Memory of mice and men: CD8+ T-cell cross-reactivity and heterologous immunity

Immunological Reviews

Volumn 211, Issue , 2006, Pages 164-181

  Selin, Liisa K ^a   Brehm, Michael A ^a   Naumov, Yuri N ^a   Cornberg, Markus ^b   Kim, Sung Kwon ^c   Clute, Shalyn C ^d   Welsh, Raymond M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c Valeant Pharmaceuticals International   (United States)

^d Discovery Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; CYTOKINE; EPITOPE; GAMMA INTERFERON; HLA A2 ANTIGEN; HLA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR;

ALLOGRAFT; APOPTOSIS; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL FUNCTION; CELL POPULATION; CELL TRANSFER; CELLULAR IMMUNITY; CROSS REACTION; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; EPSTEIN BARR VIRUS; GRAFT REJECTION; HEPATITIS; HEPATITIS C VIRUS; HUMAN; HUMORAL IMMUNITY; IMMUNOMODULATION; INFECTIOUS MONONUCLEOSIS; INFLUENZA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOCYTOPENIA; MEMORY T LYMPHOCYTE; NONHUMAN; PICHINDE ARENAVIRUS; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; VACCINIA VIRUS; VIRUS INFECTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CROSS REACTIONS; EPITOPES, T-LYMPHOCYTE; HUMANS; IMMUNOLOGIC MEMORY; MICE; MODELS, MOLECULAR; VIRUS DISEASES;

EID: 33745066404     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2006.00394.x     Document Type: Review

References (185)

1. Ahmed R Gray D. Immunological memory and protective immunity: understanding their relation. Science 1996 272: 54 60.
2. Dutton RW Bradley LM Swain SL. T cell memory. Annu Rev Immunol 1998 16: 201 223.
3. Zinkernagel RM. On differences between immunity and immunological memory. Curr Opin Immunol 2002 14: 523 536.
4. Pewe LL Netland JM Heard SB Perlman S. Very diverse CD8 T cell clonotypic responses after virus infections. J Immunol 2004 172: 3151 3156.
5. Naumov YN Naumova EN Hogan KT Selin LK Gorski J. A fractal clonotype distribution in the CD8+ memory T cell repertoire could optimize potential for immune responses. J Immunol 2003 170: 3994 4001.
6. Falk K Rotzschke O Stevanovic S Jung G Rammensee H. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 1991 351: 290 296.
7. 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.
8. Kjer-Nielsen L, et al. A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 2003 18: 53 64.
9. Rudolph MG Wilson IA. The specificity of TCR/pMHC interaction. Curr Opin Immunol 2002 14: 52 65.
10. Reiser JB, et al. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat Immunol 2003 4: 241 247.
11. Reiser JB, et al. A T cell receptor CDR3beta loop undergoes conformational changes of unprecedented magnitude upon binding to a peptide/MHC class I complex. Immunity 2002 16: 345 354.
12. Burrows SR. Cross-reactive recognition of viral and self-peptides by a 'public' T cell receptor expressed by cytotoxic T lymphocytes expanded in multiple unrelated individuals. Immunol Lett 2004 93: 7 9.
13. Barnett LA Fujinami RS. Molecular mimicry: a mechanism for autoimmune injury. FASEB J 1992 6: 840 844.
14. Boniface J Reich Z Lyons DS Davis MM. Thermodynamics of T cell receptor binding to peptide-MHC: evidence for a general mechanism of molecular scanning. Proc Natl Acad Sci USA 1999 96: 11446 11451.
15. Willcox B, et al. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 1999 10: 357 365.
16. Borg N, et al. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nat Immunol 2005 6: 171 180.
17. Wu L Tuot D Lyons D Garcia K Davis MM. Two-step binding mechanism for T-cell receptor recognition of peptide MHC. Nature 2002 418: 552 556.
18. Daniel C Horvath S Allen PM. A basis for alloreactivity: MHC helical residues broaden peptide recognition by the TCR. Immunity 1998 8: 543 552.
