Home LiteratureArticle Details
PMID: 20536568 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Heterologous immunity between viruses.

Immunological reviews ·Vol. 235 ·No. 1 ·2010-05-00 ·Pages 244-66

Welsh RM, Che JW, Brehm MA, Selin LK

Abstract

Immune memory responses to previously encountered pathogens can sometimes alter the immune response to and the course of infection of an unrelated pathogen by a process known as heterologous immunity. This response can lead to enhanced or diminished protective immunity and altered immunopathology. Here, we discuss the nature of T-cell cross-reactivity and describe matrices of epitopes from different viruses eliciting cross-reactive CD8(+) T-cell responses. We examine the parameters of heterologous immunity mediated by these cross-reactive T cells during viral infections in mice and humans. We show that heterologous immunity can disrupt T-cell memory pools, alter the complexity of the T-cell repertoire, change patterns of T-cell immunodominance, lead to the selection of viral epitope-escape variants, alter the pathogenesis of viral infections, and, by virtue of the private specificity of T-cell repertoires within individuals, contribute to dramatic variations in viral disease. We propose that heterologous immunity is an important factor in resistance to and variations of human viral infections and that issues of heterologous immunity should be considered in the design of vaccines.

MeSH Terms
Animals Antigens, Viral/immunology Autoimmunity CD8-Positive T-Lymphocytes/immunology,virology Cross Reactions Epitopes, T-Lymphocyte Graft Rejection Humans Immunodominant Epitopes Immunologic Memory Mice Viral Vaccines/immunology Viruses/immunology,pathogenicity
Chemicals
Antigens, Viral Epitopes, T-Lymphocyte Immunodominant Epitopes Viral Vaccines
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Welsh Raymond M
Department of Pathology, University of Massachusetts Medical School, Worcester, MA 01655, USA. [email protected]
Che Jenny W
Brehm Michael A
Selin Liisa K
References (162)
162 references, click to expand
  1. Heterologous T cell immunity in severe hepatitis C virus infection.
    J Exp Med. 2005 Mar 7;201(5):675-80 PMID: 15753202
  2. Human CD4+ memory T cells are preferential targets for bystander activation and apoptosis.
    J Immunol. 2009 Feb 15;182(4):1962-71 PMID: 19201849
  3. Specificity and degeneracy of T cells.
    Mol Immunol. 2004 Feb;40(14-15):1047-55 PMID: 15036909
  4. Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses.
    Immunity. 1999 Dec;11(6):733-42 PMID: 10626895
  5. Pathogenic epitopes, heterologous immunity and vaccine design.
    Nat Rev Microbiol. 2007 Jul;5(7):555-63 PMID: 17558423
  6. Structural basis of 2C TCR allorecognition of H-2Ld peptide complexes.
    Immunity. 1998 May;8(5):553-62 PMID: 9620676
  7. Minimal bystander activation of CD8 T cells during the virus-induced polyclonal T cell response.
    J Exp Med. 1997 May 5;185(9):1629-39 PMID: 9151900
  8. Comprehensive early and lasting loss of memory CD8 T cells and functional memory during acute and persistent viral infections.
    J Immunol. 2004 Mar 1;172(5):3139-50 PMID: 14978120
  9. Heterologous immunity provides a potent barrier to transplantation tolerance.
    J Clin Invest. 2003 Jun;111(12):1887-95 PMID: 12813024
  10. Cross-reactive memory T cells for Epstein-Barr virus augment the alloresponse to common human leukocyte antigens: degenerate recognition of major histocompatibility complex-bound peptide by T cells and its role in alloreactivity.
