A peripheral CD4+ T cell precursor for naive, memory, and regulatory T cells

Journal of Experimental Medicine

Volumn 207, Issue 13, 2010, Pages 2883-2894

  Zhao, Chunfang ^a   Davies, Joanna D ^a  

^a TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD44V ANTIGEN; CD5 ANTIGEN; INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 2; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL POPULATION; CELL SIZE; LYMPHOCYTOPENIA; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STEM CELL; THYMOPOIESIS; THYMUS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD44; ANTIGENS, CD5; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOLOGIC MEMORY; INTERLEUKIN-2; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE COUNT; MICE; MICE, INBRED BALB C; MICE, SCID; PRECURSOR CELLS, T-LYMPHOID; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 78650343116     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20100598     Document Type: Article

References (55)

1. Apostolou, I., and H. von Boehmer. 2004. In vivo instruction of suppressor commitment in naive T cells. J. Exp. Med. 199:1401-1408. doi:10.1084/jem.20040249 (Pubitemid 38685731)
2. Azzam, H.S., A. Grinberg, K. Lui, H. Shen, E.W. Shores, and P.E. Love. 1998. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188:2301-2311. doi:10.1084/jem.188.12.2301 (Pubitemid 29028502)
3. Bell, E.B., and S.M. Sparshott. 1997. The peripheral T-cell pool: regulationby non-antigen induced proliferation? Semin. Immunol. 9:347-353. doi:10.1006/smim.1997.0092 (Pubitemid 28021492)
4. Bottomly, K., M. Luqman, L. Greenbaum, S. Carding, J. West, T. Pasqualini, and D.B. Murphy. 1989. A monoclonal antibody to murine CD45R distinguishes CD4 T cell populations that produce different cytokines. Eur. J. Immunol. 19:617-623. doi:10.1002/eji.1830190407 (Pubitemid 19152926)
5. Boursalian, T.E., J. Golob, D.M. Soper, C.J. Cooper, and P.J. Fink. 2004. Continued maturation of thymic emigrants in the periphery. Nat. Immunol. 5:418-425. doi:10.1038/ni1049 (Pubitemid 38500091)
6. Brossard, C., M. Semichon, A. Trautmann, and G. Bismuth. 2003. CD5 inhibits signaling at the immunological synapse without impairing its formation. J. Immunol. 170:4623-4629.
7. Budd, R.C., J.C. Cerottini, C. Horvath, C. Bron, T. Pedrazzini, R.C. Howe, and H.R. MacDonald. 1987. Distinction of virgin and memory T lymphocytes. Stable acquisition of the Pgp-1 glycoprotein concomitant with antigenic stimulation. J. Immunol. 138:3120-3129.
8. Croft, M., and C. Dubey. 1997. Accessory molecule and costimulation requirements for CD4 T cell response. Crit. Rev. Immunol. 17:89-118.
9. Dalloul, A. 2009. CD5: A safeguard against autoimmunity and a shield for cancer cells. Auto. Rev. 8:349-353. doi:10.1016/j.autrev.2008.11.007
10. Ernst, B., D.-S. Lee, J.M. Chang, J. Sprent, and C.D. Surh. 1999. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity. 11:173-181. doi:10.1016/S1074-7613(00)80092-8 (Pubitemid 29428810)
11. Eyrich, M., T. Croner, C. Leiler, P. Lang, P. Bader, T. Klingebiel, D. Niethammer, and P.G. Schlegel. 2002. Distinct contributions of CD4(+) and CD8(+) naive and memory T-cell subsets to overall T-cellreceptor repertoire complexity following transplantation of T-celldepleted CD34-selected hematopoietic progenitor cells from unrelated donors. Blood. 100:1915-1918. doi:10.1182/blood-2001-11-0005 (Pubitemid 34925175)
12. Fontenot, J.D., and A.Y. Rudensky. 2005. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6:331-337. doi:10.1038/ni1179 (Pubitemid 41716769)
13. Fontenot, J.D., M.A. Gavin, and A.Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4:330-336. doi:10.1038/ni904 (Pubitemid 36432314)
14. Freitas, A.A., and B.B. Rocha. 1993. Lymphocyte lifespans: homeostasis, selection and competition. Immunol. Today. 14:25-29. doi:10.1016/ 0167-5699(93)90320-K
15. Freitas, A.A., and B. Rocha. 2000. Population biology of lymphocytes: the flight for survival. Annu. Rev. Immunol. 18:83-111. doi:10.1146/annurev. immunol.18.1.83