19. Speir JA, et al. Structural basis of 2C TCR allorecognition of H-2Ld peptide complexes. Immunity 1998 8: 553 562.
20. Alam SM Gascoigne NR. Posttranslational regulation of TCR Valpha allelic exclusion during T cell differentiation. J Immunol 1998 160: 3883 3890.
21. Mason D. A very high level of crossreactivity is an essential feature of the T cell repertoire. Immunol Today 1998 19: 395 404.
22. Cabaniols JP Fazilleau N Casrouge A Kourilsky P Kanellopoulos JM. Most alpha/beta T cell receptor diversity is due to terminal deoxynucleotidyl transferase. J Exp Med 2001 194: 1385 1390.
23. Gilfillan S, et al. Efficient immune responses in mice lacking N-region diversity. Eur J Immunol 1995 25: 3115 3122.
24. Gavin MA Bevan MJ. Increased peptide promiscuity provides a rationale for the lack of N regions in the neonatal T cell repertoire. Immunity 1995 3: 793 800.
25. Zarozinski CC Welsh RM. Minimal bystander activation of CD8 T cells during the virus- induced polyclonal T cell response. J Exp Med 1997 185: 1629 1639.
26. Daly K Nguyen P Woodland DL Blackman MA. Immunodominance of major histocompatibility complex class-I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. J Virol 1995 69: 7416 7422.
27. Welsh RM Selin LK Szomolanyi-Tsuda E. Immunological memory to viral infections. Annu Rev Immunol 2004 22: 711 743.
28. Haanen JBAG Wolkers MC Kruisbeek AM Schumacher TNM. Selective expansion of cross-reactive CD8+ memory T cells by viral variants. J Exp Med 1999 190: 1319 1328.
29. Effros RB Doherty PC Gerhard W Bennick JR. Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses. J Exp Med 1977 145: 557 568.
30. Boon AC, et al. Recognition of homo- and heterosubtypic variants of influenza A viruses by human CD8+ T lymphocytes. J Immunol 2004 172: 2453 2460.
31. Mongkolsapaya J, et al. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 2003 9: 921 927.
32. Zivny J, et al. Partial agonist effect influences the CTL response to a heterologous dengue virus serotype. J Immunol 1999 163: 2754 2760.
33. Maeda K Toyosaki-Maeda T Rothman AL Ennis FA. Identification and analysis for cross-reactivity among hantaviruses of the H-2b-restrictied cytotoxic T-lymphocyte epitopes in Sin Nombre virus nucleocapsid protein. J Gen Virol 2004 85: 1909 1919.
34. 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.
35. Spaulding AC Kurane I Ennis FA Rothman AL. 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 73: 398 403.
36. 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: 523 533.
37. 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.
38. Clute SC, et al. Cross-reactive influenza virus-specific CD8 T cells contribute to the lymphoproliferation in Epstein - Barr virus-associated infectious mononucleosis. J Clin Invest 2005 115: 3602 3612.
39. 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.
40. Nilges K, et al. 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 75: 5464 5474.
41. Veiga-Fernandes H Walter U Bourgeois C McLean A Rocha B. Response of naive and memory CD8 T cells to antigen stimulation in vivo. Nat Immunol 2000 1: 47 53.
42. Kaech SM Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2001 2: 415 422.
43. 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.
44. 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.
45. 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.
46. Chen HD Fraire A Joris I Welsh R Selin LK. Specific history of heterologous virus infections determines antiviral immunity and immunopathology in the lung. Am J Pathol 2003 188: 1341 1355.
47. Ostler T Pircher H Ehl S. 'Bystander' recruitment of systemic memory T cells delays the immune response to respiratory virus infection. Eur J Immunol 2003 33: 1839 1848.
48. Brehm MA Markees TG Daniels KA Greiner DL Rossini AA Welsh RM. Direct visualization of cross-reactive effector and memory allo-specific CD8 T cells generated in response to viral infections. J Immunol 2003 170: 4077 4086.
