The role of naive T cell precursor frequency and recruitment in dictating immune response magnitude

Journal of Immunology

Volumn 188, Issue 9, 2012, Pages 4135-4140

  Jenkins, Marc K ^a   Moon, James J ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE; T LYMPHOCYTE RECEPTOR;

ANTIGEN PRESENTING CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL POPULATION; ENRICHMENT CULTURE; IMMUNE RESPONSE; LIGAND BINDING; LYMPHOCYTE COUNT; LYMPHOCYTE CULTURE; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; POPULATION SIZE; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS; HUMANS; IMMUNITY, CELLULAR; PEPTIDES; PRECURSOR CELLS, T-LYMPHOID; RECEPTORS, ANTIGEN, T-CELL;

EID: 84860346184     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102661     Document Type: Review

References (57)

1. Henrickson, S. E., T. R. Mempel, I. B. Mazo, B. Liu, M. N. Artyomov, H. Zheng, A. Peixoto, M. P. Flynn, B. Senman, T. Junt, et al. 2008. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat. Immunol. 9: 282-291. (Pubitemid 351267325)
2. Obst, R., H. M. van Santen, D. Mathis, and C. Benoist. 2005. Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J. Exp. Med. 201: 1555-1565. (Pubitemid 40721001)
3. Prlic, M., G. Hernandez-Hoyos, and M. J. Bevan. 2006. Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J. Exp. Med. 203: 2135-2143. (Pubitemid 44352234)
4. Itano, A. A., S. J. McSorley, R. L. Reinhardt, B. D. Ehst, E. Ingulli, A. Y. Rudensky, and M. K. Jenkins. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19: 47-57. (Pubitemid 36859900)
5. Sant, A. J., F. A. Chaves, S. A. Jenks, K. A. Richards, P. Menges, J. M. Weaver, and C. A. Lazarski. 2005. The relationship between immunodominance, DM editing, and the kinetic stability of MHC class II: peptide complexes. Immunol. Rev. 207: 261-278. (Pubitemid 41415023)
6. Yewdell, J. W. 2006. Confronting complexity: real-world immunodominance in antiviral CD8+ T cell responses. Immunity 25: 533-543. (Pubitemid 44529047)
7. Moon, J. J., H. H. Chu, M. Pepper, S. J. McSorley, S. C. Jameson, R. M. Kedl, and M. K. Jenkins. 2007. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27: 203-213. (Pubitemid 47284919)
8. Nikolich-Zugich, J., M. K. Slifka, and I. Messaoudi. 2004. The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 4: 123-132. (Pubitemid 38209206)
9. Jenkins, M. K., H. H. Chu, J. B. McLachlan, and J. J. Moon. 2010. On the composition of the preimmune repertoire of T cells specific for Peptide-major histocompatibility complex ligands. Annu. Rev. Immunol. 28: 275-294.
10. Corradin, G., H. M. Etlinger, and J. M. Chiller. 1977. Lymphocyte specificity to protein antigens. I. Characterization of the antigen-induced in vitro T cell-dependent proliferative response with lymph node cells from primed mice. J. Immunol. 119: 1048-1053. (Pubitemid 8202973)
11. Geiger, R., T. Duhen, A. Lanzavecchia, and F. Sallusto. 2009. Human naive and memory CD4+ T cell repertoires specific for naturally processed antigens analyzed using libraries of amplified T cells. J. Exp. Med. 206: 1525-1534.
12. Altman, J. D., P. A. H. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96. (Pubitemid 26332731)
13. Bodinier, M., M. A. Peyrat, C. Tournay, F. Davodeau, F. Romagne, M. Bonneville, and F. Lang. 2000. Efficient detection and immunomagnetic sorting of specific T cells using multimers of MHC class I and peptide with reduced CD8 binding. Nat. Med. 6: 707-710. (Pubitemid 30398798)
