The JNK pathway regulates the in vivo deletion of immature CD4+CD8+ thymocytes

Journal of Experimental Medicine

Volumn 188, Issue 10, 1998, Pages 1817-1830

  Rincón, Mercedes ^a,b   Whitmarsh, Alan ^d   Yang, Derek D ^b,c,f   Weiss, Linda ^a   Dérijard, Benoit ^d,e   Jayaraj, Prash ^b   Davis, Roger J ^d   Flavell, Richard A ^b,c  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e CENTRE DE BIOCHIMIE   (France)

^f ELI LILLY AND COMPANY   (United States)

Author keywords

Apoptosis; JNK; T lymphocyte; Thymic development

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL SUBPOPULATION; DEVELOPMENT; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; THYMOCYTE; THYMUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD3; APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; GENE EXPRESSION REGULATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 4; MAP KINASE KINASE 7; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, T-CELL; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THYMUS GLAND;

EID: 0032538817     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.10.1817     Document Type: Article

References (69)

1. Fink, P.J., and M.J. Bevan. 1995. Positive selection of thymocytes. Adv. Immunol. 59:99-133.
2. Kisielow, P., and H. von Boehmer. 1995. Development and selection of T cells: facts and puzzles. Adv. Immunol. 58:87-209.
3. Nossal, G.J.V. 1994. Negative selection of lymphocytes. Cell. 76:229-239.
4. Whitmarsh, A.J., and R.J. Davis. 1996. Transcription factor AP-1: regulation by mitogen activated protein kinases signal transduction pathways. J. Mol. Med. 17:2360-2371.
5. Ip, Y.T., and R.J. Davis. 1998. Signal transduction by the c-Jun N-terminal kinase (JNK): from inflammation to development. Curr. Opin. Cell Biol. 10:205-219.
6. Su, B., E. Jacinto, M. Hibi, T. Kallunki, M. Karin, and Y. Ben-Neriah. 1994. JNK is involved in signal integration during costimulation of T lymphocytes. Cell. 77:727-736.
7. Crompton, T., K.C. Gilmour, and M.J. Owen. 1996. The MAP kinase pathway controls differentiation from double-negative to double-positive thymocytes. Cell. 86:243-251.
8. Alberola-Ila, J., K.A. Forbush, R. Seger, E.G. Krebs, and R.M. Perlmutter. 1995. Selective requirement for MAP kinase activation in thymocyte differentiation. Nature. 373: 620-623.
9. Swan, K.A., J. Alberola-Ila, J.A. Gross, M.W. Appleby, K.A. Forbush, J.F. Thomas, and R.M. Perlmutter. 1995. Involvement of p21ras distinguishes positive and negative selection in thymocytes. EMBO (Eur. Mol. Biol. Organ.) J. 14:276-285.
10. O'Shea, C.C., T. Crompton, I.R. Rosewell, A.C. Hayday, and M.J. Owen. 1996. Raf regulates positive selection. Eur. J. Immunol. 26:2350-2355.
11. Alberola-Ila, J., K.A. Hogquist, K.A. Swan, M.J. Bevan, and R.M. Perlmutter. 1996. Positive and negative selection invoke distinct signaling pathways. J. Exp. Med. 184:9-18.
12. + thymocytes. Proc. Natl. Acad. Sci. USA. 93: 4683-4687.
13. 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.
14. Sen, J., R. Kapeller, R. Fragoso, R. Sen, L.I. Zon, and S.J. Burakoff. 1996. Intrathymic signals in thymocytes are mediated by p38 mitogen-activated protein kinase. J. Immunol. 156:4535-4538.
15. Gupta, S., T. Barrett, A.J. Whitmarsh, J. Cavanagh, H.K. Sluss, B. Dérijard, and R.J. Davis. 1996. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO (Eur. Mol. Biol. Organ.) J. 15:2760-2770.
16. Yang, D.D., C.-Y. Kuan, A.J. Whitmarsh, M. Rincón, T.S. Zheng, R.J. Davis, P. Rakic, and R.A. Flavell. 1997. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature. 389:865-870.
17. Dérijard, B., J. Raingeaud, T. Barret, I.-H. Wu, J. Han, R.J. Ulevitch, and R.J. Davis. 1995. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science. 267:683-685.
18. Sánchez, I., R.T. Hughes, B.J. Mayer, K. Yee, J.R. Woodgett, J. Avruch, J.M. Kyriakis, and L.I. Zon. 1994. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature. 372:794-798.
19. Lin, A., A. Minden, H. Martinetto, F.-X. Claret, C. Lange-Carter, F. Mercurio, G.L. Johnson, and M. Karin. 1995. Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science. 268:286-290.
