Effective T helper cell responses against retroviruses: Are all clonotypes equal?

Journal of Leukocyte Biology

Volumn 96, Issue 1, 2014, Pages 27-37

  Thorborn, Georgina ^a   Young, George R ^a   Kassiotis, George ^a,b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

CD4; Cell; Immunological memory; TCR avidity; TCR diversity

Indexed keywords

EPITOPE; NEUTRALIZING ANTIBODY; T LYMPHOCYTE RECEPTOR;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; B LYMPHOCYTE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL MATURATION; ENVELOPE GENE; GENETIC ASSOCIATION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; MITOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION; VACCINATION;

CD4 T CELL; IMMUNOLOGICAL MEMORY; TCR AVIDITY; TCR DIVERSITY;

AIDS VACCINES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; HIV INFECTIONS; HIV-1; HUMANS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, HELPER-INDUCER; VACCINATION;

EID: 84903548103     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.2RI0613-347R     Document Type: Review

References (127)

1. Baudino, L., Yoshinobu, K., Morito, N., Santiago-Raber, M. L., Izui, S. (2010) Role of endogenous retroviruses in murine SLE. Autoimmun. Rev. 10, 27-34.
2. Hancks, D. C., Kazazian, H. H., Jr., (2012) Active human retrotransposons: variation and disease. Curr. Opin. Genet. Dev. 22, 191-203.
3. Stoye, J. P. (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat. Rev. Microbiol. 10, 395-406.
4. Young, G. R., Eksmond, U., Salcedo, R., Alexopoulou, L., Stoye, J. P., Kassiotis, G. (2012) Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 491, 774-778.
5. Daugherty, M. D., Malik, H. S. (2012) Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46, 677-700.
6. Yap, M. W., Nisole, S., Stoye, J. P. (2005) A single amino acid change in the SPRY domain of human Trim5α leads to HIV-1 restriction. Curr. Biol. 15, 73-78.
7. Kaiser, S. M., Malik, H. S., Emerman, M. (2007) Restriction of an extinct retrovirus by the human TRIM5α antiviral protein. Science 316, 1756-1758.
8. Nisole, S., Stoye, J. P., Saib, A. (2005) TRIM family proteins: retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 3, 799-808.
9. Barbalat, R., Ewald, S. E., Mouchess, M. L., Barton, G. M. (2011) Nucleic acid recognition by the innate immune system. Annu. Rev. Immunol. 29, 185-214.
10. Kane, M., Case, L. K., Wang, C., Yurkovetskiy, L., Dikiy, S., Golovkina, T. V. (2011) Innate immune sensing of retroviral infection via Toll-like receptor 7 occurs upon viral entry. Immunity 35, 135-145.
11. Yoshinobu, K., Baudino, L., Santiago-Raber, M. L., Morito, N., Dunand-Sauthier, I., Morley, B. J., Evans, L. H., Izui, S. (2009) Selective up-regulation of intact, but not defective env RNAs of endogenous modified polytropic retrovirus by the Sgp3 locus of lupus-prone mice. J. Immunol. 182, 8094-8103.
12. Chen, Y. Z., Matsushita, S., Nishimura, Y. (1996) Response of a human T cell clone to a large panel of altered peptide ligands carrying single residue substitutions in an antigenic peptide: characterization and frequencies of TCR agonism and TCR antagonism with or without partial activation. J. Immunol. 157, 3783-3790.
13. Gras, S., Chen, Z., Miles, J. J., Liu, Y. C., Bell, M. J., Sullivan, L. C., Kjer-Nielsen, L., Brennan, R. M., Burrows, J. M., Neller, M. A., et al. (2010) Allelic polymorphism in the T cell receptor and its impact on immune responses. J. Exp. Med. 207, 1555-1567.
14. Gras, S., Burrows, S. R., Turner, S. J., Sewell, A. K., McCluskey, J., Rossjohn, J. (2012) A structural voyage toward an understanding of the MHC-I-restricted immune response: lessons learned and much to be learned. Immunol. Rev. 250, 61-81.