14. McDermott, A. B., H. M. Spiegel, J. Irsch, G. S. Ogg, and D. F. Nixon. 2001. A simple and rapid magnetic bead separation technique for the isolation of tetramer-positive virus-specific CD8 T cells. AIDS 15: 810-812. (Pubitemid 32423236)
15. Keenan, R. D., J. Ainsworth, N. Khan, R. Bruton, M. Cobbold, M. Assenmacher, D. W. Milligan, and P. A. Moss. 2001. Purification of cytomegalovirus-specific CD8 T cells from peripheral blood using HLA-peptide tetramers. Br. J. Haematol. 115: 428-434. (Pubitemid 34203513)
16. Jäger, E., H. Höhn, A. Necker, R. Förster, J. Karbach, K. Freitag, C. Neukirch, C. Castelli, R. D. Salter, A. Knuth, and M. J. Maeurer. 2002. Peptide-specific CD8+ T-cell evolution in vivo: response to peptide vaccination with Melan-A/MART-1. Int. J. Cancer 98: 376-388. (Pubitemid 34188681)
17. Jang, M. H., N. P. Seth, and K. W. Wucherpfennig. 2003. Ex vivo analysis of thymic CD4 T cells in nonobese diabetic mice with tetramers generated from I-A(g7)/class II-associated invariant chain peptide precursors. J. Immunol. 171: 4175-4186. (Pubitemid 37238694)
18. Day, C. L., N. P. Seth, M. Lucas, H. Appel, L. Gauthier, G. M. Lauer, G. K. Robbins, Z. M. Szczepiorkowski, D. R. Casson, R. T. Chung, et al. 2003. Ex vivo analysis of human memory CD4 T cells specific for hepatitis C virus using MHC class II tetramers. J. Clin. Invest. 112: 831-842. (Pubitemid 38063741)
19. Lemaître, F., M. Viguier, M. S. Cho, J. M. Fourneau, B. Maillère, P. Kourilsky, P. M. Van Endert, and L. Ferradini. 2004. Detection of low-frequency human antigen-specific CD4(+) T cells using MHC class II multimer bead sorting and immunoscope analysis. Eur. J. Immunol. 34: 2941-2949. (Pubitemid 39430169)
20. Barnes, E., S. M. Ward, V. O. Kasprowicz, G. Dusheiko, P. Klenerman, and M. Lucas. 2004. Ultra-sensitive class I tetramer analysis reveals previously unde-tectable populations of antiviral CD8+ T cells. Eur. J. Immunol. 34: 1570-1577. (Pubitemid 39256038)
21. Lucas, M., C. L. Day, J. R. Wyer, S. L. Cunliffe, A. Loughry, A. J. McMichael, and P. Klenerman. 2004. Ex vivo phenotype and frequency of influenza virus-specific CD4 memory T cells. J. Virol. 78: 7284-7287. (Pubitemid 38781568)
22. Scriba, T. J., M. Purbhoo, C. L. Day, N. Robinson, S. Fidler, J. Fox, J. N. Weber, P. Klenerman, A. K. Sewell, and R. E. Phillips. 2005. Ultrasensitive detection and phenotyping of CD4+ T cells with optimized HLA class II tetramer staining. J. Immunol. 175: 6334-6343. (Pubitemid 41598873)
23. Chu, H. H., J. J. Moon, A. C. Kruse, M. Pepper, and M. K. Jenkins. 2010. Negative selection and peptide chemistry determine the size of naive foreign peptide-MHC class II-specific CD4+ T cell populations. J. Immunol. 185: 4705-4713.
24. Chu, H. H., J. J. Moon, K. Takada, M. Pepper, J. A. Molitor, T. W. Schacker, K. A. Hogquist, S. C. Jameson, and M. K. Jenkins. 2009. Positive selection optimizes the number and function of MHCII-restricted CD4+ T cell clones in the naive polyclonal repertoire. Proc. Natl. Acad. Sci. USA 106: 11241-11245.
25. Pepper, M., A. J. Pagán, B. Z. Igyártó, J. J. Taylor, and M. K. Jenkins. 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.
26. Lee, S. J., J. B. McLachlan, J. R. Kurtz, D. Fan, S. E. Winter, A. J. Baumler, M. K. Jenkins, and S. J. McSorley. 2012. Temporal expression of bacterial proteins instructs host CD4 T cell expansion and Th17 development. PLoS Pathog. 8: e1002499.
