Scholar
  126. 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 (2005) Lack of prominent peptide-major histocompatibility complex features limits repertoire diversity in virus-specific CD8+T cell populations. Nat Immunol 6:382–389PubMedGoogle Scholar
  127. Urbani S, Amadei B, Fisicaro P, Pilli M, Missale G, Bertoletti A, Ferrari C (2005) Heterologous T cell immunity in severe hepatitis C virus infection. J Exp Med 201:675–680PubMedGoogle Scholar
  128. van Stipdonk MJ, Lemmens EE, Schoenberger SP (2001) Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2:423–429PubMedGoogle Scholar
  129. Varga SM, Wang X, Welsh RM, Braciale TJ (2001) Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4+ T cells. Immunity 15:637–646PubMedGoogle Scholar
  130. von Herrath MG, Dockter J, Oldstone MB (1994) How virus induces a rapid or slow onset insulin-dependent diabetes mellitus in a transgenic model. Immunity 1:231–242Google Scholar
  131. Walzl G, Tafuro S, Moss P, Openshaw PJ, Hussell T (2000) Influenza virus lung infection protects from respiratory syncytial virus-induced immunopathology. J Exp Med 192:1317–1326PubMedGoogle Scholar
  132. Wang XZ, Stepp SE, Brehm MA, Chen HD, Selin LK, Welsh RM (2003) Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity 18:631–642PubMedGoogle Scholar
  133. Wang XZ, Brehm MA, Welsh RM (2004) Preapoptotic phenotype of viral epitopespecific CD8 T cells precludes memory development and is an intrinsic property of the epitope. J Immunol 173:5138–5147PubMedGoogle Scholar
  134. Wang Y, Smith JA, Gefter ML, Perkins DL (1992) Immunodominance: intermolecular competition between MHC class II molecules by covalently linked T cell epitopes. J Immunol 148:3034–3041PubMedGoogle Scholar
  135. Wedemeyer H, Mizukoshi E, Davis AR, Bennink JR, Rehermann B (2001) Cross-reactivity between hepatitis C virus and influenza A virus determinant-specific cytotoxic T cells. J Virol 75:11392–11400PubMedGoogle Scholar
  136. Welsh RM (1978) Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice. I. Characterization of natural killer cell induction. J Exp Med 148:163–181PubMedGoogle Scholar
  137. Welsh RM (1984) Natural killer cells and interferon. Crit Rev Immunol 5:55–93PubMedGoogle Scholar
  138. Welsh RM, Selin LK (2002) No one is naive: the significance of heterologous T-cell immunity. Nat Rev Immunol 2:417–426PubMedGoogle Scholar
  139. Welsh RM, Selin LK, Szomolanyi-Tsuda E (2004) Immunological memory to viral infections. Annu Rev Immunol 22:711–743PubMedGoogle Scholar
  140. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, Von Andrian UH, Ahmed R (2003) Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 4:225–234PubMedGoogle Scholar
  141. Wiley JA, Hogan RJ, Woodland DL, Harmsen AG (2001) Antigen-specific CD8(+) T cells persist in the upper respiratory tract following influenza virus infection. J Immunol 167:3293–3299PubMedGoogle Scholar
  142. Willcox BE, Gao GF, Wyer JR, Ladbury JE, Bell JI, Jakobsen BK, van der Merwe PA (1999) TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 10:357–365PubMedGoogle Scholar
  143. Wilson JDK, Ogg GS, Allen RL, Goulder PJR, Kelleher A, Sewell AK, O’Callaghan CA, Rowland-Jones SL, Callan MFC, McMichael AJ (1998) Oligoclonal expansions of CD8+ T cells in chronic HIV infection are antigen specific. J Exp Med 188:785–790PubMedGoogle Scholar
  144. Wu LC, Tuot DS, Lyons DS, Garcia KC, Davis MM (2002) Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 418:552–556PubMedGoogle Scholar
  145. Xiong Y, Luscher MA, Altman JD, Hulsey M, Robinson HL, Ostrowski M, Barber BH, MacDonald KS (2001) Simian immunodeficiency virus (SIV) infection of rhesus macaque induces SIV-specific CD8+ T cells with a defect in effector function that is reversible on extended IL-2 incubation. J Virol 75:3028–3033PubMedGoogle Scholar
  146. Yang H, Joris I, Majno G, Welsh RM (1985) Necrosis of adipose tissue induced by sequential infections with unrelated viruses. Am J Pathol 120:173–177PubMedGoogle Scholar
  147. Yewdell JW, Bennink JR (1999) Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17:51–88PubMedGoogle Scholar
  148. Zhou S, Ou R, Huang L, Moskophidis D (2002) Critical role for perforin-, Fas/FasL-, and TNFR1-mediated cytotoxic pathways in down-regulation of antigen-specific T cells during persistent viral infection. J Virol 76:829–840PubMedGoogle Scholar
  149. Zimmermann C, Brduscha-Riem K, Blaser C, Zinkernagel RM, Pircher H (1996) Visualization, characterization, and turnover of CD8+ memory T cells in virus-infected hosts. J Exp Med 183:1367–1375Google Scholar
  150. Zivny J, DeFronzo M, Jarry W, Jameson J, Cruz J, Ennis FA, Rothman AL (1999) Partial agonist effect influences the CTL response to a heterologous dengue virus serotype. J Immunol 163:2754–2760PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  • R. M. Welsh
    • 1
  • S. K. Kim
    • 1
  • M. Cornberg
    • 1
  • S. C. Clute
    • 1
  • L. K. Selin
    • 1
  • Y. N. Naumov
    • 1
  1. 1.Department of PathologyUniversity of Massachusetts Medical SchoolWorcesterUSA

Personalised recommendations