TOX Provides a Link between Calcineurin Activation and CD8 Lineage Commitment

Journal of Experimental Medicine

Volumn 199, Issue 8, 2004, Pages 1089-1099

  Aliahmad, Parinaz ^a   O'Flaherty, Emmett ^a   Han, Peggy ^a   Goularte, Olivia D ^a   Wilkinson, Beverley ^a   Satake, Masanobu ^b   Molkentin, Jeffery D ^c   Kaye, Jonathan ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Gene regulation; HMG box; Runx; T cell development; TCR signaling

Indexed keywords

CALCINEURIN; CD4 ANTIGEN; CD8 ANTIGEN; DNA; HIGH MOBILITY GROUP B PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN; NUCLEAR FACTOR; RNA; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DEMETHYLATION; FLOW CYTOMETRY; GENE CONTROL; GENE EXPRESSION; IMMUNOBLOTTING; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THYMOCYTE; UPREGULATION;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; BASE SEQUENCE; CALCINEURIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DNA PRIMERS; ENZYME ACTIVATION; GENE SILENCING; HMGB PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 2442597781     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20040051     Document Type: Article

References (64)

1. Starr, T.K., S.C. Jameson, and K.A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21: 139-176.
2. van Oers, N.S. 1999. T cell receptor-mediated signs and signals governing T cell development. Semin. Immunol. 11:227-237.
3. Kioussis, D., and W. Ellmeier. 2002. Chromatin and CD4, CD8A and CD8B gene expression during thymic differentiation. Nat. Rev. Immunol. 2:909-919.
4. Harker, N., T. Naito, M. Cortes, A. Hostert, S. Hirschberg, M. Tolaini, K. Roderick, K. Georgopoulos, and D. Kioussis. 2002. The CD8alpha gene locus is regulated by the Ikaros family of proteins. Mol. Cell. 10:1403-1415.
5. Taniuchi, I., M. Osato, T. Egawa, M.J. Sunshine, S.C. Bae, T. Komori, Y. Ito, and D.R. Littman. 2002. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell. 111: 621-633.
6. Chi, T.H., M. Wan, K. Zhao, I. Taniuchi, L. Chen, D.R. Littman, and G.R. Crabtree. 2002. Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes. Nature. 418:195-199.
7. Chi, T.H., M. Wan, P.P. Lee, K. Akashi, D. Metzger, P. Chambon, C.B. Wilson, and G.R. Crabtree. 2003. Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity. 19:169-182.
8. Gebuhr, T.C., G.I. Kovalev, S. Bultman, V. Godfrey, L. Su, and T. Magnuson. 2003. The role of Brg1, a catalytic subunit of mammalian chromatin-remodeling complexes, in T cell development. J. Exp. Med. 198:1937-1949.
9. Itano, A., P. Salmon, D. Kioussis, M. Tolaini, P. Corbella, and E. Robey. 1996. The cytoplasmic domain of CD4 promotes the development of CD4 lineage T cells. J. Exp. Med. 183:731-741.
10. Matechak, E.O., N. Killeen, S.M. Hedrick, and B.J. Fowlkes. 1996. MHC class II-specific T cells can develop in the CD8 lineage when CD4 is absent. Immunity. 4:337-347.
11. Sharp, L.L., D.A. Schwarz, C.M. Bott, C.J. Marshall, and S.M. Hedrick. 1997. The influence of the MAPK pathway on T cell lineage commitment. Immunity. 7:609-618.
12. Basson, M.A., U. Bommhardt, M.S. Cole, J.Y. Tso, and R. Zamoyska. 1998. CD3 ligation on immature thymocytes generates antagonist-like signals appropriate for CD8 lineage commitment, independently of T cell receptor specificity. J. Exp. Med. 187:1249-1260.
13. Yasutomo, K., C. Doyle, L. Miele, C. Fuchs, and R.N. Germain. 2000. The duration of antigen receptor signalling determines CD4+ versus CD8+ T-cell lineage fate. Nature. 404:506-510.
14. Hernandez-Hoyos, G., S.J. Sohn, E.V. Rothenberg, and J. Alberola-Ila. 2000. Lck activity controls CD4/CD8 T cell lineage commitment. Immunity. 12:313-322.
15. Watanabe, N., H. Arase, M. Onodera, P.S. Ohashi, and T. Saito. 2000. The quantity of TCR signal determines positive selection and lineage commitment of T cells. J. Immunol. 165: 6252-6261.
16. Wilkinson, B., and J. Kaye. 2001. Requirement for sustained MAPK signaling in both CD4 and CD8 lineage commitment: a threshold model. Cell. Immunol. 211:86-95.
17. Adachi, S., and M. Iwata. 2002. Duration of calcineurin and Erk signals regulates CD4/CD8 lineage commitment of thymocytes. Cell. Immunol. 215:45-53.
18. Shao, H., B. Wilkinson, B. Lee, P.C. Han, and J. Kaye. 1999. Slow accumulation of active mitogen-activated protein kinase during thymocyte differentiation regulates the temporal pattern of transcription factor gene expression. J. Immunol. 163:603-610.