15. Jenkins, M. K., Chu, H. H., McLachlan, J. B., Moon, J. J. (2010) On the composition of the preimmune repertoire of T cells specific for peptide-major histocompatibility complex ligands. Annu. Rev. Immunol. 28, 275-294.
16. Loveridge, J. A., Rosenberg, W. M., Kirkwood, T. B., Bell, J. I. (1991) The genetic contribution to human T-cell receptor repertoire. Immunology 74, 246-250.
17. Turner, S. J., Doherty, P. C., McCluskey, J., Rossjohn, J. (2006) Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6, 883-894.
18. Obst, R., van Santen, H. M., Mathis, D., Benoist, C. (2005) Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J. Exp. Med. 201, 1555-1565.
19. Fazilleau, N., McHeyzer-Williams, L. J., Rosen, H., McHeyzer-Williams, M. G. (2009) The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat. Immunol. 10, 375-384.
20. Tubo, N. J., Pagan, A. J., Taylor, J. J., Nelson, R. W., Linehan, J. L., Ertelt, J. M., Huseby, E. S., Way, S. S., Jenkins, M. K. (2013) Single naive CD4(+) T cells from a diverse repertoire produce different effector cell types during infection. Cell 153, 785-796.
21. Davis, M. M., Bjorkman, P. J. (1988) T-cell antigen receptor genes and T-cell recognition. Nature 334, 395-402.
22. Davis, M. M., Boniface, J. J., Reich, Z., Lyons, D., Hampl, J., Arden, B., Chien, Y. (1998) Ligand recognition by α β T cell receptors. Annu. Rev. Immunol. 16, 523-544.
23. Casrouge, A., Beaudoing, E., Dalle, S., Pannetier, C., Kanellopoulos, J., Kourilsky, P. (2000) Size estimate of the α β TCR repertoire of naive mouse splenocytes. J. Immunol. 164, 5782-5787.
24. Mackelprang, R., Carlson, C. S., Subrahmanyan, L., Livingston, R. J., Eberle, M. A., Nickerson, D. A. (2002) Sequence variation in the human T-cell receptor loci. Immunol. Rev. 190, 26-39.
25. Kjer-Nielsen, L., Clements, C. S., Purcell, A. W., Brooks, A. G., Whisstock, J. C., Burrows, S. R., McCluskey, J., Rossjohn, J. (2003) A structural basis for the selection of dominant αβ T cell receptors in antiviral immunity. Immunity 18, 53-64.
26. Antunes, I., Tolaini, M., Kissenpfennig, A., Iwashiro, M., Kuribayashi, K., Malissen, B., Hasenkrug, K., Kassiotis, G. (2008) Retrovirus-specificity of regulatory T cells is neither present nor required in preventing retrovirus-induced bone marrow immune pathology. Immunity 29, 782-794.
27. Ploquin, M. J., Eksmond, U., Kassiotis, G. (2011) B cells and TCR avidity determine distinct functions of CD4+ T cells in retroviral infection. J. Immunol. 187, 3321-3330.
28. Young, G. R., Ploquin, M. J., Eksmond, U., Wadwa, M., Stoye, J. P., Kassiotis, G. (2012) Negative selection by an endogenous retrovirus promotes a higher-avidity CD4+ T cell response to retroviral infection. PLoS Pathog. 8, e1002709.
29. Morris, G. P., Allen, P. M. (2012) How the TCR balances sensitivity and specificity for the recognition of self and pathogens. Nat. Immunol. 13, 121-128.
30. Persaud, S. P., Parker, C. R., Lo, W. L., Weber, K. S., Allen, P. M. (2014) Intrinsic CD4(+) T cell sensitivity and response to a pathogen are set and sustained by avidity for thymic and peripheral complexes of self peptide and MHC. Nat. Immunol. 15, 266-274.
