No one is naive: The significance of heterologous T-cell immunity

Nature Reviews Immunology

Volumn 2, Issue 6, 2002, Pages 417-426

  Welsh, Raymond M ^a   Selin, Liisa K ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; CELLULAR IMMUNITY; HELPER CELL; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOPATHOLOGY; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL; VIRUS INFECTION; ADIPOSE TISSUE; ANIMAL; BIOLOGICAL MODEL; IMMUNOLOGY; LUNG; LYMPHOCYTE ACTIVATION; METABOLISM; VIRUS;

ADIPOSE TISSUE; ANIMALS; HUMANS; IMMUNOLOGIC MEMORY; LUNG; LYMPHOCYTE ACTIVATION; MICE; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; VIRUS DISEASES; VIRUSES;

EID: 0036593039     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri820     Document Type: Review

References (104)

1. Matthew, A. et 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. 72, 3999-4004 (1998). This study shows that different dengue-virus serotypes have high homology in terms of T-cell epitopes, and they induce crossreactive T-cell responses.
2. Halstead, S. B. Antibody, macrophages, dengue-virus infection, shock and hemorrhage: a pathogenetic cascade. Rev. Infect. Dis. 11, S830-S839 (1989).
3. Bjorkman, P. J. MHC restriction in three dimensions: a view of T-cell receptor/ligand interactions. Cell 89, 167-170 (1997).
4. Yewdell, J. W. & Bennink, J. R. Immunodominance in major histocompatibility complex class-I-restricted T-lymphocyte responses. Annu. Rev. Immunol. 17, 51-88 (1999).
5. Falk, K., Rotzschke, O., Stevanovic, S., Jung, G. & Rammensee, H. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351, 290-296 (1991).
6. + T-cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nature Immunol. 2, 415-422 (2001).
7. van Stipdonk, M. J., Lemmens, E. E. & Schoenberger, S. P. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differantiation. Nature Immunol. 2, 423-429 (2001).
8. Mercado, R. et al. Early programming of T-cell populations responding to bacterial infection. J. Immunol. 165, 6833-6839 (2000).
9. + T cells during viral infections, and shows that this population remains stable in long-term memory, and that heterologous virus infections disrupt this stability and cause reductions in the memory response to previously encountered viruses.
10. Razvi, E. S., Jiang, Z., Woda, B. A. & Welsh, R. M. 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, 79-91 (1995).
11. Masopust, D., Vezys, V., Marzo, A. L. & Lefrancois, L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413-2417 (2001). Memory T cells reside at high frequencies in peripheral organs.
12. + T cells migrate into peripheral organs as they disappear from the lymphoid organs at the end stage of the T-cell response to viral infections.
13. Van der Most, R. G. et al. Identification of Db- and Kb-restricted subdominant cytotoxic T-cell responses in lymphocytic choriomeningitis virus-infected mice. Virology 240, 158-167 (1998).
14. Chen, W., Anton, L. C., Bennink, J. R. & Yewdell, J. W. Dissecting the multifactorial causes of immunodominance in class-I-restricted T-cell responses to viruses. Immunity 12, 83-93 (2000).
15. Vitiello, A. et al. Immunodominance analysis of CTL responses to influenza PR8 virus reveals two dominant and subdominant Kb-restricted epitopes. J. Immunol. 157, 5555-5562 (1996).
16. + T-cell response during acute and persistent murine γ-herpesvirus infection. Eur. J. Immunol. 29, 1059-1067 (1999).
17. Wallace, M. E., Keating, R., Heath, W. R. & Carbone, F. R. The cytotoxic T-cell response to herpes simplex virus type 1 infection of C57BL/6 mice is almost entirely directed against a single immunodominant determinant. J. Virol. 73, 7619-7626 (1999).
18. + T-cell response to influenza A viruses. J. Immunol. 165, 2404-2409 (2000).
19. + T-cell response is similar.
20. Bousso, P. et al. Individual variations in the murine T-cell response to a specific peptide reflect variability in naive repertoire. Immunity 9, 169-178 (1998).
21. Blattman, J. N., Sourdive, D. J., Murali-Krishna, K., Ahmed, R. & Altman, J. D. Evolution of the T-cell repertoire during primary, memory and recall responses to viral infection. J. Immunol. 165, 6081-6090 (2000).