27. Dileepan, T., J. L. Linehan, J. J. Moon, M. Pepper, M. K. Jenkins, and P. P. Cleary. 2011. Robust antigen specific th17 T cell response to group A Streptococcus is dependent on IL-6 and intranasal route of infection. PLoS Pathog. 7: e1002252.
28. Rees, W., J. Bender, T. K. Teague, R. M. Kedl, F. Crawford, P. Marrack, and J. Kappler. 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. (Pubitemid 29398809)
29. McSorley, S. J., B. T. Cookson, and M. K. Jenkins. 2000. Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J. Immunol. 164: 986-993. (Pubitemid 30043726)
30. Robertson, J. M., P. E. Jensen, and B. D. Evavold. 2000. DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 164: 4706-4712. (Pubitemid 30238071)
31. Geginat, G., S. Schenk, M. Skoberne, W. Goebel, and H. Hof. 2001. A novel approach of direct ex vivo epitope mapping identifies dominant and subdominant CD4 and CD8 T cell epitopes from Listeria monocytogenes. J. Immunol. 166: 1877-1884. (Pubitemid 32114674)
32. Kwok, W. W., V. Tan, L. Gillette, C. T. Littell, M. A. Soltis, R. B. Lafond, J. Yang, E. A. James, and J. H. Delong. 2012. Frequency of epitope-specific naive CD4+ T cells correlates with immunodominance in the human memory repertoire. J. Immunol. 188: 2537-2544.
33. Arstila, T. P., A. Casrouge, V. Baron, J. Even, J. Kanellopoulos, and P. Kourilsky. 1999. A direct estimate of the human alphabeta T cell receptor diversity. Science 286: 958-961.
34. Casrouge, A., E. Beaudoing, S. Dalle, C. Pannetier, J. Kanellopoulos, and P. Kourilsky. 2000. Size estimate of the alpha beta TCR repertoire of naive mouse splenocytes. J. Immunol. 164: 5782-5787. (Pubitemid 30389821)
35. Sabatino, J. J., Jr., J. Huang, C. Zhu, and B. D. Evavold. 2011. High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses. J. Exp. Med. 208: 81-90.
36. Day, E. B., K. L. Charlton, N. L. La Gruta, P. C. Doherty, and S. J. Turner. 2011. Effect of MHC class I diversification on influenza epitope-specific CD8+ T cell precursor frequency and subsequent effector function. J. Immunol. 186: 6319-6328.
37. Kosmrlj, A., E. L. Read, Y. Qi, T. M. Allen, M. Altfeld, S. G. Deeks, F. Pereyra, M. Carrington, B. D. Walker, and A. K. Chakraborty. 2010. Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 465: 350-354.
38. Turner, S. J., K. Kedzierska, H. Komodromou, N. L. La Gruta, M. A. Dunstone, A. I. Webb, R. Webby, H. Walden, W. Xie, J. McCluskey, et al. 2005. Lack of prominent peptide-major histocompatibility complex features limits repertoire diversity in virus-specific CD8+ T cell populations. Nat. Immunol. 6: 382-389. (Pubitemid 41716778)
39. Obar, J. J., K. M. Khanna, and L. Lefrançois. 2008. Endogenous naive CD8+ T cell precursor frequency regulates primary and memory responses to infection. Immunity 28: 859-869.
40. Kotturi, M. F., I. Scott, T. Wolfe, B. Peters, J. Sidney, H. Cheroutre, M. G. von Herrath, M. J. Buchmeier, H. Grey, and A. Sette. 2008. Naive precursor frequencies and MHC binding rather than the degree of epitope diversity shape CD8+ T cell immunodominance. J. Immunol. 181: 2124-2133.
41. Tan, A. C., N. L. La Gruta, W. Zeng, and D. C. Jackson. 2011. Precursor frequency and competition dictate the HLA-A2-restricted CD8+ T cell responses to influenza A infection and vaccination in HLA-A2.1 transgenic mice. J. Immunol. 187: 1895-1902.