31. Mandl, J. N., Monteiro, J. P., Vrisekoop, N., Germain, R. N. (2013) T cell-positive selection uses self-ligand binding strength to optimize repertoire recognition of foreign antigens. Immunity 38, 263-274.
32. Kassiotis, G., Garcia, S., Simpson, E., Stockinger, B. (2002) Impairment of immunological memory in the absence of MHC despite survival of memory T cells. Nat. Immunol. 3, 244-250.
33. Stefanova, I., Dorfman, J. R., Germain, R. N. (2002) Self-recognition promotes the foreign antigen sensitivity of naive T lymphocytes. Nature 420, 429-434.
34. Acha-Orbea, H., MacDonald, H. R. (1995) Superantigens of mouse mammary tumor virus. Annu. Rev. Immunol. 13, 459-486.
35. Punkosdy, G. A., Blain, M., Glass, D. D., Lozano, M. M., O'Mara, L., Dudley, J. P., Ahmed, R., Shevach, E. M. (2011) Regulatory T-cell expansion during chronic viral infection is dependent on endogenous retroviral superantigens. Proc. Natl. Acad. Sci. USA 108, 3677-3682.
36. Myers, L., Joedicke, J. J., Carmody, A. B., Messer, R. J., Kassiotis, G., Dudley, J. P., Dittmer, U., Hasenkrug, K. J. (2013) IL-2-independent and TNF-α-dependent expansion of Vβ5+ natural regulatory T cells during retrovirus infection. J. Immunol. 190, 5485-5495.
37. Ribot, J., Romagnoli, P., van Meerwijk, J. P. (2006) Agonist ligands expressed by thymic epithelium enhance positive selection of regulatory T lymphocytes from precursors with a normally diverse TCR repertoire. J. Immunol. 177, 1101-1107.
38. Conrad, B., Weissmahr, R. N., Boni, J., Arcari, R., Schupbach, J., Mach, B. (1997) A human endogenous retroviral superantigen as candidate autoimmune gene in type I diabetes. Cell 90, 303-313.
39. Tai, A. K., Lin, M., Chang, F., Chen, G., Hsiao, F., Sutkowski, N., Huber, B. T. (2006) Murine Vβ3+ and Vβ7+ T cell subsets are specific targets for the HERV-K18 Env superantigen. J. Immunol. 177, 3178-3184.
40. Ebert, P. J., Jiang, S., Xie, J., Li, Q. J., Davis, M. M. (2009) An endogenous positively selecting peptide enhances mature T cell responses and becomes an autoantigen in the absence of microRNA miR-181a. Nat. Immunol. 10, 1162-1169.
41. Kosmrlj, A., Read, E. L., Qi, Y., Allen, T. M., Altfeld, M., Deeks, S. G., Pereyra, F., Carrington, M., Walker, B. D., Chakraborty, A. K. (2010) Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 465, 350-354.
42. Zhu, J., Paul, W. E. (2010) Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol. Rev. 238, 247-262.
43. Pike, R., Filby, A., Ploquin, M. J., Eksmond, U., Marques, R., Antunes, I., Hasenkrug, K., Kassiotis, G. (2009) Race between retroviral spread and CD4+ T-cell response determines the outcome of acute Friend virus infection. J. Virol. 83, 11211-11222.
44. Moon, J. J., Chu, H. H., Pepper, M., McSorley, S. J., Jameson, S. C., Kedl, R. M., Jenkins, M. K. (2007) Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27, 203-213.
45. Germain, R. N., Stefanova, I. (1999) The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Annu. Rev. Immunol. 17, 467-522.
46. Corse, E., Gottschalk, R. A., Allison, J. P. (2011) Strength of TCR-peptide/ MHC interactions and in vivo T cell responses. J. Immunol. 186, 5039-5045.
47. Stone, J. D., Chervin, A. S., Kranz, D. M. (2009) T-cell receptor binding affinities and kinetics: impact on T-cell activity and specificity. Immunology 126, 165-176.