    Eur J Immunol. 1997 Jul;27(7):1726-36 PMID: 9247584
  11. Probing degeneracy in T-cell recognition using peptide combinatorial libraries.
    Immunol Today. 1998 Apr;19(4):163-8 PMID: 9577092
  12. Dynamics of memory T cell proliferation under conditions of heterologous immunity and bystander stimulation.
    J Immunol. 2002 Jul 1;169(1):90-8 PMID: 12077233
  13. Necrosis of adipose tissue induced by sequential infections with unrelated viruses.
    Am J Pathol. 1985 Aug;120(2):173-7 PMID: 4025507
  14. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function, and responsiveness.
    Adv Immunol. 1979;27:51-177 PMID: 92183
  15. Virus-induced polyclonal cytotoxic T lymphocyte stimulation.
    J Immunol. 1989 Mar 1;142(5):1710-8 PMID: 2537363
  16. Non-specific beneficial effect of measles immunisation: analysis of mortality studies from developing countries.
    BMJ. 1995 Aug 19;311(7003):481-5 PMID: 7647643
  17. A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus.
    Nat Biotechnol. 2006 Jul;24(7):817-9 PMID: 16767078
  18. High frequency of cross-reactive cytotoxic T lymphocytes elicited during the virus-induced polyclonal cytotoxic T lymphocyte response.
    J Exp Med. 1993 Feb 1;177(2):317-27 PMID: 8093891
  19. Bystander activation of CD8+ T lymphocytes during experimental mycobacterial infection.
    Infect Immun. 2004 Dec;72(12):6884-91 PMID: 15557609
  20. Molecular mimicry: a mechanism for autoimmune injury.
    FASEB J. 1992 Feb 1;6(3):840-4 PMID: 1740233
  21. Chronic Leishmania donovani infection promotes bystander CD8+-T-cell expansion and heterologous immunity.
    Infect Immun. 2005 Dec;73(12):7996-8001 PMID: 16299292
  22. Immunopathology in RSV infection is mediated by a discrete oligoclonal subset of antigen-specific CD4(+) T cells.
    Immunity. 2001 Oct;15(4):637-46 PMID: 11672545
  23. Cross-reactive influenza virus-specific CD8+ T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis.
    J Clin Invest. 2005 Dec;115(12):3602-12 PMID: 16308574
  24. Essential flexibility in the T-cell recognition of antigen.
    Nature. 1996 Apr 11;380(6574):495-8 PMID: 8606766
  25. THE IMMUNOLOGICAL BASIS OF ACQUIRED CELLULAR RESISTANCE.
    J Exp Med. 1964 Jul 1;120:105-20 PMID: 14194388
  26. Influenza basic polymerase 2 peptides are recognized by influenza nucleoprotein-specific cytotoxic T lymphocytes.
    Mol Immunol. 1992 Sep;29(9):1089-96 PMID: 1495499
  27. Cytolytically active memory CTL present in lymphocytic choriomeningitis virus-immune mice after clearance of virus infection.
    J Immunol. 1997 Jun 1;158(11):5366-73 PMID: 9164957
  28. Direct visualization of cross-reactive effector and memory allo-specific CD8 T cells generated in response to viral infections.
    J Immunol. 2003 Apr 15;170(8):4077-86 PMID: 12682237
  29. Recognition of conserved amino acid motifs of common viruses and its role in autoimmunity.
    PLoS Pathog. 2005 Dec;1(4):e41 PMID: 16362076
  30. Cross-reactivity between hepatitis C virus and Influenza A virus determinant-specific cytotoxic T cells.
    J Virol. 2001 Dec;75(23):11392-400 PMID: 11689620
  31. Multiple glycines in TCR alpha-chains determine clonally diverse nature of human T cell memory to influenza A virus.
    J Immunol. 2008 Nov 15;181(10):7407-19 PMID: 18981164
  32. Analysis of murine CD8(+) T-cell clones specific for the Dengue virus NS3 protein: flavivirus cross-reactivity and influence of infecting serotype.