19. Bommhardt, U., M.A. Basson, U. Krummrei, and R. Zamoyska. 1999. Activation of the extracellular signal-related kinase/mitogen-activated protein kinase pathway discriminates CD4 versus CD8 lineage commitment in the thymus. J. Immunol. 163:715-722.
20. Shao, H., D.H. Kono, L.Y. Chen, E.M. Rubin, and J. Kaye. 1997. Induction of the early growth response (Egr) family of transcription factors during thymic selection. J. Exp. Med. 185:731-744.
21. Bain, G., C.B. Cravatt, C. Loomans, J. Alberola-Ila, S.M. Hedrick, and C. Murre. 2001. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat. Immunol. 2:165-171.
22. Bettini, M., H. Xi, J. Milbrandt, and G.J. Kersh. 2002. Thymocyte development in early growth response gene 1-deficient mice. J. Immunol. 169:1713-1720.
23. Rivera, R.R., C.P. Johns, J. Quan, R.S. Johnson, and C. Murre. 2000. Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity. 12:17-26.
24. Gao, E.K., D. Lo, R. Cheney, O. Kanagawa, and J. Sprent. 1988. Abnormal differentiation of thymocytes in mice treated with cyclosporin A. Nature. 336:176-179.
25. Jenkins, M.K., R.H. Schwartz, and D.M. Pardoll. 1988. Effects of cyclosporine A on T cell development and clonal deletion. Science. 241:1655-1658.
26. Chan, V.S., C. Wong, and P.S. Ohashi. 2002. Calcineurin Aα plays an exclusive role in TCR signaling in mature but not in immature T cells. Eur. J. Immunol. 32:1223-1229.
27. Bueno, O.F., E.B. Brandt, M.E. Rothenberg, and J.D. Molkentin. 2002. Defective T cell development and function in calcineurin Aβ-deficient mice. Proc. Natl. Acad. Sci. USA. 99:9398-9403.
28. Hayden-Martinez, K., L.P. Kane, and S.M. Hedrick. 2000. Effects of a constitutively active form of calcineurin on T cell activation and thymic selection. J. Immunol. 165:3713-3721.
29. Crabtree, G.R., and E.N. Olson. 2002. NFAT signaling: choreographing the social lives of cells. Cell. 109:S67-S79.
30. Amasaki, Y., S. Adachi, Y. Ishida, M. Iwata, N. Arai, K. Arai, and S. Miyatake. 2002. A constitutively nuclear form of NFATx shows efficient transactivation activity and induces differentiation of CD4(+)CD8(+) T cells. J. Biol. Chem. 277:25640-25648.
31. Wilkinson, B., J.Y. Chen, P. Han, K.M. Rufner, O.D. Goularte, and J. Kaye. 2002. TOX: an HMG box protein implicated in the regulation of thymocyte selection. Nat. Immunol. 3:272-280.
32. Mombaerts, P., J. Iacomini, R.S. Johnson, K. Herrup, S. Tonegawa, and V.E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 68:869-877.
33. Shinkai, Y., G. Rathbun, K.P. Lam, E.M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A.M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 68: 855-867.
34. Mombaerts, P., A.R. Clarke, M.A. Rudnicki, J. Iacomini, S. Itohara, J.J. Lafaille, L. Wang, Y. Ichikawa, R. Jaenisch, M.L. Hooper, et al. 1992. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature. 360:225-231.
35. Grusby, M.J., H. Auchincloss, Jr., R. Lee, R.S. Johnson, J.P. Spencer, M. Zijlstra, R. Jaenisch, V.E. Papaioannou, and L.H. Glimcher. 1993. Mice lacking major histocompatibility complex class I and class II molecules. Proc. Natl. Acad. Sci. USA. 90:3913-3917.
36. Sha, W.C., C.A. Nelson, R.D. Newberry, D.M. Kranz, J.H. Russell, and D.Y. Loh. 1988. Positive and negative selection of an antigen receptor on T cells in transgenic mice. Nature. 336:73-76.
37. Kaye, J., M.L. Hsu, M.E. Sauron, S.C. Jameson, N.R. Gascoigne, and S.M. Hedrick. 1989. Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature. 341:746-749.
38. Murphy, K.M., A.B. Heimberger, and D.Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+ CD8+TCRlo thymocytes in vivo. Science. 250:1720-1723.
39. Hayashi, K., N. Abe, T. Watanabe, M. Obinata, M. Ito, T. Sato, S. Habu, and M. Satake. 2001. Overexpression of AML1 transcription factor drives thymocytes into the CD8 single-positive lineage. J. Immunol. 167:4957-4965.
40. Godfrey, D.I., J. Kennedy, T. Suda, and A. Zlotnik. 1993. A developmental pathway involving four phenotypically and functionally distinct subsets of CD3-CD4-CD8- triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J. Immunol. 150:4244-4252.