22. Mason, D. A very high level of crossreactivity is an essential feature of the T-cell repertoire. Immunol. Today 19, 395-404 (1998). This paper provides theoretical calculations that indicate that T cells must be highly crossreactive.
23. + and can be selectively activated with phorbol ester and calcium ionophore. Cell. Immunol. 113, 268-277 (1988).
24. Bradley, L. M., Croft, M. & Swain, S. L. T-cell memory: new perspectives. Immunol. Today 14, 197-199 (1993).
25. + T cells are hyperactive to antigenic challenge in vitro. J. Exp. Med. 184. 2141-2151 (1996).
26. +) to TCR/CD8 signaling in response to antigen. J. Immunol. 160, 3236-3243 (1998).
27. Veiga-Fernandes, H., Walter, U., Bourgeois, C., McLean, A. & Rocha, B. Response of naive and memory CD8 T cells to antigen stimulation in vivo. Nature Immunol. 1, 47-53 (2000).
28. b-restricted anti-vesicular stomatitis virus and alloreactive cytotoxic T cells. J. Immunol. 138, 3654-3660 (1987).
29. Braciale, T. J., Andrew, M. E. & Braciale, V. L. Simultaneous expression of H-2-restricted and alloreactive recognition by a cloned line of influenza virus-specific cytotoxic T lymphocytes. J. Exp. Med. 153, 1371-1376 (1981).
30. Anderson, R. W., Bennick, J. R., Yewdell, J. W., Maloy, W. L. & Coligan, J. E. Influenza basic polymerase 2 peptides are recognized by influenza nucleoprotein-specific cytotoxic T lymphocytes. Mol. Immunol. 29, 1089-1096 (1992).
31. d-restricted, influenza-specific CTL clone. Mol. Immunol. 28, 1-7 (1991).
32. Yang, H. & Welsh, R. M. Induction of alloreactive cytotoxic T cells by acute virus infection of mice. J. Immunol. 136, 1186-1193 (1986).
33. Tomkinson, B. E., Maziarz, R. & Sullivan, J. L. Characterization of the T-cell-mediated cellular cytotoxicity during infectious mononucleosis. J. Immunol. 143, 660-670 (1989).
34. Strang, G. & Rickinson, A. B. Multiple HLA class-I-dependent cytotoxicities constitute the 'non-HLA-estricted' response in infectious mononucleosis. Eur. J. Immunol. 17, 1007-1013 (1987).
35. Burrows, S. R. et al. 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. 27, 1726-1736 (1997).
36. Burrows, S. R., Khanna, R., Silins, S. L. & Moss, D. J. The influence of antiviral T-cell responses on the alloreactive repertoire. Immunol. Today 20, 203-207 (1999).
37. Nahill, S. R. & Welsh, R. M. High frequency of cross-reactive cytotoxic T lymphocytes elicited during the virus-induced polyclonal cytotoxic T-lymphocyte response. J. Exp. Med. 177, 317-327 (1993).
38. Selin, L. K., Nahill, S. R. & Welsh, R. M. Cross-reactivities in memory cytotoxic T-lymphocyte recognition of heterologous viruses. J. Exp. Med. 179, 1933-1943 (1994).
39. Yang, H., Dundon, R. L., Nahill, S. R. & Welsh, R. M. Virus-induced polyclonal cytotoxic T-lymphocyte stimulation. J. Immunol. 142, 1710-1718 (1989).
40. Daniel, C., Horvath, S. & Allen, R. M. A basis for alloreactivity: MHC helical residues broaden peptide recognition by the TCR. Immunity 8, 543-552 (1998).
41. a peptide complexes. Immunity 8, 553-562 (1998).
42. Alam, S. M. & Gascoigne, N. R. Posttranslational regulation of TCR Vα allelic exclusion during T-cell differentiation. J. Immunol. 160, 3883-3890 (1998).
43. Welsh, R. M. et al. Virus-induced abrogation of transplantation tolerance induced by donor-specific transfusion and anti-CD 154 antibody. J. Virol. 74, 2210-2218 (2000).
44. + T-cell responses cannot be predicted by major histocompatibility complex class I haplotype. J. Virol. 74, 9144-9151 (2000). These authors show that predictable hierarchies of immunodominant epitopes of HIV are not seen in the 'wild' human population.
45. Day, C. L. et al. Relative dominance of epitope-specific cytotoxic T-lymphocyte responses in human immunodeficiency virus type-1-infected persons with shared HLA alleles. J. Virol. 75, 6279-6291 (2001).
46. Fazekas de St Groth, S. & Webster, R. G. Disquisitions on original antigenic sin. II. Proof in lower creatures. J. Exp. Med. 124, 347-361 (1966).
47. + T-cell populations during infection.
48. Klenerman, P. & Zinkernagel, R. M. Original antigenic sin impairs cytotoxic T-lymphocyte responses to viruses bearing variant epitopes Nature 394, 421-422 (1998).