    J Virol. 1999 Jan;73(1):398-403 PMID: 9847344
  33. 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. 2004 May;24(3):258-71 PMID: 15114056
  34. Viral strategies of immune evasion.
    Science. 1998 Apr 10;280(5361):248-53 PMID: 9535648
  35. Heterologous immunity revisited.
    Parasitology. 2001;122 Suppl:S51-9 PMID: 11442196
  36. A very high level of crossreactivity is an essential feature of the T-cell receptor.
    Immunol Today. 1998 Sep;19(9):395-404 PMID: 9745202
  37. Cutting edge: CD4 and CD8 T cells are intrinsically different in their proliferative responses.
    J Immunol. 2002 Feb 15;168(4):1528-32 PMID: 11823476
  38. Single-cell PCR analysis of TCR repertoires selected by antigen in vivo: a high magnitude CD8 response is comprised of very few clones.
    Immunity. 1996 Jan;4(1):47-55 PMID: 8574851
  39. A basis for alloreactivity: MHC helical residues broaden peptide recognition by the TCR.
    Immunity. 1998 May;8(5):543-52 PMID: 9620675
  40. The repertoire of T cells shaped by a single MHC/peptide ligand.
    Cell. 1996 Feb 23;84(4):521-9 PMID: 8598039
  41. Crossreactivity of the T-cell receptor.
    Immunol Today. 1998 Sep;19(9):428-9 PMID: 9745208
  42. Evolution of the T cell repertoire during primary, memory, and recall responses to viral infection.
    J Immunol. 2000 Dec 1;165(11):6081-90 PMID: 11086040
  43. 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 PMID: 13651915
  44. A fractal clonotype distribution in the CD8+ memory T cell repertoire could optimize potential for immune responses.
    J Immunol. 2003 Apr 15;170(8):3994-4001 PMID: 12682227
  45. Apoptosis regulators Bim and Fas function concurrently to control autoimmunity and CD8+ T cell contraction.
    Immunity. 2008 Feb;28(2):218-30 PMID: 18275832
  46. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity.
    J Virol. 1995 Aug;69(8):4633-9 PMID: 7609027
  47. High frequencies of virus-specific CD8+ T-cell precursors.
    J Virol. 2009 Dec;83(24):12907-16 PMID: 19812167
  48. Induction of alloreactive cytotoxic T cells by acute virus infection of mice.
    J Immunol. 1986 Feb 15;136(4):1186-93 PMID: 2418107
  49. Rapid production of TNF-alpha following TCR engagement of naive CD8 T cells.
    J Immunol. 2005 Oct 15;175(8):5043-9 PMID: 16210607
  50. Narrowed TCR repertoire and viral escape as a consequence of heterologous immunity.
    J Clin Invest. 2006 May;116(5):1443-56 PMID: 16614754
  51. An analysis of cytomegalovirus infection and HLA antigen matching on the outcome of renal transplantation.
    Ann Surg. 1978 Feb;187(2):110-7 PMID: 204263
  52. T cell cross-reactivity and conformational changes during TCR engagement.
    J Exp Med. 2004 Dec 6;200(11):1455-66 PMID: 15583017
  53. Quantitative analysis of hepatitis C virus-specific CD8(+) T cells in peripheral blood and liver using peptide-MHC tetramers.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5692-7 PMID: 10318946
  54. Secreted respiratory syncytial virus G glycoprotein induces interleukin-5 (IL-5), IL-13, and eosinophilia by an IL-4-independent mechanism.