48. Huang, J., Zarnitsyna, V. I., Liu, B., Edwards, L. J., Jiang, N., Evavold, B. D., Zhu, C. (2010) The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464, 932-936.
49. Govern, C. C., Paczosa, M. K., Chakraborty, A. K., Huseby, E. S. (2010) Fast on-rates allow short dwell time ligands to activate T cells. Proc. Natl. Acad. Sci. USA 107, 8724-8729.
50. Malherbe, L., Hausl, C., Teyton, L., McHeyzer-Williams, M. G. (2004) Clonal selection of helper T cells is determined by an affinity threshold with no further skewing of TCR binding properties. Immunity 21, 669-679.
51. Fasso, M., Anandasabapathy, N., Crawford, F., Kappler, J., Fathman, C. G., Ridgway, W. M. (2000) T cell receptor (TCR)-mediated repertoire selection and loss of TCR vβ diversity during the initiation of a CD4(+) T cell response in vivo. J. Exp. Med. 192, 1719-1730.
52. Gett, A. V., Sallusto, F., Lanzavecchia, A., Geginat, J. (2003) T cell fitness determined by signal strength. Nat. Immunol. 4, 355-360.
53. Celli, S., Lemaitre, F., Bousso, P. (2007) Real-time manipulation of T cell-dendritic cell interactions in vivo reveals the importance of prolonged contacts for CD4+ T cell activation. Immunity 27, 625-634.
54. Yarke, C. A., Dalheimer, S. L., Zhang, N., Catron, D. M., Jenkins, M. K., Mueller, D. L. (2008) Proliferating CD4+ T cells undergo immediate growth arrest upon cessation of TCR signaling in vivo. J. Immunol. 180, 156-162.
55. Foulds, K. E., Shen, H. (2006) Clonal competition inhibits the proliferation and differentiation of adoptively transferred TCR transgenic CD4 T cells in response to infection. J. Immunol. 176, 3037-3043.
56. Weaver, J. M., Chaves, F. A., Sant, A. J. (2009) Abortive activation of CD4 T cell responses during competitive priming in vivo. Proc. Natl. Acad. Sci. USA 106, 8647-8652.
57. Whitmire, J. K., Benning, N., Eam, B., Whitton, J. L. (2008) Increasing the CD4+ T cell precursor frequency leads to competition for IFN-γ thereby degrading memory cell quantity and quality. J. Immunol. 180, 6777-6785.
58. Blair, D. A., Lefrancois, L. (2007) Increased competition for antigen during priming negatively impacts the generation of memory CD4 T cells. Proc. Natl. Acad. Sci. USA 104, 15045-15050.
59. Gerlach, C., Rohr, J. C., Perié, L., van Rooij, N., van Heijst, J. W., Velds, A., Urbanus, J., Naik, S. H., Jacobs, H., Beltman, J. B., et al. (2013) Heterogeneous differentiation patterns of individual CD8+ T cells. Science 340, 635-639.
60. Buchholz, V. R., Flossdorf, M., Hensel, I., Kretschmer, L., Weissbrich, B., Graf, P., Verschoor, A., Schiemann, M., Hofer, T., Busch, D. H. (2013) Disparate individual fates compose robust CD8+ T cell immunity. Science 340, 630-635.
61. O'Shea, J. J., Paul, W. E. (2010) Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 327, 1098-1102.
62. Hosken, N. A., Shibuya, K., Heath, A. W., Murphy, K. M., O'Garra, A. (1995) The effect of antigen dose on CD4+ T helper cell phenotype development in a T cell receptor-α β-transgenic model. J. Exp. Med. 182, 1579-1584.
63. Constant, S., Pfeiffer, C., Woodard, A., Pasqualini, T., Bottomly, K. (1995) Extent of T cell receptor ligation can determine the functional differentiation of naive CD4+ T cells. J. Exp. Med. 182, 1591-1596.
64. Rogers, P. R., Croft, M. (1999) Peptide dose, affinity, and time of differentiation can contribute to the Th1/Th2 cytokine balance. J. Immunol. 163, 1205-1213.