49. Tough, D. F., Borrow, P. & Sprent, J. Induction of bystander T-cell proliferation by viruses and type I interferon in vivo. Science 272, 1947-1950 (1996).
50. Sprent, J., Zhang, X., Sun, S. & Tough, D. T-cell turnover in vivo and the role of cytokines. Immunol. Lett. 65, 21-25 (1999).
51. Zarozinski, C. C. & Welsh, R. M. Minimal bystander activation of CD8 T cells during the virus-induced polyclonal T-cell response. J. Exp. Med. 185, 1629-1639 (1997).
52. + T cells.
53. Mahalingam, S., Foster, P. S., Lobigs, S., Farber, J. M. & Karupiah, G. Interferon-inducible chemokines and immunity to poxvirus infections. Immunol. Rev. 177, 127-133 (2000).
54. + T cells to the lung during influenza pneumonia. J. Immunol. 167, 6983-6990 (2001).
55. + memory T cells by opposing cytokines. Science 288, 675-678 (2000).
56. + T cells. Proc. Natl Acad. Sci. USA 96, 8597-8602 (1999).
57. + T-cell proliferation in the persistent phases of a γ-herpesvirus infection. J. Virol. 75, 4435-4438 (2001).
58. + T-cell responses to an influenza virus. J. Immunol. 167, 2753-2758 (2001).
59. Lau, L. L., Jamieson, B. D., Somasundaram, T. & Ahmed, R. Cytotoxic T-cell memory without antigen. Nature 369, 648-652 (1994).
60. + memory. Nature Med. 7, 892-893 (2001).
61. Razvi, E. S., Welsh, R. M. & McFarland, H. I. In vivo state of antiviral CTL precursors: characterization of a cycling population containing CTL precursors in immune mice. J. Immunol. 154, 620-632 (1995).
62. Sprent, J. & Tough, D. F. Lymphocyte life-span and memory. Science 265, 1395-1400 (1996).
63. + memory T cells in virus-infected hosts. J. Exp. Med. 183, 1367-1375 (1996).
64. + T cells that are specific for previously encountered viruses are reduced in number by heterologous viral infections, and there is a selective loss of some specificities but not others.
65. + T cells in heterologous antiviral immunity and immunopathology in the lung. Nature Immunol. 2, 1067-1076 (2001). This study shows the recruitment and activation of LCMV-specific memory T cells into the lung during vaccinia virus infection, which results in marked immunopathology in a respiratory model of heterologous immunity.
66. + T cells during acute infection with lymphocytic choriomeningitis virus. J. Immunol. 161, 3215-3218 (1998).
67. H1 dominance during lymphocytic choriomeningitis virus infection. J. Virol. 74, 4429-4432 (2000).
68. + T-cell memory.
69. Selin, L. K., Varga, S. M., Wong, I. C. & Welsh, R. M. Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T-cell populations. J. Exp. Med. 188, 1705-1715 (1998). This shows the principle of heterologous immunity and immunopathology during viral infections.
70. Schlesinger, C., Meyer, C. A., Veeraraghavan, S. & Koss, M. N. Constructive (obliterative) bronchiolitis: diagnosis, etiology and a critical review of the literature. Ann. Diagn. Pathol. 2, 321-334 (1998).
71. Ploegh, H. L. Viral strategies of immune evasion. Science 280, 248-253 (1998).
72. Aaby, P. et al. Non-specific beneficial effect of measles immunisation: analysis of mortality studies from developing countries. BMJ 311, 481-485 (1995).
73. + T-cell mechanisms in the control of respiratory virus infections. Immunol. Rev. 159, 105-117 (1997).
74. Jameson, J., Cruz, J. & Ennis, F. A. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J. Virol. 72, 8682-8689 (1998). This paper identifies several influenza virus T-cell epitopes, some of which are crossreactive between strains.
75. Yang, H., Jons, I., Majno, G. & Welsh, R. M. Necrosis of adipose tissue induced by sequential infections with unrelated viruses. Am. J. Pathol. 120, 173-177 (1985).
76. Bolognia, J. & Braverman, I. M. In Harrison's Principles of Internal Medicine (eds Isselbacher, K. J. et al.) 290-307 (McGraw-Hill, New York, 1992).
77. Zhao, Z.-S., Granucci, F., Yeh, L., Schaffer, P. A. & Cantor, H. Molecular mimicry by herpes simplex virus type-1: autoimmune disease after viral infection. Science 279, 1344-1347 (1998).