    J Virol. 1999 Oct;73(10):8485-95 PMID: 10482601
  55. T cell homeostatic proliferation elicits effective antitumor autoimmunity.
    J Clin Invest. 2002 Jul;110(2):185-92 PMID: 12122110
  56. The many important facets of T-cell repertoire diversity.
    Nat Rev Immunol. 2004 Feb;4(2):123-32 PMID: 15040585
  57. Protection against vaccinia virus challenge by CD8 memory T cells resolved by molecular mimicry.
    J Virol. 2007 Jan;81(2):934-44 PMID: 17079318
  58. Herpesvirus latency confers symbiotic protection from bacterial infection.
    Nature. 2007 May 17;447(7142):326-9 PMID: 17507983
  59. The privacy of T cell memory to viruses.
    Curr Top Microbiol Immunol. 2006;311:117-53 PMID: 17048707
  60. 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 Aug 14;1(1):3 PMID: 14527342
  61. 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 Dec 15;98(13):3739-44 PMID: 11739180
  62. Interferon enhances the susceptibility of virus-infected fibroblasts to cytotoxic T cells.
    J Exp Med. 1985 Jan 1;161(1):257-62 PMID: 2578543
  63. Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8987-90 PMID: 1833769
  64. Resting memory CD8+ T cells are hyperreactive to antigenic challenge in vitro.
    J Exp Med. 1996 Dec 1;184(6):2141-51 PMID: 8976170
  65. Stability and diversity of T cell receptor repertoire usage during lymphocytic choriomeningitis virus infection of mice.
    J Exp Med. 1998 Dec 7;188(11):1993-2005 PMID: 9841914
  66. Cutting edge: persistent viral infection prevents tolerance induction and escapes immune control following CD28/CD40 blockade-based regimen.
    J Immunol. 2002 Nov 15;169(10):5387-91 PMID: 12421910
  67. Partial agonist effect influences the CTL response to a heterologous dengue virus serotype.
    J Immunol. 1999 Sep 1;163(5):2754-60 PMID: 10453018
  68. 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 Apr 1;176(7):4284-95 PMID: 16547266
  69. The influence of antiviral T-cell responses on the alloreactive repertoire.
    Immunol Today. 1999 May;20(5):203-7 PMID: 10322297
  70. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung.
    Nat Immunol. 2001 Nov;2(11):1067-76 PMID: 11668342
  71. Viral infection and renal transplant rejection.
    Br Med J. 1972 Dec 2;4(5839):520-2 PMID: 4566016
  72. Induction or prevention of immunopathological disease by cloned cytotoxic T cell lines specific for lymphocytic choriomeningitis virus.
    Eur J Immunol. 1986 Apr;16(4):387-93 PMID: 3084281
  73. Identification and analysis for cross-reactivity among hantaviruses of H-2b-restricted cytotoxic T-lymphocyte epitopes in Sin Nombre virus nucleocapsid protein.
    J Gen Virol. 2004 Jul;85(Pt 7):1909-1919 PMID: 15218176
  74. Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations.
    J Exp Med. 1998 Nov 2;188(9):1705-15 PMID: 9802982
  75. Virus-specific CD8+ T-cell responses in mice transgenic for a T-cell receptor beta chain selected at random.
    J Virol. 1994 May;68(5):3065-70 PMID: 7908699
  76. Memory of mice and men: CD8+ T-cell cross-reactivity and heterologous immunity.
    Immunol Rev. 2006 Jun;211:164-81 PMID: 16824126
  77. Viruses can silently prime for and trigger central nervous system autoimmune disease.
    J Neurovirol. 2001 Jun;7(3):220-7 PMID: 11517396
  78. The role of T cells in anti-herpes simplex virus immunity. I. Induction of antigen-specific cytotoxic T lymphocytes.
    J Immunol. 1977 Sep;119(3):939-44 PMID: 70478
  79. BCG vaccination scar associated with better childhood survival in Guinea-Bissau.
    Int J Epidemiol. 2005 Jun;34(3):540-7 PMID: 15659474
  80. T cell receptor recognition motifs govern immune escape patterns in acute SIV infection.
    Immunity. 2004 Dec;21(6):793-803 PMID: 15589168
  81. Multiple HLA class I-dependent cytotoxicities constitute the "non-HLA-restricted" response in infectious mononucleosis.
    Eur J Immunol. 1987 Jul;17(7):1007-13 PMID: 2440688
  82. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses.
    Annu Rev Immunol. 1999;17:51-88 PMID: 10358753
  83. Vaccinia virus-specific CD4+ T cell responses target a set of antigens largely distinct from those targeted by CD8+ T cell responses.