49. Adams AB, et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J Clin Invest 2003 111: 1887 1895.
50. Zhao Z-S Granucci F Yeh L Schaffer PA Cantor H. Molecular mimicry by herpes simplex vrus-type 1: autoimmune disease after viral infection. Science 1998 279: 1344 1347.
51. 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.
52. Yewdell JW Bennink JR. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 1999 17: 51 88.
53. Maryanski JL Attuil V Bucher P Walker PR. A quantitative, single-cell PCR analysis of an antigen-specific TCR repertoire selected during an in vivo CD8 response: direct evidence for a wide range of clone sizes with uniform tissue distribution. Mol Immunol 1999 36: 745 753.
54. Wang XZ Stepp SE Brehm MA Chen HD Selin LK Welsh RM. Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity 2003 18: 631 642.
55. Cohen GB, et al. Clonotype tracking of TCR repertoires during chronic virus infections. Virology 2002 304: 474 484.
56. 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.
57. 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.
58. Camereon TO Cohen GB Islam SA Stern LJ. Examination of the highly diverse CD4 T-cell repertoire directed against an influenza peptide: a step toward TCR proteomics. Immunogenetics 2002 54: 611 620.
59. Bousso P, et al. Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoire. Immunity 1998 9: 169 178.
60. Betts MR, et al. Putative immunodominant human immunodeficiency virus-specific CD8(+) T cell responses cannot be predicted by major histocompatibility complex class I haplotype. J Virol 2000 74: 9144 9151.
61. Koziel MJ Walker BD. Characteristics of the intrahepatic cytotoxic T lymphocyte response in chronic hepatitis C virus infection. Springer Semin Immunopathol 1997 19: 69 83.
62. Hohn H, et al. Longitudinal analysis of Mycobacterium tuberculosis 19-kDa antigen-specific T cells in patients with pulmonary tuberculosis: association with disease activity and cross-reactivity to a peptide from HIVenv gp120. Eur J Immunol 2003 33: 1613 1623.
63. 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: 90 98.
64. Cornberg M, et al. Narrowed T cell receptor repertoire and viral escape as a consequence of heterologous immunity. J Clin Invest 2006 116: ( in press).
65. Dong T, et al. HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J Exp Med 2004 200: 1547 1757.
66. Wilson JDK, et al. Oligoclonal expansions of CD8+ T cells in chronic HIV infection are antigen specific. J Exp Med 1998 188: 785 790.
67. Pantaleo G, et al. Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV. Nature 1994 370: 463 467.
68. Meyer-Olson D, et al. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J Exp Med 2004 200: 307 319.
69. Borrow P, et al. 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 3: 205 211.
70. Welsh RM Kim SK Cornberg M Clute SC Selin LK Naumov YN. The privacy of T cell memory to viruses. Curr Top Microbiol Immunol ( in press).
71. Selin LK Welsh RM. Plasticity of T cell memory responses to viruses. Immunity 2004 20: 5 16.
72. Ploegh HL. Viral strategies of immune evasion. Science 1998 280: 248 253.
73. Doherty PC Zinkernagel RM. T-cell-mediated immunopathology in viral infections. Transplant Rev 1974 19: 89 120.
74. Cole GA Nathanson N Prendergast RA. Requirement for θ-bearing cells in lymphocytic choriomeningitis virus-induced central nervous system disease. Nature 1972 238: 335 337.
75. 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.
76. 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.
77. 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.
78. 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.
79. 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.
80. Smoller BR Weishar M Gray MH. An unusual cutaneous manifestation in Crohn's disease. Arch Pathol Lab Med 1990 6: 609 610.
81. Requena L Requena C. Erythema nodosum. Dermatol Online 2002 8: 4.
82. 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.
83. Nettesheim P Szakal AK. Morphogenesis of alveolar bronchiolization. Lab Invest 1972 26: 210 219.
84. de St. Groth SF Webster RG. Disquisitions on original antigenic sin. II. Proof in lower creatures. J Exp Med 1966 124: 347 361.