16. Friedlein, G., F. El Hage, I. Vergnon, C. Richon, P. Saulnier, Y. Lécluse, A. Caignard, L. Boumsell, G. Bismuth, S. Chouaib, and F. Mami- Chouaib. 2007. Human CD5 protects circulating tumor antigenspecific CTL from tumor-mediated activation-induced cell death. J. Immunol. 178:6821-6827.
17. Ge, Q., H. Hu, H.N. Eisen, and J. Chen. 2002. Different contributions of thymopoiesis and homeostasis-driven proliferation to the reconstitution of naive and memory T cell compartments. Proc. Natl. Acad. Sci. USA. 99:2989-2994. doi:10.1073/pnas.052714099 (Pubitemid 34240573)
18. Goldrath, A.W., and M.J. Bevan. 1999. Low-affinity ligands for the TCR drive proliferation of mature CD8+ T cells in lymphopenic hosts. Immunity. 11:183-190. doi:10.1016/S1074-7613(00)80093-X (Pubitemid 29428811)
19. Goldrath, A.W., L.Y. Bogatzki, and M.J. Bevan. 2000. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J. Exp. Med. 192:557-564. doi:10.1084/jem.192.4.557 (Pubitemid 30666256)
20. Gorochov, G., A.U. Neumann, A. Kereveur, C. Parizot, T.S. Li, C. Katlama, M. Karmochkine, G. Raguin, B. Autran, and P. Debré. 1998. Perturbation of CD4+ and CD8+ T-cell repertoires during progression to AIDS and regulation of the CD4+ repertoire during antiviral therapy. Nat. Med. 4:215-221. doi:10.1038/nm0298-215 (Pubitemid 28137377)
21. Greenberg, P.D., and S.R. Riddell. 1999. Deficient cellular immunity-finding and fixing the defects. Science. 285:546-551. doi:10.1126/ science.285.5427.546
22. Han, M., L. Harrison, P. Kehn, K. Stevenson, J. Currier, and M.A. Robinson. 1999. Invariant or highly conserved TCR alpha are expressed on double-negative (CD3+CD4-CD8-) and CD8+ T cells. J. Immunol. 163:301-311.
23. Haribhai, D., W. Lin, B. Edwards, J. Ziegelbauer, N.H. Salzman, M.R. Carlson, S.H. Li, P.M. Simpson, T.A. Chatila, and C.B. Williams. 2009. A central role for induced regulatory T cells in tolerance induction in experimental colitis. J. Immunol. 182:3461-3468. doi:10.4049/ jimmunol.0802535
24. Jameson, S.C. 2002. Maintaining the norm: T-cell homeostasis. Nat. Rev. Immunol. 2:547-556.
25. Jonsson, R., K.A. Brokstad, T. Hansen, T. Davies, and E. Ulvestad. 2002. The evolution and breakdown of the immune system: implications for development of autoimmune diseases. Scand. J. Immunol. 56:323-326. doi:10.1046/j.1365-3083. 2002.01158.x (Pubitemid 35002038)
26. Jores, R., and T. Meo. 1993. Few V gene segments dominate the T cell receptor beta-chain repertoire of the human thymus. J. Immunol. 151:6110-6122.
27. Jorgensen, J.L., U. Esser, B. Fazekas de St Groth, P.A. Reay, and M.M. Davis. 1992. Mapping T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature. 355:224-230. doi:10.1038/355224a0
28. Kassiotis, G., R. Zamoyska, and B. Stockinger. 2003. Involvement of avidity for major histocompatibility complex in homeostasis of naive and memory T cells. J. Exp. Med. 197:1007-1016. doi:10.1084/jem.20021812 (Pubitemid 36523198)
29. Khattri, R., T. Cox, S.A. Yasayko, and F. Ramsdell. 2003. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4:337-342. doi:10.1038/ni909 (Pubitemid 36432315)
30. Kimmig, S., G.K. Przybylski, C.A. Schmidt, K. Laurisch, B. Möwes, A. Radbruch, and A. Thiel. 2002. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 195:789-794. doi:10.1084/jem.20011756 (Pubitemid 34259723)
31. Kirberg, J., N. Bosco, J.-C. Deloulme, R. Ceredig, and F. Agenès. 2008. Peripheral T lymphocytes recirculating back into the thymus can mediate thymocyte positive selection. J. Immunol. 181:1207-1214.
32. Kretschmer, K., I. Apostolou, D. Hawiger, K. Khazaie, M.C. Nussenzweig, and H. von Boehmer. 2005. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6:1219-1227. doi:10.1038/ni1265 (Pubitemid 43045633)
33. Lainscak, M., G.S. Filippatos, M. Gheorghiade, G.C. Fonarow, and S.D. Anker. 2008. Cachexia: common, deadly, with an urgent need for precise definition and new therapies. Am. J. Cardiol. 101:8E-10E. doi:10.1016 /j.amjcard.2008.02.065
34. Lee, W.T., X.M. Yin, and E.S. Vitetta. 1990. Functional and ontogenetic analysis of murine CD45Rhi and CD45Rlo CD4+ T cells. J. Immunol. 144:3288-3295.
35. Lyons, A.B., and C.R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods. 171:131-137. doi:10.1016/ 0022-1759(94)90236-4