    J Immunol. 2007 Jun 1;178(11):6814-20 PMID: 17513729
  84. Amino acid similarity accounts for T cell cross-reactivity and for "holes" in the T cell repertoire.
    PLoS One. 2008 Mar 19;3(3):e1831 PMID: 18350167
  85. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape.
    J Exp Med. 2004 Aug 2;200(3):307-19 PMID: 15289502
  86. CD4 T-cell-mediated heterologous immunity between mycobacteria and poxviruses.
    J Virol. 2009 Apr;83(8):3528-39 PMID: 19193795
  87. Rapid quantification of naive alloreactive T cells by TNF-alpha production and correlation with allograft rejection in mice.
    Blood. 2007 Jan 15;109(2):819-26 PMID: 16973964
  88. Dengue virus-reactive CD8+ T cells display quantitative and qualitative differences in their response to variant epitopes of heterologous viral serotypes.
    J Immunol. 2006 Mar 1;176(5):2817-24 PMID: 16493038
  89. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens.
    Nat Immunol. 2002 Jul;3(7):627-34 PMID: 12055626
  90. Human memory cytotoxic T-lymphocyte (CTL) responses to Hantaan virus infection: identification of virus-specific and cross-reactive CD8(+) CTL epitopes on nucleocapsid protein.
    J Virol. 1999 Jul;73(7):5301-8 PMID: 10364276
  91. Polyspecificity of T cell and B cell receptor recognition.
    Semin Immunol. 2007 Aug;19(4):216-24 PMID: 17398114
  92. Virus-induced abrogation of transplantation tolerance induced by donor-specific transfusion and anti-CD154 antibody.
    J Virol. 2000 Mar;74(5):2210-8 PMID: 10666251
  93. Resistance to vaccinia virus is less dependent on TNF under conditions of heterologous immunity.
    J Immunol. 2009 Nov 15;183(10):6554-60 PMID: 19846867
  94. Very diverse CD8 T cell clonotypic responses after virus infections.
    J Immunol. 2004 Mar 1;172(5):3151-6 PMID: 14978121
  95. Individuality of Ag-selected and preimmune TCR repertoires.
    Immunol Res. 2001;23(1):75-84 PMID: 11417861
  96. Respiratory manifestations of chicken pox; special consideration of the features of primary varicella pneumonia.
    AMA Arch Intern Med. 1956 Jul;98(1):91-9 PMID: 13338899
  97. 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 May;72(5):3999-4004 PMID: 9557687
  98. Cutting edge: re-evaluating the in vivo cytokine responses of CD8+ T cells during primary and secondary viral infections.
    J Immunol. 2005 May 15;174(10):5936-40 PMID: 15879085
  99. Attrition of memory CD8 T cells.
    Nature. 2009 Jun 4;459(7247):E3-4; discussion E4 PMID: 19494857
  100. Depletion of T cells by type I interferon: differences between young and aged mice.
    J Immunol. 2005 Aug 1;175(3):1820-6 PMID: 16034124
  101. Private specificities of heterologous immunity.
    Curr Opin Immunol. 2006 Jun;18(3):331-7 PMID: 16597500
  102. Clonotypic structure of the human CD4+ memory T cell response to cytomegalovirus.
    J Immunol. 2001 Aug 1;167(3):1151-63 PMID: 11466329
  103. Survival of mouse pancreatic islet allografts in recipients treated with allogeneic small lymphocytes and antibody to CD40 ligand.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9560-4 PMID: 7568172
  104. Programming for CD8 T cell memory development requires IL-12 or type I IFN.
    J Immunol. 2009 Mar 1;182(5):2786-94 PMID: 19234173
  105. Specificity of peptide binding by the HLA-A2.1 molecule.
    J Immunol. 1989 Nov 1;143(9):2939-47 PMID: 2553813
  106. 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 May;77(9):5464-74 PMID: 12692247
  107. Influenza virus lung infection protects from respiratory syncytial virus-induced immunopathology.
    J Exp Med. 2000 Nov 6;192(9):1317-26 PMID: 11067880
  108. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals.