85. Welsh RM Rothman AL. Dengue immune response: low affinity, high febrility. Nat Med 2003 9: 820 822.
86. Silins SL, et al. Asymptomatic primary Epstein - Barr virus infection occurs in the absence of blood T-cell repertoire perturbations despite high levels of systemic virus load. Blood 2001 98: 3739 3744.
87. Rickinson AB Kieff E. Epstein - Barr virus. In: Fields BN, et al., eds. Virology, Vol. 2. Philadelphia: Lippincott-Raven Publishers, 1996:2397 2446.
88. Lawson TM, et al. Functional differences between influenza A-specific cytotoxic T lymphocyte clones expressing dominant and subdominant TCR. Int Immunol 2001 13: 1383 1390.
89. Farci P, et al. Hepatitis C virus-associated fulminant hepatic failure. N Engl J Med 1996 335: 631 634.
90. Urbani S, et al. Heterologous T cell immunity in severe hepatitis C virus infection. J Exp Med 2005 201: 675 680.
91. Rehermann B Shin EC. Private aspects of heterologous immunity. J Exp Med 2005 201: 667 670.
92. 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.
93. Douglass JA O'Hehir RE. What determines asthma phenotype? Respiratory infections and asthma. Am J Respir Crit Care Med 2000 161: S211 S214.
94. Yang H Welsh RM. Induction of alloreactive cytotoxic T cells by acute virus infection of mice. J Immunol 1986 136: 1186 1193.
95. Yang H Dundon PL Nahill SR Welsh RM. Virus-induced polyclonal cytotoxic T lymphocyte stimulation. J Immunol 1989 142: 1710 1718.
96. Williams MA, et al. Characterization of virus-mediated inhibition of mixed chimerism and allospecific tolerance. J Immunol 2001 167: 4987 4995.
97. Welsh RM, et al. Virus-induced abrogation of transplantation tolerance induced by donor-specific transfusion and anti-CD154 antibody. J Virol 2000 74: 2210 2218.
98. Williams MA, et al. Cutting edge: persistent viral infection prevents tolerance induction and escapes immune control following CD28/CD40 blockade-based regimen. J Immunol 169: 5387 5391.
99. Nahill SR Welsh RM. High frequency of cross-reactive cytotoxic T lymphocytes elicited during the virus-induced polyclonal cytotoxic T lymphocyte response. J Exp Med 1993 177: 317 327.
100. Burrows SR Khanna R Burrows JM Moss DJ. An alloresponse in humans is dominated by cytotoxic T lymphocytes (CTL) cross-reactive with a single Epstein - Barr Virus CTL epitope: implications for graft-versus-host disease. J Exp Med 1994 179: 1155 1161.
101. Braciale TJ Andrew ME Braciale VL. Simultaneous expression of H-2 restricted and alloreactive recognition by a cloned line of influenza virus-specific cytotoxic T lymphocytes. J Exp Med 1981 153: 1371 1376.
102. Jennings SR. Cross-reactive recognition of mouse cells expressing the bm3 and bm11 mutations within H-2Kb by H-2Kb-restricted herpes simplex virus-specific cytotoxic T lymphocytes. J Immunol 1985 135: 3530 3536.
103. Sheil JM Bevan MJ Lefrancois L. Characterization of dual-reactive H-2Kb-restricted anti- vesicular stomatitus virus and alloreactive cytotoxic T cells. J Immunol 1987 138: 3654 3660.
104. Gamadia LE, et al. Cross-reactivity of cytomegalovirus-specific CD8+ T cells to allo-major histocompatibility complex class I molecules. Transplantation 2004 77: 1879 1885.
105. Heeger PS, et al. Pretransplant frequency of donor-specific, IFN-gamma-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J Immunol 1999 163: 2267 2275.
106. Suchin EJ Langmuir PB Palmer E Sayegh MH Wells AD Turka LA. Quantifying the frequency of alloreactive T cells in vivo: new answers to an old question. J Immunol 2001 166: 973 981.
107. Lindahl KF Wilson DB. Histocompatibility antigen-activated cytotoxic T lymphocytes. II. Estimates of the frequency and specificity of precursors. J Exp Med 1977 145: 508 522.