41. Fehling, H.J., A. Krotkova, C. Saint-Ruf, and H. von Boehmer. 1995. Crucial role of the pre-T-cell receptor alpha gene in development of alpha beta but not gamma delta T cells. Nature. 375:795-798.
42. Shinkai, Y., and F.W. Alt. 1994. CD3 epsilon-mediated signals rescue the development of CD4+CD8+ thymocytes in RAG-2-/- mice in the absence of TCR beta chain expression. Int. Immunol. 6:995-1001.
43. Carbone, A.M., P. Marrack, and J.W. Kappler. 1988. Demethylated CD8 gene in CD4+ T cells suggests that CD4+ cells develop from CD8+ precursors. Science. 242:1174-1176.
44. Pestano, G.A., Y. Zhou, L.A. Trimble, J. Daley, G.F. Weber, and H. Cantor. 1999. Inactivation of misselected CD8 T cells by CD8 gene methylation and cell death. Science. 284: 1187-1191.
45. Swat, W., M. Dessing, H. von Boehmer, and P. Kisielow. 1993. CD69 expression during selection and maturation of CD4+8+ thymocytes. Eur. J. Immunol. 23:739-746.
46. Ramsdell, F., M. Jenkins, Q. Dinh, and B.J. Fowlkes. 1991. The majority of CD4+8- thymocytes are functionally immature. J. Immunol. 147:1779-1785.
47. Sawada, S., J.D. Scarborough, N. Killeen, and D.R. Littman. 1994. A lineage-specific transcriptional silencer regulates CD4 gene expression during T lymphocyte development. Cell. 77:917-929.
48. Groves, T., M. Parsons, N.G. Miyamoto, and C.J. Guidos. 1997. TCR engagement of CD4+CD8+ thymocytes in vitro induces early aspects of positive selection, but not apoptosis. J. Immunol. 158:65-75.
49. Woolf, E., C. Xiao, O. Fainaru, J. Lotem, D. Rosen, V. Negreanu, Y. Bemstein, D. Goldenberg, O. Brenner, G. Berke, et al. 2003. Runx3 and Runx1 are required for CD8 T cell development during thymopoiesis. Proc. Natl. Acad. Sci. USA. 100:7731-7736.
50. Hayashi, K., W. Natsume, T. Watanabe, N. Abe, N. Iwai, H. Okada, Y. Ito, M. Asano, Y. Iwakura, S. Habu, et al. 2000. Diminution of the AML1 transcription factor function causes differential effects on the fates of CD4 and CD8 single-positive T cells. J. Immunol. 165:6816-6824.
51. D'Ambrosio, D., D.A. Cantrell, L. Frati, A. Santoni, and R. Testi. 1994. Involvement of p21ras activation in T cell CD69 expression. Eur. J. Immunol. 24:616-620.
52. Gounari, F., I. Aifantis, K. Khazaie, S. Hoeflinger, N. Harada, M.M. Taketo, and H. von Boehmer. 2001. Somatic activation of beta-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat. Immunol. 2:863-869.
53. Lee, P.P., D.R. Fitzpatrick, C. Beard, H.K. Jessup, S. Lehar, K.W. Makar, M. Perez-Melgosa, M.T. Sweetser, M.S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity. 15:763-774.
54. Adlam, M., and G. Siu. 2003. Hierarchical interactions control CD4 gene expression during thymocyte development. Immunity. 18:173-184.
55. Thomas, J.O., and A.A. Travers. 2001. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem. Sci. 26:167-174.
56. Bartfeld, D., L. Shimon, G.C. Couture, D. Rabinovich, F. Frolow, D. Levanon, Y. Groner, and Z. Shakked. 2002. DNA recognition by the RUNX1 transcription factor is mediated by an allosteric transition in the RUNT domain and by DNA bending. Structure (Camb). 10:1395-1407.
57. Wang, J.H., A. Nichogiannopoulou, L. Wu, L. Sun, A.H. Sharpe, M. Bigby, and K. Georgopoulos. 1996. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity. 5:537-549.
58. Winandy, S., L. Wu, J.H. Wang, and K. Georgopoulos. 1999. Pre-T cell receptor (TCR) and TCR-controlled checkpoints in T cell differentiation are set by Ikaros. J. Exp. Med. 190: 1039-1048.
59. Kim, J., S. Sif, B. Jones, A. Jackson, J. Koipally, E. Heller, S. Winandy, A. Viel, A. Sawyer, T. Ikeda, et al. 1999. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity. 10:345-355.
60. Brown, K.E., S.S. Guest, S.T. Smale, K. Hahm, M. Merkenschlager, and A.G. Fisher. 1997. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell. 91:845-854.
61. Wang, W., T. Chi, Y. Xue, S. Zhou, A. Kuo, and G.R. Crabtree. 1998. Architectural DNA binding by a high-mobility-group/kinesin-like subunit in mammalian SWI/SNF-related complexes. Proc. Natl. Acad. Sci. USA. 95:492-498.
62. O'Flaherty, E., and J. Kaye. 2003. TOX defines a conserved subfamily of HMG-box proteins. BMC Genomics. 4:13.
63. Travers, A.A. 2003. Priming the nucleosome: a role for HMGB proteins? EMBO Rep. 4:131-136.
64. Hernandez-Hoyos, G., M.K. Anderson, C. Wang, E.V. Rothenberg, and J. Alberola-Ila. 2003. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity. 19:83-94.