    J Clin Invest. 2008 Oct;118(10):3478-90 PMID: 18802496
  109. Size estimate of the alpha beta TCR repertoire of naive mouse splenocytes.
    J Immunol. 2000 Jun 1;164(11):5782-7 PMID: 10820256
  110. Immunological memory to viral infections.
    Annu Rev Immunol. 2004;22:711-43 PMID: 15032594
  111. A direct estimate of the human alphabeta T cell receptor diversity.
    Science. 1999 Oct 29;286(5441):958-61 PMID: 10542151
  112. Turnover of naive- and memory-phenotype T cells.
    J Exp Med. 1994 Apr 1;179(4):1127-35 PMID: 8145034
  113. Lack of prominent peptide-major histocompatibility complex features limits repertoire diversity in virus-specific CD8+ T cell populations.
    Nat Immunol. 2005 Apr;6(4):382-9 PMID: 15735650
  114. Poxvirus CD8+ T-cell determinants and cross-reactivity in BALB/c mice.
    J Virol. 2006 Jul;80(13):6318-23 PMID: 16775319
  115. A viral epitope that mimics a self antigen can accelerate but not initiate autoimmune diabetes.
    J Clin Invest. 2004 Nov;114(9):1290-8 PMID: 15520861
  116. Visualization, characterization, and turnover of CD8+ memory T cells in virus-infected hosts.
    J Exp Med. 1996 Apr 1;183(4):1367-75 PMID: 8666895
  117. Early programming of T cell populations responding to bacterial infection.
    J Immunol. 2000 Dec 15;165(12):6833-9 PMID: 11120806
  118. CD8+ memory T cells (CD44high, Ly-6C+) are more sensitive than naive cells to (CD44low, Ly-6C-) to TCR/CD8 signaling in response to antigen.
    J Immunol. 1998 Apr 1;160(7):3236-43 PMID: 9531279
  119. Characterization of the T cell-mediated cellular cytotoxicity during acute infectious mononucleosis.
    J Immunol. 1989 Jul 15;143(2):660-70 PMID: 2472449
  120. Attrition of virus-specific memory CD8+ T cells during reconstitution of lymphopenic environments.
    J Immunol. 2003 Jul 15;171(2):655-63 PMID: 12847230
  121. Type 1 IFN mediates cross-talk between innate and adaptive immunity that abrogates transplantation tolerance.
    J Immunol. 2007 Nov 15;179(10):6620-9 PMID: 17982052
  122. The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: uncovering new tricks for an old virus.
    J Virol. 2007 May;81(10):4928-40 PMID: 17329346
  123. Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation.
    Nat Immunol. 2001 May;2(5):423-9 PMID: 11323696
  124. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes.
    Nature. 1998 Jul 30;394(6692):482-5 PMID: 9697771
  125. Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr, and Bcl-2-transgenic mice.
    Am J Pathol. 1995 Jul;147(1):79-91 PMID: 7604887
  126. 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 Jan 1;193(1):49-53 PMID: 16323131
  127. Elevated natural killer cell-mediated cytotoxicity, plasma interferon, and tumor cell rejection in mice persistently infected with lymphocytic choriomeningitis virus.
    J Immunol. 1983 Aug;131(2):991-6 PMID: 6190947
  128. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever.
    Nat Med. 2003 Jul;9(7):921-7 PMID: 12808447
  129. Defective generation but normal maintenance of memory T cells in old mice.
    Eur J Immunol. 2002 Jun;32(6):1567-73 PMID: 12115639
  130. Attrition of bystander CD8 T cells during virus-induced T-cell and interferon responses.
    J Virol. 2001 Jul;75(13):5965-76 PMID: 11390598
  131. Development of the Mycobacterium bovis BCG vaccine: review of the historical and biochemical evidence for a genealogical tree.