108. Ford WL Simmonds SJ Atkikn RC. Early cellular events in a systemic graft-vs.-host reaction. II. Autoradiographic estimates of donor lymphocytes which response to Ag-B-determined antigenic complexes. J Exp Med 1975 141: 681 696.
109. Heeger PS. T-cell allorecognition and transplant rejection: a summary and update. Am J Transplant 2003 3: 525 533.
110. Bendjelloul F Desin TS Shoker AS. Donor non-specific IFN-gamma production by primed alloreactive cells as a potential screening test to predict the alloimmune response. Transpl Immunol 2004 12: 167 176.
111. Nickel P, et al. Enzyme-linked immunosorbent spot assay for donor-reactive interferon-gamma-producing cells identifies T-cell presensitization and correlates with graft function at 6 and 12 months in renal-transplant recipients. Transplantation 2004 78: 1640 1646.
112. Sester U, et al. Rapid identification of preformed alloreactive T cells for use in a clinical setting. Transplantation 2004 78: 607 614.
113. Brehm MA Daniels KA Welsh RM. Rapid production of TNF-α following TCR-engagement of naïve CD8 T cells. J Immunol 2005 175: 5043 5049.
114. Tomkinson BE Maziarz R Sullivan JL. Characterization of the T cell-mediated cellular cytotoxicity during infectious mononucleosis. J Immunol 1989 143: 660 670.
115. Strang G Rickinson AB. Multiple HLA class I-dependent cytotoxicities constitute the 'non-HLA-restricted' response in infectious mononucleosis. Eur J Immunol 1987 17: 1007 1013.
116. Brehm MA Daniels KA Ortaldo JA Welsh RM. Rapid conversion of effector mechanisms from NK to T cells during virus-induced lysis of allogeneic implants in vivo. J Immunol 2005 174: 6663 6671.
117. Oberg L, et al. Loss or mismatch of MHC class I is sufficient to trigger NK cell-mediated rejection of resting lymphocytes in vivo - role of KARAP/DAP12-dependent and - independent pathways. Eur J Immunol 2004 34: 1646 1653.
118. Chen G Dong JH. Individualized immunosuppression: new strategies from pharmacokinetics, pharmacodynamics and pharmacogenomics. Hepatobiliary Pancreat Dis Int 2005 4: 332 338.
119. Odorico JS Sollinger HW. Technical and immunosuppressive advances in transplantation for insulin-dependent diabetes mellitus. World J Surg 2002 26: 194 211.
120. Shapiro R Young JB Milford EL Trotter JF Bustami RT Leichtman AB. Immunosuppression: evolution in practice and trends, 1993-2003. Am J Transplant 2005 5: 874 886.
121. Kenyon NS, et al. Long-term survival and function of intrahepatic islet allografts in baboons treated with humanized anti-CD154. Diabetes 1999 48: 1473 1481.
122. Kirk AD, et al. CTLA4-Ig and anti-CD40 ligand prevent renal allograft rejection in primates. Proc Natl Acad Sci USA 1997 94: 8789 8794.
123. Larsen CP, et al. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 1996 381: 434 438.
124. Markees TG, et al. Prolonged survival of skin allografts in recipients treated with donor splenocytes and antibody to CD40 ligand. Transplantation 1997 64: 329 335.
125. Parker DC, et al. Survival of mouse pancreatic islet allografts in recipients treated with allogeneic small lymphocytes and antibody to CD40 ligand. Proc Natl Acad Sci USA 1995 92: 9560 9564.
126. Hancock WW Sayegh MH Zheng XG Peach R Linsley PS Turka LA. Costimulatory function and expression of CD40 ligand, CD80, and CD86 in vascularized murine cardiac allograft rejection. Proc Natl Acad Sci USA 1996 93: 13967 13972.
127. Thornley TB, et al. Toll-like receptor agonists abrogate costimulation blockade-induced transplantation tolerance. J Immunol 2006 176: 1561 1570.
128. Chen Y Heeger PS Valujskikh A. In vivo helper functions of alloreactive memory CD4+ T cells remain intact despite donor-specific transfusion and anti-CD40 ligand therapy. J Immunol 2004 172: 5456 5466.