20. 2-terminal kinase. Proc. Natl. Acad. Sci. USA. 94:7337-7342.
21. Dérijard, B., M. Hibi, I.-H. Wu, T. Barret, B. Su, T. Deng, M. Karin, and R.J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell. 76:1025-1037.
22. Wildin, R.S., A.M. Garvin, S. Pawar, D.B. Lewis, K.M. Abraham, K.A. Forbush, S.F. Ziegler, J.M. Allen, and R.M. Perlmutter. 1991. Developmental regulation of lck gene expression in T lymphocytes. J. Exp. Med. 173:383-393.
23. Brinster, R.L., J.M. Allen, R.R. Behringer, R.E. Gelinas, and R.D. Palmiter. 1988. Introns increase transcriptional efficiency in transgenic mice. Proc. Natl. Acad. Sci. USA. 85: 836-840.
24. Hogan, B., F. Constantini, and E. Lacy. 1986. Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 332 pp.
25. Rincón, M., and R.A. Flavell. 1994. AP-1 transcriptional activity requires both T-cell receptor-mediated and co-stimulatory signals in primary T lymphocytes. EMBO (Eur. Mol. Biol. Organ.) J. 13:4370-4381.
26. + T cells to effector Th1 and Th2 cells. Genes Funct. 1:51-68.
27. Favaloro, J., R. Freisman, and R. Kamen. 1980. Transcription maps of polyoma virus specific mRNA. Analysis by two dimensional nucleases S1 gel mapping. Methods Enzymol. 65:718.
28. Raingeaud, J., S. Gupta, J. Roger, M. Dickens, J. Han, R.J. Ulevitch, and R.J. Davis. 1995. Pro-inflammatory cytokines and environmental stress cause p38 MAP kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270:7420-7426.
29. 2 and the increase of intracellular cAMP inhibit the expression of interleukin 2 receptors in human T cells. Eur. J. Immunol. 18:1791-1796.
30. Liener, I.E., N. Sharon, and I.J. Goldstein. 1986. The Lectins: Properties, Functions and Applications in Biology and Medicine. Academic Press LTD, London. 600 pp.
31. + thymocytes. J. Immunol. 151:1868-1880.
32. + thymocytes by T cell receptor-induced apoptosis requires a costimulatory signal that can be provided by CD28. J. Exp. Med. 179:709-713.
33. Kishimoto, H., Z.C. Cai, A. Brunmark, M.R. Jackson, P.A. Peterson, and J. Sprent. 1996. Differing roles for B7 and intercellular adhesion molecules-1 in negative selection of thymocytes. J. Exp. Med. 184:531-537.
34. Kishimoto, H., and J. Sprent. 1997. Negative selection in the thymus includes semimature T cells. J. Exp. Med. 185:263-271.
35. Kishimoto, H., C.D. Surh, and J. Sprent. 1995. Upregulation of surface markers on dying thymocytes. J. Exp. Med. 181: 649-655.
36. Smith, C.A., G.T. Williams, R. Kingston, E.J. Jenkinson, and J.J. Owen. 1989. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature. 337:181-184.
37. Shi, Y.F., R.P. Bissonnette, N. Parfrey, M. Szalay, R.T. Kubo, and D.R. Green. 1991. In vivo administration of monoclonal antibodies to the CD3 T cells receptor complex induces cell death (apoptosis) in immature thymocytes. J. Immunol. 146:3340-3346.
38. + lymphocytes in embryonic thymus organ cultures. Immunology. 63:639-642.
39. Lee, S.L., R.L. Wesselschmidt, G.P. Linette, O. Kanagawa, J.H. Russell, and J. Milbrandt. 1995. Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nurr77). Science. 269:532-534.
40. Field, S.J., F.-Y. Tsai, F. Kuo, D.M. Livingston, S.H. Orkin, and M.E. Greenberg. 1996. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell. 85:549-561.
41. Rincón, M., and R.A. Flavell. 1996. Regulation of AP-1 and NFAT transcription factors during thymic selection of T cells. Mol. Cell. Biol. 16:1074-1084.
42. Huang, C., W.-Y. Ma, M. Dawson, M. Rincón, R.A. Flavell, and Z. Dong. 1997. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc. Natl. Acad. Sci. USA. 94:5826-5830.
43. + T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature. 341:746-749.
44. Renno, T., M. Hahne, J. Tschopp, and R. MacDonald. 1996. Peripheral T cells undergoing superantigen-induced apoptosis in vivo express B22O and upregulate Fas and Fas ligand. J. Exp. Med. 183:431-437.
45. Xia, Z., M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinase on apoptosis. Science. 270:1326-1331.
46. Rincón, M., H. Enslen, J. Raingeaud, M. Recht, T. Zapton, M.S.-S. Su, L.A. Penix, R.J. Davis, and R.A. Flavell. 1998. Interferon-γ expression by Th1 effector T cells mediated by the p38 MAP kinase signaling pathway. EMBO (Eur. Mol. Biol. Organ.) J. 17:2817-2829.
