Antiviral memory phenotype T cells in unexposed adults

Immunological Reviews

Volumn 255, Issue 1, 2013, Pages 95-109

  Su, Laura F ^a   Davis, Mark M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antigens; Memory; Repertoire development; T cells; T cell receptors; Viral

Indexed keywords

ANTIVIRUS AGENT; BCG VACCINE; CD4 ANTIGEN; CD8 ANTIGEN; CYTOCHROME C; DEATH RECEPTOR; DIPHTHERIA PERTUSSIS TETANUS VACCINE; GAMMA INTERFERON; INFLUENZA VACCINE; INTERLEUKIN 2; INTERLEUKIN 7; MEASLES VACCINE; OREXIN; S6 KINASE; SMALLPOX VACCINE; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CROSS REACTION; DENGUE; ENVIRONMENTAL FACTOR; HEPATITIS B VIRUS; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; MEASLES; MEASLES VACCINATION; MEMORY T LYMPHOCYTE; MICROBIOME; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVACCINATION; SIGNAL TRANSDUCTION; SMALLPOX; THYMUS;

ANTIGENS; MEMORY; REPERTOIRE DEVELOPMENT; T CELLS; T-CELL RECEPTORS; VIRAL;

ADULT; ANIMALS; ANTIGENS, VIRAL; HUMANS; IMMUNOLOGIC MEMORY; RECEPTORS, ANTIGEN, T-CELL; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; VIRUS DISEASES; VIRUSES;

EID: 84881656591     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12095     Document Type: Article

References (120)