65. Milner, J. D., Fazilleau, N., McHeyzer-Williams, M., Paul, W. (2010) Cutting edge: lack of high affinity competition for peptide in polyclonal CD4+ responses unmasks IL-4 production. J. Immunol. 184, 6569-6573.
66. Fahey, L. M., Wilson, E. B., Elsaesser, H., Fistonich, C. D., McGavern, D. B., Brooks, D. G. (2011) Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J. Exp. Med. 208, 987-999.
67. Harker, J. A., Lewis, G. M., Mack, L., Zuniga, E. I. (2011) Late interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection. Science 334, 825-829.
68. Marshall, H. D., Chandele, A., Jung, Y. W., Meng, H., Poholek, A. C., Parish, I. A., Rutishauser, R., Cui, W., Kleinstein, S. H., Craft, J., et al. (2011) Differential expression of Ly6C and T-bet distinguish effector and memory Th1 CD4(+) cell properties during viral infection. Immunity 35, 633-646.
69. Pepper, M., Pagan, A. J., Igyarto, B. Z., Taylor, J. J., Jenkins, M. K. (2011) Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 35, 583-595.
70. Nurieva, R. I., Chung, Y., Hwang, D., Yang, X. O., Kang, H. S., Ma, L., Wang, Y. H., Watowich, S. S., Jetten, A. M., Tian, Q., et al. (2008) Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29, 138-149.
71. Deenick, E. K., Chan, A., Ma, C. S., Gatto, D., Schwartzberg, P. L., Brink, R., Tangye, S. G. (2010) Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 33, 241-253.
72. Baumjohann, D., Preite, S., Reboldi, A., Ronchi, F., Ansel, K. M., Lanzavecchia, A., Sallusto, F. (2013) Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38, 596-605.
73. Choi, Y. S., Yang, J. A., Yusuf, I., Johnston, R. J., Greenbaum, J., Peters, B., Crotty, S. (2013) Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory. J. Immunol. 190, 4014-4026.
74. Leddon, S. A., Sant, A. J. (2012) The peptide specificity of the endogenous T follicular helper cell repertoire generated after protein immunization. PLoS One 7, e46952.
75. Lindqvist, M., van Lunzen, J., Soghoian, D. Z., Kuhl, B. D., Ranasinghe, S., Kranias, G., Flanders, M. D., Cutler, S., Yudanin, N., Muller, M. I., et al. (2012) Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J. Clin. Invest. 122, 3271-3280.
76. Perreau, M., Savoye, A. L., De Crignis, E., Corpataux, J. M., Cubas, R., Haddad, E. K., De Leval, L., Graziosi, C., Pantaleo, G. (2013) Follicular helper T cells serve as the major CD4 T cell compartment for HIV-1 infection, replication, and production. J. Exp. Med. 210, 143-156.
77. Cubas, R. A., Mudd, J. C., Savoye, A. L., Perreau, M., van Grevenynghe, J., Metcalf, T., Connick, E., Meditz, A., Freeman, G. J., Abesada-Terk, G., Jr., et al. (2013) Inadequate T follicular cell help impairs B cell immunity during HIV infection. Nat. Med. 19, 494-499.
78. Vingert, B., Perez-Patrigeon, S., Jeannin, P., Lambotte, O., Boufassa, F., Lemaitre, F., Kwok, W. W., Theodorou, I., Delfraissy, J. F., Theze, J., et al. (2010) HIV controller CD4+ T cells respond to minimal amounts of Gag antigen due to high TCR avidity. PLoS Pathog. 6, e1000780.
79. Liu, X., Yan, X., Zhong, B., Nurieva, R. I., Wang, A., Wang, X., Martin-Orozco, N., Wang, Y., Chang, S. H., Esplugues, E., et al. (2012) Bcl6 expression specifies the T follicular helper cell program in vivo. J. Exp. Med. 209, 1841-1824.