129. Zhai Y Meng L Gao F Busuttil RW Kupiec-Weglinski JW. Allograft rejection by primed/memory CD8 (+) T cells is CD154 blockade resistant: therapeutic implications for sensitized transplant recipients. J Immunol 2002 169: 4667 4673.
130. Pantenburg B Heinzel F Das L Heeger PS Valujskikh A. T cells primed by Leishmania major infection cross-react with alloantigens and alter the course of allograft rejection. J Immunol 2002 169: 3686 3693.
131. Budd RC, et al. Distinction of virgin and memory T lymphocytes. Stable acquisition of the Pgp-1 glycoprotein concomitant with antigenic stimulation. J Immunol 1987 138: 3120 3129.
132. Kieper WC Jameson SC. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc Natl Acad Sci USA 1999 96: 13306 13311.
133. Bendelac A Rivera MN Park SH Roark JH. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu Rev Immunol 1997 15: 535 562.
134. McMahon CW, et al. Viral and bacterial infections induce expression of multiple NK cell receptors in responding CD8(+) T cells. J Immunol 2002 169: 1444 1452.
135. Peacock CD Welsh RM. Origin and fate of lymphocytic choriomeningitis virus-specific CD8+ T cells coexpressing the inhibitory NK cell receptor Ly49G2. J Immunol 2004 173: 478 484.
136. 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.
137. 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.
138. 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.
139. Prlic M Lefrancois L Jameson SC. Multiple choices. regulation of memory CD8 T cell generation and homeostasis by interleukin (IL) -7 and IL-15. J Exp Med 2002 195: F49 F52.
140. Tan JT Ernst B Kieper WC LeRoy E Sprent J Surh CD. 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 2002 195: 1523 1532.
141. Kieper WC, et al. Overexpression of interleukin (IL) -7 leads to IL-15-independent generation of memory phenotype CD8+ T cells. J Exp Med 2002 195: 1533 1539.
142. 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.
143. Lau LL Jamieson BD Somasundaram T Ahmed R. Cytotoxic T-cell memory without antigen. Nature 1994 369: 648 652.
144. Homann D Teyton L Oldstone MB. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ memory. Nat Med 2001 7: 892 893.
145. Varga SM Welsh RM. High frequency of virus-specific interleukin-2- producing CD4+ T cells and Th1 dominance during lymphocytic choriomeningitis virus infection. J Virol 2000 74: 4429 4432.
146. Swain SL Hu H Huston G. Class II-independent generation of CD4 memory T cells from effectors. Science 1999 286: 1381 1383.
147. Varga SM Welsh RM. Stability of virus-specific CD4+ T cell frequencies from acute infection into long term memory. J Immunol 1998 161: 367 374.
148. Varga SM Selin LK Welsh RM. Independent regulation of lymphocytic choriomeningitis virus-specific T cell memory pools: relative stability of CD4 memory under conditions of CD8 memory T cell loss. J Immunol 2001 166: 1554 1561.
149. Murali-Krishna K Lau LL Sambhara S Lemonnier F Altman J Ahmed R. Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 1999 286: 1377 1381.
150. Bourgeois C Rocha B Tanchot C. A role for CD40 expression on CD8+ T cells in the generation of CD8+ T cell memory. Science 2002 297: 2060 2063.
151. Sun JC Bevan MJ. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 2003 300: 339 342.
152. Janssen EM Lemmens EE Wolfe T Christen U von Herrath MG Schoenberger SP. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 2003 421: 852 856.
153. Demkowicz WE Littaua RA Wang J Ennis FA. Human cytotoxic T-cell memory: long-lived responses to vaccinia virus. J Virol 1996 70: 2627 2631.
154. Crotty S Felgner P Davies H Glidewell J Villarreal L Ahmed R. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol 2003 171: 4969 4973.
155. Hammarlund E, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med 2003 9: 1131 1137.
156. 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: 3139 3150.