    Tuber Lung Dis. 1999;79(4):243-50 PMID: 10692993
  132. Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade.
    Rev Infect Dis. 1989 May-Jun;11 Suppl 4:S830-9 PMID: 2665015
  133. Viral infection of transgenic mice expressing a viral protein in oligodendrocytes leads to chronic central nervous system autoimmune disease.
    J Exp Med. 1996 Dec 1;184(6):2371-84 PMID: 8976191
  134. Two-step binding mechanism for T-cell receptor recognition of peptide MHC.
    Nature. 2002 Aug 1;418(6897):552-6 PMID: 12152083
  135. Cuttine edge: T cells from aged mice are resistant to depletion early during virus infection.
    J Immunol. 2003 Oct 1;171(7):3353-7 PMID: 14500628
  136. Selective expansion of cross-reactive CD8(+) memory T cells by viral variants.
    J Exp Med. 1999 Nov 1;190(9):1319-28 PMID: 10544203
  137. Immunization of mice with vaccinia virus-M2 recombinant induces epitope-specific and cross-reactive Kd-restricted CD8+ cytotoxic T cells.
    J Virol. 1993 Jul;67(7):4086-92 PMID: 7685408
  138. Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses.
    J Exp Med. 1977 Mar 1;145(3):557-68 PMID: 233901
  139. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses.
    J Exp Med. 1994 Jun 1;179(6):1933-43 PMID: 8195718
  140. Private specificities of CD8 T cell responses control patterns of heterologous immunity.
    J Exp Med. 2005 Feb 21;201(4):523-33 PMID: 15710651
  141. Enhanced susceptibility to cytotoxic T lymphocytes of target cells isolated from virus-infected or interferon-treated mice.
    J Virol. 1986 Sep;59(3):735-9 PMID: 3488417
  142. In vivo state of antiviral CTL precursors. Characterization of a cycling cell population containing CTL precursors in immune mice.
    J Immunol. 1995 Jan 15;154(2):620-32 PMID: 7529281
  143. Multiple sclerosis and virus induced immune responses: autoimmunity can be primed by molecular mimicry and augmented by bystander activation.
    Autoimmunity. 2006 Feb;39(1):9-19 PMID: 16455578
  144. Beneficial non-targeted effects of BCG--ethical implications for the coming introduction of new TB vaccines.
    Tuberculosis (Edinb). 2006 Nov;86(6):397-403 PMID: 16901755
  145. Antibody-dependent enhancement of infection and the pathogenesis of viral disease.
    Clin Infect Dis. 1994 Sep;19(3):500-12 PMID: 7811870
  146. Memory CD8 T-cell compartment grows in size with immunological experience.
    Nature. 2009 Jan 8;457(7226):196-9 PMID: 19005468
  147. Specific history of heterologous virus infections determines anti-viral immunity and immunopathology in the lung.
    Am J Pathol. 2003 Oct;163(4):1341-55 PMID: 14507643
  148. Recognition of disparate HA and NS1 peptides by an H-2Kd-restricted, influenza specific CTL clone.
    Mol Immunol. 1991 Jan-Feb;28(1-2):1-7 PMID: 1707132
  149. Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR.
    Nat Immunol. 2001 Aug;2(8):711-7 PMID: 11477407
  150. Cross-reactive antigen is required to prevent erosion of established T cell memory and tumor immunity: a heterologous bacterial model of attrition.
    J Immunol. 2002 Aug 1;169(3):1197-206 PMID: 12133940
  151. Naive precursor frequencies and MHC binding rather than the degree of epitope diversity shape CD8+ T cell immunodominance.