80. Luthje, K., Kallies, A., Shimohakamada, Y., Belz, G. T., Light, A., Tarlinton, D. M., Nutt, S. L. (2012) The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat. Immunol. 13, 491-498.
81. MacLeod, M. K., David, A., McKee, A. S., Crawford, F., Kappler, J. W., Marrack, P. (2011) Memory CD4 T cells that express CXCR5 provide accelerated help to B cells. J. Immunol. 186, 2889-2896.
82. Hale, J. S., Youngblood, B., Latner, D. R., Mohammed, A. U., Ye, L., Akondy, R. S., Wu, T., Iyer, S. S., Ahmed, R. (2013) Distinct memory CD4+ T cells with commitment to T follicular helper-and T helper 1-cell lineages are generated after acute viral infection. Immunity 38, 805-817.
83. Sallusto, F., Geginat, J., Lanzavecchia, A. (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763.
84. Brooks, D. G., Teyton, L., Oldstone, M. B., McGavern, D. B. (2005) Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. J. Virol. 79, 10514-10527.
85. Welsh, R. M., Selin, L. K., Szomolanyi-Tsuda, E. (2004) Immunological memory to viral infections. Annu. Rev. Immunol. 22, 711-743.
86. McHeyzer-Williams, M. G., Davis, M. M. (1995) Antigen-specific development of primary and memory T cells in vivo. Science 268, 106-111.
87. Savage, P. A., Boniface, J. J., Davis, M. M. (1999) A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10, 485-492.
88. McHeyzer-Williams, L. J., Panus, J. F., Mikszta, J. A., McHeyzer-Williams, M. G. (1999) Evolution of antigen-specific T cell receptors in vivo: preimmune and antigen-driven selection of preferred complementarity-determining region 3 (CDR3) motifs. J. Exp. Med. 189, 1823-1838.
89. Sabatino, J. J., Jr., Huang, J., Zhu, C., Evavold, B. D. (2011) High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses. J. Exp. Med. 208, 81-90.
90. Williams, M. A., Ravkov, E. V., Bevan, M. J. (2008) Rapid culling of the CD4+ T cell repertoire in the transition from effector to memory. Immunity 28, 533-545.
91. Kim, C., Jay, D. C., Williams, M. A. (2012) Stability and function of secondary Th1 memory cells are dependent on the nature of the secondary stimulus. J. Immunol. 189, 2348-2355.
92. Slifka, M. K., Whitton, J. L. (2001) Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat. Immunol. 2, 711-717.
93. Fahmy, T. M., Bieler, J. G., Edidin, M., Schneck, J. P. (2001) Increased TCR avidity after T cell activation: a mechanism for sensing low-density antigen. Immunity 14, 135-143.
94. Kim, C., Wilson, T., Fischer, K. F., Williams, M. A. (2013) Sustained interactions between T cell receptors and antigens promote the differentiation of CD4(+) memory T cells. Immunity 39, 508-520.
95. Baumgartner, C. K., Yagita, H., Malherbe, L. P. (2012) A TCR affinity threshold regulates memory CD4 T cell differentiation following vaccination. J. Immunol. 189, 2309-2317.
96. Rees, W., Bender, J., Teague, T. K., Kedl, R. M., Crawford, F., Marrack, P., Kappler, J. (1999) An inverse relationship between T cell receptor affinity and antigen dose during CD4(+) T cell responses in vivo and in vitro. Proc. Natl. Acad. Sci. USA 96, 9781-9786.
97. Weber, K. S., Li, Q. J., Persaud, S. P., Campbell, J. D., Davis, M. M., Allen, P. M. (2012) Distinct CD4+ helper T cells involved in primary and secondary responses to infection. Proc. Natl. Acad. Sci. USA 109, 9511-9516.
98. Ertelt, J. M., Johanns, T. M., Mysz, M. A., Nanton, M. R., Rowe, J. H., Aguilera, M. N., Way, S. S. (2011) Selective culling of high avidity antigen-specific CD4+ T cells after virulent Salmonella infection. Immunology 134, 487-497.