42. Schmidt, J., C. Neumann-Haefelin, T. Altay, E. Gostick, D. A. Price, V. Lohmann, H. E. Blum, and R. Thimme. 2011. Immunodominance of HLA-A2-restricted hepatitis C virus-specific CD8+ T cell responses is linked to naive-precursor frequency. J. Virol. 85: 5232-5236.
43. Yager, E. J., M. Ahmed, K. Lanzer, T. D. Randall, D. L. Woodland, and M. A. Blackman. 2008. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 205: 711-723. (Pubitemid 351439315)
44. Flesch, I. E., W. P. Woo, Y. Wang, V. Panchanathan, Y. C. Wong, N. L. La Gruta, T. Cukalac, and D. C. Tscharke. 2010. Altered CD8(+) T cell immunodominance after vaccinia virus infection and the naive repertoire in inbred and F(1) mice. J. Immunol. 184: 45-55.
45. La Gruta, N. L., W. T. Rothwell, T. Cukalac, N. G. Swan, S. A. Valkenburg, K. Kedzierska, P. G. Thomas, P. C. Doherty, and S. J. Turner. 2010. Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J. Clin. Invest. 120: 1885-1894.
46. Ruckwardt, T. J., A. M. Malloy, E. Gostick, D. A. Price, P. Dash, J. L. McClaren, P. G. Thomas, and B. S. Graham. 2011. Neonatal CD8 T-cell hierarchy is distinct from adults and is influenced by intrinsic T cell properties in respiratory syncytial virus infected mice. PLoS Pathog. 7: e1002377.
47. van Heijst, J. W., C. Gerlach, E. Swart, D. Sie, C. Nunes-Alves, R. M. Kerkhoven, R. Arens, M. Correia-Neves, K. Schepers, and T. N. Schumacher. 2009. Recruitment of antigen-specific CD8+ T cells in response to infection is markedly efficient. Science 325: 1265-1269.
48. Zehn, D., S. Y. Lee, and M. J. Bevan. 2009. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458: 211-214.
49. Malherbe, L., C. Hausl, L. Teyton, and M. G. McHeyzer-Williams. 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. (Pubitemid 39487890)
50. Hamilton, S. E., J. M. Schenkel, A. D. Akue, and S. C. Jameson. 2010. IL-2 complex treatment can protect naive mice from bacterial and viral infection. J. Immunol. 185: 6584-6590.
51. Haluszczak, C., A. D. Akue, S. E. Hamilton, L. D. Johnson, L. Pujanauski, L. Teodorovic, S. C. Jameson, and R. M. Kedl. 2009. The antigen-specific CD8+ T cell repertoire in unimmunized mice includes memory phenotype cells bearing markers of homeostatic expansion. J. Exp. Med. 206: 435-448.
52. Akue, A. D., J. Y. Lee, and S. C. Jameson. 2012. Derivation and maintenance of virtual memory CD8 T cells. J. Immunol. 188: 2516-2523.
53. Moon, J. J., P. Dash, T. H. Oguin, III, J. L. McClaren, H. H. Chu, P. G. Thomas, and M. K. Jenkins. 2011. Quantitative impact of thymic selection on Foxp3+ and Foxp3-subsets of self-peptide/MHC class II-specific CD4+ T cells. Proc. Natl. Acad. Sci. USA 108: 14602-14607.
54. Pepper, M., J. L. Linehan, A. J. Pagán, T. Zell, T. Dileepan, P. P. Cleary, and M. K. Jenkins. 2010. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 11: 83-89.
55. Zhao, J., J. Zhao, C. Fett, K. Trandem, E. Fleming, and S. Perlman. 2011. IFN-γ-and IL-10-expressing virus epitope-specific Foxp3(+) T reg cells in the central nervous system during encephalomyelitis. J. Exp. Med. 208: 1571-1577.
56. Legoux, F., E. Debeaupuis, K. Echasserieau, H. De La Salle, X. Saulquin, and M. Bonneville. 2010. Impact of TCR reactivity and HLA phenotype on naive CD8 T cell frequency in humans. J. Immunol. 184: 6731-6738.
57. Alanio, C., F. Lemaitre, H. K. Law, M. Hasan, and M. L. Albert. 2010. Enumeration of human antigen-specific naive CD8+ T cells reveals conserved precursor frequencies. Blood 115: 3718-3725.