47. Ohashi, P.S., H. Pircher, K. Burki, R.M. Zinkernagel, and H. Hengartner. 1990. Distinct sequence of negative or positive selection implied by thymocytes T cell-receptor densities. Nature. 346:861-863.
48. Allen, P.M. 1994. Peptides in positive and negative selection: a delicate balance. Cell. 76:593-596.
49. + thymocytes by T-cell receptor peptide antagonists. Proc. Natl. Acad. Sci. USA. 91:4057-4061.
50. Vasquez, N.J., L.P. Kane, and S.M. Hedrick. 1994. Intracellular signals that mediate thymic negative selection. Immunity. 1:45-56.
51. + thymocytes negative selection. J. Immunol. 156:4594-4601.
52. + thymocytes undergoing thymic selection: requirement of calcineurin activation for thymic positive selection but not negative selection. J. Exp. Med. 181:927-941.
53. Page, D.M., L.P. Kane, T.M. Onami, and S.M. Hedrick. 1996. Cellular and biochemical requirements for thymocyte negative selection. Semin. Immunol. 8:69-82.
54. Turner, M., J. Mee, A.E. Walters, M.E. Quinn, A.L. Mellor, R. Zamoyska, and V.L.J. Tybulewicz. 1997. A requirement for the Rho-family GTP exchange factor Vav in positive and negative selection of thymocytes. Immunity. 7:451-460.
55. Katzav, L.P., D. Martin-Zanca, and M. Barbacid. 1989. Vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells. EMBO. (Eur. Mol. Biol. Organ.) J. 8:2283-2290.
56. Adams, J.M., H. Houston, J. Allen, T. Lints, and R. Harvey. 1992. The hematopoietically expressed vav proto-oncogene shares homology with the dbl GDP-GTP exchange factor, the bcr gene and a yeast gene (CDC42) involved in cytoskeletal organization. Oncogene. 7:611-618.
57. Boguski, M.S., A. Bairoch, T.K. Attwood, and G.S. Michaels. 1992. Proto-vav and gene expression. Nature. 358:113.
58. Crespo, P., X.R. Bustelo, D.S. Aaronson, O.A. Coso, M. López-Barahona, M. Barbacid, and J.S. Gutkind. 1996. Rac-1 dependent stimulation of the JNK/SAPK signaling pathway by Vav. Oncogene. 13:455-460.
59. Teramoto, H., P. Salem, K.C. Robbins, X.R. Bustelo, and J.S. Gutkind. 1997. Tyrosine phosphorylation of the vav proto-oncogene product links FcReRI to the Racl-JNK pathway. J Biol. Chem. 272:10751-10755.
60. Nishina, H., K.D. Fischer, L. Radvanyl, A. Shahinian, R. Haken, E.A. Rubie, A. Bernstein, T.W. Mak, J.R. Woodgett, and J.M. Penninger. 1997. Stress-signaling kinase Sek i protects thymocytes from apoptosis mediated by CD95 and CD3. Nature. 385:350-353.
61. 2 terminal kinase activation, and defects in AP-1 transcriptional activity. Proc. Natl. Acad. Sci. USA. 94:3004-3009.
62. Swat, W., K. Fujikawa, S. Ganiatsas, D.D. Yang, R.J. Xavier, N.L. Harris, L. Davidson, R. Ferrini, R.J. Davis, M.A. Labow, et al. 1998. SEK1/MKK4 is required for maintenance of a normal peripheral lymphoid compartment but not for T lymphocyte development. Immunity. 8:625-634.
63. Jones, L.A., D.J. Izon, J.D. Nieland, P.S. Linsley, and A.M. Kruisbeek. 1993. CD28-B7 interactions are not required for intrathymic clonal deletion. Int. Immunol. 5:503-512.
64. + thymocytes. J. Immunol. 149:3217-3224.
65. Amakawa, R., A. Hakem, T. Kundig, T. Matsuyama, J.J. Simard, E. Timms, A. Wakeham, H.W. Mittruecker, H. Griesser, H. Takimoto, et al. 1996. Impaired negative selection of T cells in Hodgkin's disease antigen CD30-deficient mice. Cell. 84:551-562.
66. Foy, T.M., D.M. Page, T.J. Waldschmidt, A. Schoneveld, J.D. Laman, S.R. Masters, L. Tygrett, J.A. Ledbetter, A. Aruffo, E. Claassen, et al. 1995. An essential role for gp39, the ligand for CD40 in thymic selection. J. Exp. Med. 182: 1377-1388.
67. Castro, J.E., J.A. Listman, B.A. Jacabson, Y. Wang, P.A. Lopez, S. Ju, P.W. Finn, and D.L. Perkins. 1996. Fas modulation of apoptosis during negative selection of thymocytes. Immunity. 5:617-627.
68. Verheij, M., R. Bose, X.-H. Lin, B. Yao, W.D. Jarvis, S. Grant, M.J. Birrer, E. Szabo, L.I. Zon, J.M. Kyriakis, et al. 1996. Requirement for ceramide-initiated SAPK/JNK signaling in stress-induced apoptosis. Nature. 380:75-79.
69. Chen, Y.R., C.F. Meyer, and T.-H. Tan. 1996. Persistent activation of c-Jun N-terminal kinase JNK1 in γ-radiation-induced apoptosis. J. Biol. Chem. 271:631-634.