99. Caserta, S., Kleczkowska, J., Mondino, A., Zamoyska, R. (2010) Reduced functional avidity promotes central and effector memory CD4 T cell responses to tumor-associated antigens. J. Immunol. 185, 6545-6554.
100. Anderton, S. M., Radu, C. G., Lowrey, P. A., Ward, E. S., Wraith, D. C. (2001) Negative selection during the peripheral immune response to antigen. J. Exp. Med. 193, 1-11.
101. Pitcher, C. J., Quittner, C., Peterson, D. M., Connors, M., Koup, R. A., Maino, V. C., Picker, L. J. (1999) HIV-1-specific CD4+ T cells are detectable in most individuals with active HIV-1 infection, but decline with prolonged viral suppression. Nat. Med. 5, 518-525.
102. Malhotra, U., Holte, S., Zhu, T., Delpit, E., Huntsberry, C., Sette, A., Shankarappa, R., Maenza, J., Corey, L., McElrath, M. J. (2003) Early induction and maintenance of Env-specific T-helper cells following human immunodeficiency virus type 1 infection. J. Virol. 77, 2663-2674.
103. Malherbe, L., Mark, L., Fazilleau, N., McHeyzer-Williams, L. J., McHeyzer-Williams, M. G. (2008) Vaccine adjuvants alter TCR-based selection thresholds. Immunity 28, 698-709.
104. Nishikawa, H., Qian, F., Tsuji, T., Ritter, G., Old, L. J., Gnjatic, S., Odunsi, K. (2006) Influence of CD4+CD25+ regulatory T cells on low/high-avidity CD4+ T cells following peptide vaccination. J. Immunol. 176, 6340-6346.
105. Pace, L., Tempez, A., Arnold-Schrauf, C., Lemaitre, F., Bousso, P., Fetler, L., Sparwasser, T., Amigorena, S. (2012) Regulatory T cells increase the avidity of primary CD8+ T cell responses and promote memory. Science 338, 532-536.
106. Welsh, R. M., Che, J. W., Brehm, M. A., Selin, L. K. (2010) Heterologous immunity between viruses. Immunol. Rev. 235, 244-266.
107. Gallimore, A., Glithero, A., Godkin, A., Tissot, A. C., Pluckthun, A., Elliott, T., Hengartner, H., Zinkernagel, R. (1998) Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187, 1383-1393.
108. Munitic, I., Decaluwe, H., Evaristo, C., Lemos, S., Wlodarczyk, M., Worth, A., Le, B. A., Selin, L. K., Riviere, Y., Di Santo, J. P., et al. (2009) Epitope specificity and relative clonal abundance do not affect CD8 differentiation patterns during lymphocytic choriomeningitis virus infection. J. Virol. 83, 11795-11807.
109. Kirchhoff, F., Schindler, M., Specht, A., Arhel, N., Munch, J. (2008) Role of Nef in primate lentiviral immunopathogenesis. Cell. Mol. Life Sci. 65, 2621-2636.
110. McMichael, A. J., Phillips, R. E. (1997) Escape of human immunodeficiency virus from immune control. Annu. Rev. Immunol. 15, 271-296.
111. Goon, P. K., Igakura, T., Hanon, E., Mosley, A. J., Barfield, A., Barnard, A. L., Kaftantzi, L., Tanaka, Y., Taylor, G. P., Weber, J. N., et al. (2004) Human T cell lymphotropic virus type I (HTLV-I)-specific CD4+ T cells: immunodominance hierarchy and preferential infection with HTLV-I. J. Immunol. 172, 1735-1743.
112. Douek, D. C., Brenchley, J. M., Betts, M. R., Ambrozak, D. R., Hill, B. J., Okamoto, Y., Casazza, J. P., Kuruppu, J., Kunstman, K., Wolinsky, S., et al. (2002) HIV preferentially infects HIV-specific CD4+ T cells. Nature 417, 95-98.