1. Davis MM, Bjorkman PJ. T-cell antigen receptor genes and T-cell recognition. Nature 1988;334:395-402.
2. Moran AE, Hogquist KA. T-cell receptor affinity in thymic development. Immunology 2012;135:261-267.
3. Morris GP, Allen PM. How the TCR balances sensitivity and specificity for the recognition of self and pathogens. Nat Immunol 2012;13:121-128.
4. Moon JJ, et al. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 2007;27:203-213.
5. Obar JJ, Khanna KM, Lefrancois L. Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity 2008;28:859-869.
6. Kwok WW, et al. Frequency of epitope-specific naive CD4(+) T cells correlates with immunodominance in the human memory repertoire. J Immunol 2012;188:2537-2544.
7. Schmidt J, et al. Immunodominance of HLA-A2-restricted hepatitis C virus-specific CD8+ T cell responses is linked to naive-precursor frequency. J Virol 2011;85:5232-5236.
8. Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol Today 1998;19:395-404.
9. Reay PA, Kantor RM, Davis MM. Use of global amino acid replacements to define the requirements for MHC binding and T cell recognition of moth cytochrome c (93-103). J Immunol 1994;152:3946-3957.
10. Crawford F, Huseby E, White J, Marrack P, Kappler JW. Mimotopes for alloreactive and conventional T cells in a peptide-MHC display library. PLoS Biol 2004;2:E90.
11. Adams JJ, et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 2011;35:681-693.
12. Lackritz EM, et al. Estimated risk of transmission of the human immunodeficiency virus by screened blood in the United States. N Engl J Med 1995;333:1721-1725.
13. Janeway CA, Paul WE. The specificity of cellular immune responses in guinea pigs. III. The precision of antigen recognition by T lymphocytes. J Exp Med 1976;144:1641-1656.
14. Bhardwaj V, Kumar V, Geysen HM, Sercarz EE. Degenerate recognition of a dissimilar antigenic peptide by myelin basic protein-reactive T cells. Implications for thymic education and autoimmunity. J Immunol 1993;151:5000-5010.
15. Evavold BD, Sloan-Lancaster J, Wilson KJ, Rothbard JB, Allen PM. Specific T cell recognition of minimally homologous peptides: evidence for multiple endogenous ligands. Immunity 1995;2:655-663.
16. Wucherpfennig KW, Strominger JL. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell 1995;80:695-705.
17. Garcia KC, et al. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 1996;274:209-219.
18. Garboczi DN, Ghosh P, Utz U, Fan QR, Biddison WE, Wiley DC. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 1996;384:134-141.
19. Garcia KC, et al. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 1998;279:1166-1172.
20. Ding YH, 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.
21. Newell EW, et al. Structural basis of specificity and cross-reactivity in T cell receptors specific for cytochrome c-I-E(k). J Immunol 2011;186:5823-5832.
22. Reinherz EL, et al. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 1999;286:1913-1921.
23. Reiser JB, et al. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nat Immunol 2003;4:241-247.
24. Baker BM, Scott DR, Blevins SJ, Hawse WF. Structural and dynamic control of T-cell receptor specificity, cross-reactivity, and binding mechanism. Immunol Rev 2012;250:10-31.
25. Wucherpfennig KW, et al. Polyspecificity of T cell and B cell receptor recognition. Semin Immunol 2007;19:216-224.
26. Yin Y, Li Y, Mariuzza RA. Structural basis for self-recognition by autoimmune T-cell receptors. Immunol Rev 2012;250:32-48.
27. Sethi DK, et al. A highly tilted binding mode by a self-reactive T cell receptor results in altered engagement of peptide and MHC. J Exp Med 2011;208:91-102.
28. Hahn M, Nicholson MJ, Pyrdol J, Wucherpfennig KW. Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor. Nat Immunol 2005;6:490-496.
29. Li Y, Huang Y, Lue J, Quandt JA, Martin R, Mariuzza RA. Structure of a human autoimmune TCR bound to a myelin basic protein self-peptide and a multiple sclerosis-associated MHC class II molecule. EMBO J 2005;24:2968-2979.
30. Paul S, Schaefer BC. A new look at T cell receptor signaling to nuclear factor-kappaB. Trends Immunol 2013;34:269-281.
31. Zehn D, King C, Bevan MJ, Palmer E. TCR signaling requirements for activating T cells and for generating memory. Cell Mol Life Sci 2012;69:1565-1575.
32. Zhu J, Paul WE. Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol Rev 2010;238:247-262.
33. Sallusto F, Lanzavecchia A. Heterogeneity of CD4+ memory T cells: functional modules for tailored immunity. Eur J Immunol 2009;39:2076-2082.
34. McKinstry KK, Strutt TM, Swain SL. Regulation of CD4+ T-cell contraction during pathogen challenge. Immunol Rev 2010;236:110-124.
35. Jameson SC, Masopust D. Diversity in T cell memory: an embarrassment of riches. Immunity 2009;31:859-871.
36. Harrington LE, Janowski KM, Oliver JR, Zajac AJ, Weaver CT. Memory CD4 T cells emerge from effector T-cell progenitors. Nature 2008;452:356-360.
37. McKinstry KK, Golech S, Lee WH, Huston G, Weng NP, Swain SL. Rapid default transition of CD4 T cell effectors to functional memory cells. J Exp Med 2007;204:2199-2211.
38. Bannard O, Kraman M, Fearon DT. Secondary replicative function of CD8+ T cells that had developed an effector phenotype. Science 2009;323:505-509.
39. Maris CH, Miller JD, Altman JD, Jacob J. A transgenic mouse model genetically tags all activated CD8 T cells. J Immunol 2003;171:2393-2401.
40. Chang JT, et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 2007;315:1687-1691.
41. Sprent J, Surh CD. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat Immunol 2011;12:478-484.