78. Evans, C. F., Horwitz, M. S., Hobbs, M. V. & Oldstone, M. B. Viral infection of transgenic mice expressing a viral protein in oligodendrocytes leads to chronic central nervous system autoimmune disease. J. Exp. Med. 184, 2371-2384 (1996). This study shows that a virus can break tolerance to a transgene in the brain and induce transient encephalitis, which will undergo remission until exacerbated by a heterologous virus infection.
79. Swain, S. L. Helper T-cell differentiation. Curr. Opin. Immunol. 11, 180-185 (1999).
80. H1 cells. Eur. J. Immunol. 31, 1765-1771 (2001).
81. Swain, S. L. Interleukin-18: tipping the balance towards a T helper cell 1 response. J. Exp. Med. 194, F11-F14 (2001).
82. Cohn, L., Herrick, C., Niu, N., Homer, R. & Bottomly, K. IL-4 promotes airways eosinophilia by suppressing IFN-γ production: defining a novel role for IFN-γ in the regulation of allergic airway inflammation. J. Immunol. 166, 2760-2767 (2001).
83. Rook, G. A. & Stanford, J. L. Give us this day our daily germs. Immunol. Today 19, 113-116 (1998).
84. + T cells. Immunity 15, 637-646 (2001).
85. Kapikian, A. Z., Mitchell, R. H., Chanock, R. M., Shvedoff, R. A. & Stewart, C. E. 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, 405-421 (1969).
86. Cohn, L., Homer, R. J., Niu, N. & Bottomly, K. T helper 1 cells and interferon-γ regulate allergic airway inflammation and mucus production. J. Exp. Med. 190, 1309-1318 (1999).
87. Graham, B. S., Bunton, L. A., Wright, P. F. & Karzon, D. T. Role of T-lymphocyte subsets in the pathogenesis of primary infection and rechallenge with respiratory syncytial virus in mice. J. Clin. Invest. 88, 1026-1033 (1991).
88. H2-like response to RSV.
89. Johnson, T. R. & Graham, B. S. Secreted respiratory syncytial virus G glycoprotein induces interlieukin-5 (IL-5), IL-13 and eosinophilia by an IL-4-dependent mechanism. J. Virol. 73, 8485-8495 (1999).
90. Shirakawa, T., Enomoto, T., Shimazu, S. & Hopkin, J. M. The inverse association between tuberculin responses and atopic disorder. Science 275, 77-79 (1997).
91. Martinez, F. D. et al. Asthma and wheezing in the first six years of life. N. Engl. J. Med. 332, 133-138 (1995).
92. Shaheen, S. O. et al. Measles and atopy in Guinea-Bissau. Lancet 347, 1792-1796 (1996).
93. H2 response by an allergen.
94. Wedemeyer, H., Mizukoshi, E., Davis, A. R., Bennink, J. R. & Rehermann, B. Cross-reactivity between hepatitis C virus and influenza A virus determinant-specific cytotoxic T cells. J. Virol. 75, 11392-11400 (2001). Defines a strong crossreactive epitope between hepatitis C virus and influenza virus.
95. Weinstein, L. & Meade, R. H. Respiratory manifestations of chickenpox. Arch. Intern. Med. 98, 91-99 (1956).
96. Rickinson, A. B. & Kieff, E. In Virology Vol. 2 (eds Fields, B. N. et al.) 2397-2446 (Lippincott-Raven, Philadelphia, 1996).
97. Moss, D. J., Burrows, S. R., Silins, S. L., Misko, I. & Khanna, R. The immunology of Epstein-Barr virus infection. Phil. Trans. R. Soc. Lond. B Biol. Sci. 356, 475-488 (2001).
98. + lymphocytes respond to different HIV epitopes in seronegative and infected subjects. J. Clin. Invest. 107, 1303-1310 (2001). This study provides evidence of HIV-specific T cells in seronegative and HIV-negative subjects at high risk of HIV infection.
99. Tillmann, H. L. et al. Infection with GB virus C and reduced mortality among HIV-infected patients. N. Engl. J. Med. 345, 715-724 (2001).
100. Xiang, J. et al. Effect of coinfection with GB virus C on survival among patients with HIV infection. N. Engl. J. Med. 345, 707-714 (2001).
101. Barnett, L. A. & Fujinami, R. S. Molecular mimicry: a mechanism for autoimmune injury. FASEB J. 6, 840-844 (1992).
102. Janeway, C. A. Innate immunity acknowledged. Immunologist 3, 198-200 (1995).
103. Smoller, B. R., Weishar, M. & Gray, M. H. An unusual cutaneous manifestation in Crohn's disease. Arch. Pathol. Lab. Med. 6, 609-610 (1990).
104. + T-cell responses during heterologous virus infections influence immunodominance, as the T cells that are specific for the cross-reactive memory epitopes dominate acute responses to the second virus and are preferentially maintained in memory of the first virus, whereas non-crossreactive memory T cells are lost.