113. Walker, B., McMichael, A. (2012) The T-cell response to HIV. Cold Spring Harb. Perspect. Med. 2, pii: a007054.
114. Buzon, M. J., Sun, H., Li, C., Shaw, A., Seiss, K., Ouyang, Z., Martin-Gayo, E., Leng, J., Henrich, T. J., Li, J. Z., et al. (2014) HIV-1 persistence in CD4(+) T cells with stem cell-like properties. Nat. Med. 20, 139-142.
115. Chomont, N., El-Far, M., Ancuta, P., Trautmann, L., Procopio, F. A., Yassine-Diab, B., Boucher, G., Boulassel, M. R., Ghattas, G., Brenchley, J. M., et al. (2009) HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat. Med. 15, 893-900.
116. Alexander-Miller, M. A., Leggatt, G. R., Berzofsky, J. A. (1996) Selective expansion of high-or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93, 4102-4107.
117. Almeida, J. R., Price, D. A., Papagno, L., Arkoub, Z. A., Sauce, D., Bornstein, E., Asher, T. E., Samri, A., Schnuriger, A., Theodorou, I., et al. (2007) Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204, 2473-2485.
118. La Gruta, N. L., Thomas, P. G., Webb, A. I., Dunstone, M. A., Cukalac, T., Doherty, P. C., Purcell, A. W., Rossjohn, J., Turner, S. J. (2008) Epitope-specific TCRβ repertoire diversity imparts no functional advantage on the CD8+ T cell response to cognate viral peptides. Proc. Natl. Acad. Sci. USA 105, 2034-2039.
119. Iglesias, M. C., Almeida, J. R., Fastenackels, S., van Bockel, D. J., Hashimoto, M., Venturi, V., Gostick, E., Urrutia, A., Wooldridge, L., Clement, M., et al. (2011) Escape from highly effective public CD8+ T-cell clonotypes by HIV. Blood 118, 2138-2149.
120. Burton, D. R., Ahmed, R., Barouch, D. H., Butera, S. T., Crotty, S., Godzik, A., Kaufmann, D. E., McElrath, M. J., Nussenzweig, M. C., Pulendran, B., et al. (2012) A blueprint for HIV vaccine discovery. Cell. Host Microbe 12, 396-407.
121. Seder, R. A., Darrah, P. A., Roederer, M. (2008) T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8, 247-258.
122. Zhu, J., Yamane, H., Paul, W. E. (2010) Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489.
123. Yue, F. Y., Lo, C., Sakhdari, A., Lee, E. Y., Kovacs, C. M., Benko, E., Liu, J., Song, H., Jones, R. B., Sheth, P., et al. (2010) HIV-specific IL-21 producing CD4+ T cells are induced in acute and chronic progressive HIV infection and are associated with relative viral control. J. Immunol. 185, 498-506.
124. Iannello, A., Boulassel, M. R., Samarani, S., Debbeche, O., Tremblay, C., Toma, E., Routy, J. P., Ahmad, A. (2010) Dynamics and consequences of IL-21 production in HIV-infected individuals: a longitudinal and cross-sectional study. J. Immunol. 184, 114-126.
125. Obst, R., van Santen, H. M., Melamed, R., Kamphorst, A. O., Benoist, C., Mathis, D. (2007) Sustained antigen presentation can promote an immunogenic T cell response, like dendritic cell activation. Proc. Natl. Acad. Sci. USA 104, 15460-15465.
126. Kitchen, S. G., Levin, B. R., Bristol, G., Rezek, V., Kim, S., Aguilera-Sandoval, C., Balamurugan, A., Yang, O. O., Zack, J. A. (2012) In vivo suppression of HIV by antigen specific T cells derived from engineered hematopoietic stem cells. PLoS Pathog. 8, e1002649.
127. Chen, H., Ndhlovu, Z. M., Liu, D., Porter, L. C., Fang, J. W., Darko, S., Brockman, M. A., Miura, T., Brumme, Z. L., Schneidewind, A., et al. (2012) TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 13, 691-700.