42. Haluszczak C, et al. The antigen-specific CD8+ T cell repertoire in unimmunized mice includes memory phenotype cells bearing markers of homeostatic expansion. J Exp Med 2009;206:435-448.
43. Akue AD, Lee JY, Jameson SC. Derivation and maintenance of virtual memory CD8 T cells. J Immunol 2012;188:2516-2523.
44. Decman V, et al. Defective CD8 T cell responses in aged mice are due to quantitative and qualitative changes in virus-specific precursors. J Immunol 2012;188:1933-1941.
45. Rudd BD, et al. Nonrandom attrition of the naive CD8+ T-cell pool with aging governed by T-cell receptor:pMHC interactions. Proc Natl Acad Sci USA 2011;108:13694-13699.
46. Min B, Foucras G, Meier-Schellersheim M, Paul WE. Spontaneous proliferation, a response of naive CD4 T cells determined by the diversity of the memory cell repertoire. Proc Natl Acad Sci USA 2004;101:3874-3879.
47. Cho JH, Kim HO, Surh CD, Sprent J. T cell receptor-dependent regulation of lipid rafts controls naive CD8+ T cell homeostasis. Immunity 2010;32:214-226.
48. Guimond M, et al. Interleukin 7 signaling in dendritic cells regulates the homeostatic proliferation and niche size of CD4+ T cells. Nat Immunol 2009;10:149-157.
49. Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, Doherty PC. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 1998;8:683-691.
50. Casanova JL, Abel L. Inborn errors of immunity to infection: the rule rather than the exception. J Exp Med 2005;202:197-201.
51. Moore SE, Cole TJ, Collinson AC, Poskitt EM, McGregor IA, Prentice AM. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int J Epidemiol 1999;28:1088-1095.
52. Dubos RJ, Schaedler RW. Effects of cellular constituents of mycobacteria on the resistance of mice to heterologous infections I. Protective effects. J Exp Med 1957;106:703-717.
53. Howard JG, Biozzi G, Halpern BN, Stiffel C, Mouton D. The effect of Mycobacterium tuberculosis (BCG) infection on the resistance of mice to bacterial endotoxin and Salmonella enteritidis infection. Br J Exp Pathol 1959;40:281-290.
54. Yang HY, Dundon PL, Nahill SR, Welsh RM. Virus-induced polyclonal cytotoxic T lymphocyte stimulation. J Immunol 1989;142:1710-1718.
55. Selin LK, Nahill SR, Welsh RM. Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J Exp Med 1994;179:1933-1943.
56. 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.
57. 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.
58. Chen HD, Fraire AE, Joris I, Welsh RM, Selin LK. Specific history of heterologous virus infections determines anti-viral immunity and immunopathology in the lung. Am J Pathol 2003;163:1341-1355.
59. Smith KA. Edward jenner and the small pox vaccine. Front Immunol 2011;2:21.
60. Kristensen I, Aaby P, Jensen H. Routine vaccinations and child survival: follow up study in Guinea-Bissau, West Africa. BMJ 2000;321:1435-1438.
61. Veirum JE, et al. Routine vaccinations associated with divergent effects on female and male mortality at the paediatric ward in Bissau, Guinea-Bissau. Vaccine 2005;23:1197-1204.
62. Aaby P, et al. Non-specific effects of standard measles vaccine at 4.5 and 9 months of age on childhood mortality: randomised controlled trial. BMJ 2010;341:c6495.
63. Shann F, Nohynek H, Scott JA, Hesseling A, Flanagan KL. Randomized trials to study the nonspecific effects of vaccines in children in low-income countries. Pediatr Infect Dis J 2010;29:457-461.
64. Aaby P, et al. Vaccinia scars associated with better survival for adults. An observational study from Guinea-Bissau. Vaccine 2006;24:5718-5725.
65. Jensen ML, et al. Vaccinia scars associated with improved survival among adults in rural Guinea-Bissau. PLoS ONE 2006;1:e101.
66. Sorup S, et al. Smallpox vaccination and all-cause infectious disease hospitalization: a Danish register-based cohort study. Int J Epidemiol 2011;40:955-963.
67. Aronson JD. Protective vaccination against tuberculosis with special reference to BCG vaccination. Am Rev Tuberc 1948;58:255-281.
68. Garly ML, et al. BCG scar and positive tuberculin reaction associated with reduced child mortality in West Africa. A non-specific beneficial effect of BCG? Vaccine 2003;21:2782-2790.
69. Roth A, et al. Tuberculin reaction, BCG scar, and lower female mortality. Epidemiology 2006;17:562-568.
70. Roth AE, et al. Effect of revaccination with BCG in early childhood on mortality: randomised trial in Guinea-Bissau. BMJ 2010;340:c671.
71. Aaby P, et al. Long-term survival after Edmonston-Zagreb measles vaccination in Guinea-Bissau: increased female mortality rate. J Pediatr 1993;122:904-908.
72. Aaby P, et al. Sex-specific differences in mortality after high-titre measles immunization in rural Senegal. Bull World Health Organ 1994;72:761-770.
73. Holt VL, Marcuse EK, Coombs J. Pediatricians' immunization consent practices in Washington state. Am J Dis Child 1987;141:734-735.
74. Expanded programme on immunization (EPI). Safety of high titre measles vaccines. Wkly Epidemiol Rec 1992;67:357-361.
75. Aaby P, et al. Differences in female-male mortality after high-titre measles vaccine and association with subsequent vaccination with diphtheria-tetanus-pertussis and inactivated poliovirus: reanalysis of West African studies. Lancet 2003;361:2183-2188.
76. Aaby P, et al. DTP with or after measles vaccination is associated with increased in-hospital mortality in Guinea-Bissau. Vaccine 2007;25:1265-1269.
77. Biai S, Rodrigues A, Nielsen J, Sodemann M, Aaby P. Vaccination status and sequence of vaccinations as risk factors for hospitalisation among outpatients in a high mortality country. Vaccine 2011;29:3662-3669.