    J Immunol. 2008 Aug 1;181(3):2124-33 PMID: 18641351
  152. An epidemiologic study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine.
    Am J Epidemiol. 1969 Apr;89(4):405-21 PMID: 4305197
  153. Routine vaccinations and child survival: follow up study in Guinea-Bissau, West Africa.
    BMJ. 2000 Dec 9;321(7274):1435-8 PMID: 11110734
  154. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections.
    J Exp Med. 1996 Jun 1;183(6):2489-99 PMID: 8676069
  155. Cross-reactive memory CD8(+) T cells alter the immune response to heterologous secondary dengue virus infections in mice in a sequence-specific manner.
    J Infect Dis. 2008 Feb 15;197(4):608-17 PMID: 18275279
  156. Human herpesvirus 6: infection and disease following autologous and allogeneic bone marrow transplantation.
    Blood. 1996 Jun 15;87(12):5341-54 PMID: 8652850
  157. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus.
    Nat Med. 1997 Feb;3(2):205-11 PMID: 9018240
  158. Memory CD8+ T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen.
    J Exp Med. 2003 Nov 17;198(10):1583-93 PMID: 14623912
  159. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells.
    Nat Immunol. 2001 May;2(5):415-22 PMID: 11323695
  160. No one is naive: the significance of heterologous T-cell immunity.
    Nat Rev Immunol. 2002 Jun;2(6):417-26 PMID: 12093008
  161. Activation of virus-specific CD8+ T cells by lipopolysaccharide-induced IL-12 and IL-18.
    J Immunol. 2004 Dec 1;173(11):6873-81 PMID: 15557182
  162. 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 Sep 5;202(5):637-50 PMID: 16129706
Article Info
Journal
Immunological reviews
Abbr.
Immunol Rev
ISSN
1600-065X
DOI
10.1111/j.0105-2896.2010.00897.x
Email
[email protected]
Published
2010-05-00
Pages
244-66
Language
English
Region
England
NLM ID
7702118
PMCID
PMC2917921
Subset
IM
Grants
NIAID NIH HHS · AI073540 · United States
NIDDK NIH HHS · P30 DK032520-26S2 · United States
NIAID NIH HHS · AI017672 · United States
NIAID NIH HHS · P01 AI049320 · United States
NIAID NIH HHS · R01 AI046578-02 · United States
NIAID NIH HHS · R01 AI017672-20 · United States
NIAID NIH HHS · R37 AI017672 · United States
NIAID NIH HHS · P01 AI046629-010001 · United States
NIAID NIH HHS · P01 AI046629-10A1 · United States
NIAID NIH HHS · R01 AI081675 · United States
NIAID NIH HHS · R01 AI054455 · United States
NIAMS NIH HHS · R01 AR035506 · United States
NIAID NIH HHS · R01 AI081675-24 · United States
NIAID NIH HHS · AI049320 · United States
NIAID NIH HHS · AI073871 · United States
NIAID NIH HHS · U19 AI057330-05S10007 · United States
NIAMS NIH HHS · R01 AR035506-13 · United States
NIAID NIH HHS · U01 AI073871 · United States
NIAID NIH HHS · U01 AI073871-03 · United States
NIAID NIH HHS · P01 AI046629-11 · United States
NIAID NIH HHS · R01 AI046578 · United States
NIAID NIH HHS · U01 AI073871-05S1 · United States
NIDDK NIH HHS · P30 DK032520 · United States
NIAID NIH HHS · U19 AI057330 · United States
NIAID NIH HHS · P01 AI046629 · United States
NIAID NIH HHS · AI046578 · United States
NIAID NIH HHS · R37 AI017672-25 · United States
NIAID NIH HHS · P01 AI049320-010002 · United States
NIAID NIH HHS · AI46692 · United States
NIAID NIH HHS · AI054455 · United States
NIAID NIH HHS · AI081675 · United States
NIAID NIH HHS · R01 AI054455-01 · United States
NIAID NIH HHS · R01 AI017672 · United States
External Links
PubMed source DOI: 10.1111/j.0105-2896.2010.00897.x PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2