36. Maraskovsky, E., M. Teepe, P.J. Morrissey, S. Braddy, R.E. Miller, D.H. Lynch, and J.J. Peschon. 1996. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J. Immunol. 157:5315-5323.
37. McMichael, A.J., and S.L. Rowland-Jones. 2001. Cellular immune responses to HIV. Nature. 410:980-987. doi:10.1038/35073658 (Pubitemid 32335849)
38. Miller, R.A., C. Chrisp, and A. Galecki. 1997. CD4 memory T cell levels predict life span in genetically heterogeneous mice. FASEB J. 11:775-783.
39. Min, B., H. Yamane, J. Hu-Li, and W.E. Paul. 2005. Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J. Immunol. 174:6039-6044.
40. Moses, C.T., K.M. Thorstenson, S.C. Jameson, and A. Khoruts. 2003. Competition for self ligands restrains homeostatic proliferation of naïve CD4 T cells. Proc. Natl. Acad. Sci. USA. 100:1185-1190. doi:10.1073/pnas. 0334572100 (Pubitemid 36183977)
41. Mucida, D., N. Kutchukhidze, A. Erazo, M. Russo, J.J. Lafaille, and M.A. Curotto de Lafaille. 2005. Oral tolerance in the absence of naturally occurring Tregs. J. Clin. Invest. 115:1923-1933. doi:10.1172/JCI24487 (Pubitemid 40979732)
42. Mueller, D.L., S. Seiffert, W. Fang, and T.W. Behrens. 1996. Differential regulation of bcl-2 and bcl-x by CD3, CD28, and the IL-2 receptor in cloned CD4+ helper T cells. A model for the long-term survival of memory cells. J. Immunol. 156:1764-1771.
43. Pannetier, C. 1993. The sizes of the CDR3 hypervariable regions of the murine T cell receptor beta chains vary as a function of the recombined germ-line segments. Proc. Natl. Acad. Sci. USA. 90:4319-4323. doi:10 .1073/pnas.90.9.4319
44. Pannetier, C., J. Even, and P. Kourilsky. 1995. T-cell repertoire diversity and clonal expansions in normal and clinical samples. Immunol. Today. 16:176-181. doi:10.1016/0167-5699(95)80117-0
45. Park, J.-H., Q. Yu, B. Erman, J.S. Appelbaum, D. Montoya-Durango, H.L. Grimes, and A. Singer. 2004. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity. 21:289-302.doi:10.1016/j.immuni.2004.07.016 (Pubitemid 39094057)
46. Strong, J., Q. Wang, and N. Killeen. 2001. Impaired survival of T helper cells in the absence of CD4. Proc. Natl. Acad. Sci. USA. 98:2566-2571. doi:10.1073/pnas.051329698 (Pubitemid 32209522)
47. Sudo, T., S. Nishikawa, N. Ohno, N. Akiyama, M. Tamakoshi, H. Yoshida, and S. Nishikawa. 1993. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc. Natl. Acad. Sci. USA. 90:9125-9129. doi:10.1073/pnas.90.19.9125 (Pubitemid 23306464)
48. Surh, C.D., B. Ernst, and J. Sprent. 1992. Growth of epithelial cells in the thymic medulla is under the control of mature T cells. J. Exp. Med. 176:611-616. doi:10.1084/jem.176.2.611
49. Swain, S.L. 1994. Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity. 1:543-552. doi:10.1016/1074-7613(94)90044-2 (Pubitemid 2156900)
50. Tan, J.T., E. Dudl, E. LeRoy, R. Murray, J. Sprent, K.I. Weinberg, and C.D. Surh. 2001. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl. Acad. Sci. USA. 98:8732-8737. doi:10.1073/pnas. 161126098 (Pubitemid 32678096)
51. Viret, C., F.S. Wong, and C.A. Janeway Jr. 1999. Designing and maintaining the mature TCR repertoire: the continuum of self-peptide: self-MHC complex recognition. Immunity. 10:559-568. doi:10.1016/S1074-7613(00)80055-2 (Pubitemid 29262658)
52. Wang, Z., C. Zhao, R. Moya, and J.D. Davies. 2008. A novel role for CD4+ T cells in the control of cachexia. J. Immunol. 181:4676-4684.
53. Williams, M.A., E.V. Ravkov, and M.J. Bevan. 2008. Rapid culling of the CD4+ T cell repertoire in the transition from effector to memory. Immunity. 28:533-545. doi:10.1016/j.immuni.2008.02.014
54. Wu, Z., S.J. Bensinger, J. Zhang, C. Chen, X. Yuan, X. Huang, J.F.Markmann, A. Kassaee, B.R. Rosengard, W.W. Hancock, et al. 2004. Homeostatic proliferation is a barrier to transplantation tolerance. Nat. Med. 10:87-92. doi:10.1038/nm965 (Pubitemid 38524703)
55. Zhao, C., Z. Wang, M.W. Robertson, and J.D. Davies. 2008. Cachexia in the non-obese diabetic mouse is associated with CD4+ T-cell lymphopenia. Immunology. 125:48-58. doi:10.1111/j.1365-2567.2008.02819.x