78. Aaby P, Ibrahim SA, Libman MD, Jensen H. The sequence of vaccinations and increased female mortality after high-titre measles vaccine: trials from rural Sudan and Kinshasa. Vaccine 2006;24:2764-2771.
79. Aaby P, Jensen H, Walraven G. Age-specific changes in the female-male mortality ratio related to the pattern of vaccinations: an observational study from rural Gambia. Vaccine 2006;24:4701-4708.
80. Rothman AL. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 2011;11:532-543.
81. Friberg H, et al. Memory CD8+ T cells from naturally acquired primary dengue virus infection are highly cross-reactive. Immunol Cell Biol 2011;89:122-129.
82. Imrie A, et al. Differential functional avidity of dengue virus-specific T-cell clones for variant peptides representing heterologous and previously encountered serotypes. J Virol 2007;81:10081-10091.
83. Goulder PJ, Watkins DI. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol 2008;8:619-630.
84. Deeks SG, Walker BD. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 2007;27:406-416.
85. Kosmrlj A, et al. Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 2010;465:350-354.
86. Chen H, et al. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat Immunol 2012;13:691-700.
87. Fujinami RS, Oldstone MB. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 1985;230:1043-1045.
88. Cusick MF, Libbey JE, Fujinami RS. Molecular mimicry as a mechanism of autoimmune disease. Clin Rev Allergy Immunol 2012;42:102-111.
89. Munz C, Lunemann JD, Getts MT, Miller SD. Antiviral immune responses: triggers of or triggered by autoimmunity? Nat Rev Immunol 2009;9:246-258.
90. Ray CG, Palmer JP, Crossley JR, Williams RH. Coxsackie B virus antibody responses in juvenile-onset diabetes mellitus. Clin Endocrinol 1980;12:375-378.
91. Rose NR, Wolfgram LJ, Herskowitz A, Beisel KW. Postinfectious autoimmunity: two distinct phases of coxsackievirus B3-induced myocarditis. Ann NY Acad Sci 1986;475:146-156.
92. Gross DM, et al. Identification of LFA-1 as a candidate autoantigen in treatment-resistant Lyme arthritis. Science 1998;281:703-706.
93. Trollmo C, Meyer AL, Steere AC, Hafler DA, Huber BT. Molecular mimicry in Lyme arthritis demonstrated at the single cell level: LFA-1 alpha L is a partial agonist for outer surface protein A-reactive T cells. J Immunol 2001;166:5286-5291.
94. Honeyman MC, Stone NL, Falk BA, Nepom G, Harrison LC. Evidence for molecular mimicry between human T cell epitopes in rotavirus and pancreatic islet autoantigens. J Immunol 2010;184:2204-2210.
95. Wijnans L, et al. The incidence of narcolepsy in Europe: before, during, and after the influenza A(H1N1)pdm09 pandemic and vaccination campaigns. Vaccine 2013;31:1246-1254.
96. Kornum BR, Faraco J, Mignot E. Narcolepsy with hypocretin/orexin deficiency, infections and autoimmunity of the brain. Curr Opin Neurobiol 2011;21:897-903.
97. Fozza C, et al. T-cell receptor repertoire analysis in monozygotic twins concordant and discordant for type 1 diabetes. Immunobiology 2012;217:920-925.
98. Gulwani-Akolkar B, Shi B, Akolkar PN, Ito K, Bias WB, Silver J. Do HLA genes play a prominent role in determining T cell receptor V alpha segment usage in humans? J Immunol 1995;154:3843-3851.
99. 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.
100. Su LF, Kidd BA, Han A, Kotzin JJ, Davis MM. Virus-Specific CD4(+) Memory-Phenotype T Cells Are Abundant in Unexposed Adults. Immunity 2013;38:373-383.
101. Willer CJ, Dyment DA, Risch NJ, Sadovnick AD, Ebers GC. Twin concordance and sibling recurrence rates in multiple sclerosis. Proc Natl Acad Sci USA 2003;100:12877-12882.
102. Mathew A, Rothman AL. Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol Rev 2008;225:300-313.
103. Taylor G, Walker J. Charles Harrison Blackley, 1820-1900. Clin Allergy 1973;3:103-108.
104. Leibowitz U, Antonovsky A, Medalie JM, Smith HA, Halpern L, Alter M. Epidemiological study of multiple sclerosis in Israel. II. Multiple sclerosis and level of sanitation. J Neurol Neurosurg Psychiatry 1966;29:60-68.
105. Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299:1259-1260.
106. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 2009;326:1694-1697.
107. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004;303:1662-1665.
108. Hand TW, et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 2012;337:1553-1556.
109. Ivanov II, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008;4:337-349.
110. Ivanov II, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009;139:485-498.
111. Gaboriau-Routhiau V, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009;31:677-689.
112. Wu HJ, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010;32:815-827.
113. Atarashi K, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011;331:337-341.
114. Round JL, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011;332:974-977.
115. Consortium THMP. Structure, function and diversity of the healthy human microbiome. Nature 2012;486:207-214.
116. Yatsunenko T, et al. Human gut microbiome viewed across age and geography. Nature 2012;486:222-227.
117. Wu GD, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105-108.
118. Devkota S, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 2012;487:104-108.
119. Newell EW, Sigal N, Nair N, Kidd BA, Greenberg HB, Davis MM. Combinatorial tetramer staining and mass cytometry analysis facilitate T-cell epitope mapping and characterization. Nat Biotechnol 2013;31:623-629.
120. Moore SE, et al. Season of birth predicts mortality in rural Gambia. Nature 1997;388:434.