157. Selin LK, et al. 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.
158. Jiang J Lau L Shen H. Selective depletion of nonspecific T cells during the early stage of immune responses to infection. J Immunol 2003 171: 4352 4358.
159. 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.
160. Wong R, et al. Haematological manifestations in patients with severe acute respiratory syndrome: retrospective analysis. BMJ 2003 326: 1358 1362.
161. Nabeshima S Murata M Kikuchi K Ikematsu H Kashiwagi S Hayashi J. A reduction in the number of peripheral CD28+CD8+T cells in the acute phase of influenza. Clin Exp Immunol 2002 128: 339 346.
162. Razvi ES Jiang Z Woda BA Welsh RM. 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 147: 79 91.
163. Masopust D Vezys V Marzo AL Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001 291: 2413 2417.
164. Hogan RJ, et al. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J Immunol 2001 166: 1813 1822.
165. Marshall DR, et al. Measuring the diaspora for virus-specific CD8+ T cells. Proc Natl Acad Sci USA 2001 98: 6313 6318.
166. Welsh RM Bahl K Wang XZ. Apoptosis and loss of virus-specific CD8(+) T-cell memory. Curr Opin Immunol 2004 16: 271 276.
167. 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: 1820 1826.
168. Bahl K, et al. Interferon-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: 4284 4295.
169. Rathmell JC Thompson CB. Pathways of apoptosis in lymphocyte development, homeostasis, and disease. Cell 2002 109: S97 S107.
170. Selin LK, et al. CD8 memory T cells: cross-reactivity and heterologous immunity. Semin Immunol 2004 16: 335 347.
171. Hahm B Trifilo MJ Zuniga EI Oldstone MB. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 2005 22: 247 257.
172. Gil MP Salomon R Louten J Biron CA. Modulation of STAT1 protein levels: a mechanism shaping CD8 t cell responses in vivo. Blood 2006 107: 987 993.
173. Zhang X Sun S Hwang I Tough DF Sprent J. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 1998 8: 591 599.
174. Razvi ES Welsh RM. Programmed cell death of T lymphocytes during acute viral infection: a mechanism for virus-induced immune deficiency. J Virol 1993 67: 5754 5765.
175. Wang XZ Brehm MA Welsh RM. Preapoptotic phenotype of viral epitope-specific CD8 T cells precludes memory development and is an intrinsic property of the epitope. J Immunol 2004 173: 5138 5147.
176. Kaech SM Tan JT Wherry EJ Konieczny BT Surh CD Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 2003 4: 1191 1198.
177. Ray SJ, et al. The collagen binding alpa1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity 2004 20: 167 179.
178. Ayroldi E Cannarile L Migliorati G Bartoli A Nicoletti I Riccardi C. CD44 (Pgp-1) inhibits CD3 and dexamethasone-induced apoptosis. Blood 1995 86: 2672 2678.
179. Grayson JM Laniewski NG Lanier JG Ahmed R. Mitochondrial potential and reactive oxygen intermediates in antigen-specific CD8+ T cells during viral infection. J Immunol 2003 170: 4745 4751.
180. Lauer GM, et al. Full-breadth analysis of CD8+ T-cell responses in acute hepatitis C virus infection and early therapy. J Virol 2005 79: 12979 12988.
181. Zhou S Ou R Huang L Moskophidis D. 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 2002 76: 829 840.
182. Selin LK Nahill SR Welsh RM. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J Exp Med 1994 179: 1933 1943.
183. Peacock C Kim S Welsh RM. Attrition of virus-specific memory CD8(+) T cells during reconstitution of lymphopenic environments. J Immunol 2003 171: 655 663.
184. Kieper WC Burghardt JT Surh CD. A role for TCR affinity in regulating naive T cell homeostasis. J Immunol 2004 172: 40 44.
185. Fremont DH Stura EA Matsumura M Peterson PA Wilson IA. Crystal structure of an H-2Kb-ovalbumin peptide complex reveals the interplay of primary and secondary anchor positions in the major histocompatibility complex binding groove. Proc Natl Acad Sci USA 1995 92: 2479 2483.