Activation of p38 mitogen-activated protein kinase in vivo selectively induces apoptosis of CD8+ but not CD4+ T cells

Molecular and Cellular Biology

Volumn 20, Issue 3, 2000, Pages 936-946

  Merritt, Chris ^a   Enslen, Hervé ^b   Diehl, Nicole ^a   Conze, Dietrich ^a   Davis, Roger J ^b   Rincón, Mercedes ^a,c  

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

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRESS; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; LYMPH NODES; LYMPHOCYTE ACTIVATION; MAP KINASE KINASE 6; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN;

EID: 0033977922     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.3.936-946.2000     Document Type: Article

References (65)

1. Billiau, A. 1996. Interferon-g: biology and role in pathogenesis. Adv. Immunol. 62:61-130.
2. Boothby, M. R., A. L. Mora, D. C. Scherer, J. A. Brockman, and D. W. Ballard. 1997. Perturbation of the T lymphocyte lineage in transgenic mice expressing a constitutive repressor of nuclear factor(NF)-kappaB. J. Exp. Med. 185:1897-1907.
3. + T cells. J. Exp. Med. 189:1355-1360.
4. Chao, D. T., and S. J. Korsmeyer. 1998. Bcl-2 family: regulators of cell death. Ann. Rev. Immunol. 16:395-419.
5. Cheng, E. H., D. G. Kirsch, R. J. Clem, R. Ravi, M. B. Kastan, A. Bedi, K. Ueno, and J. M. Hardwick. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278:1966-1968.
6. Deak, M., A. D. Clifton, L. M. Lucocq, and D. R. Alessi. 1998. Mitogen-and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 17:4426-4441.
7. 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.
8. Dérijard, B., J. Rainjeaud, 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.
9. Diehl, N. L., H. Enslen, K. A. Fortner, C. Merrit, N. Stetson, C. Charland, R. A. Flavell, R. J. Davis, and M. Rincón. Activation of the p38 MAP kinase pathway arrests cell cycle progression and differentiation of immature thymocytes in vivo. J. Exp. Med., in press.
10. Dimmeler, S., K. Breitschopf, J. Haendeler, and A. M. Zeiher. 1999. Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteosome pathway. J. Exp. Med. 189: 1815-1822.
11. Faris, M., N. Kokot, K. Latinis, S. Kasibhatla, D. R. Green, G. A. Koretzky, and A. Nel. 1998. The c-Jun N-terminal kinase cascade plays a role in stress-induced apoptosis in Jurkat cells by up-regulating Fas ligand expression. J. Immunol. 160:134-144.
12. Fauci, A. S. 1993. Multifactorial nature of human immunodeficiency virus disease: implications for therapy. Science 262:1011-1018.
13. Foltz, I. N., J. C. Lee, P. R. Young, and J. W. Schrader. 1997. Hemopoietic growth factors with the exception of interleukin-4 activate the p38 mitogen-activated protein kinase pathway. J. Biol. Chem. 272:3296-3301.
14. Freshney, N. W., L. Rawlinson, F. Guesdun, E. Jones, S. Cowley, J. Hsuan, and J. Saklatvala. 1994. Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of the Hsp27. Cell 78:1039-1049.
15. Fukunaga, R., and T. Hunter. 1997. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J. 16:1921-1933.
16. Gratiot-Deans, J., L. Ding, L. A. Turka, and G. Nuñez. 1993. bcl-2 proto-oncogene expression during human T cell development. Evidence for biphasic regulation. J. Immunol. 151:83-91.
17. Grillot, D. A., R. Merino, and G. Nuñez. 1995. Bcl-XL displays restricted distribution during T cell development and inhibits multiple forms of apoptosis but not clonal deletion in transgenic mice. J. Exp. Med. 182:1973.
18. Han, J., Y. Jian, Z. Li, V. V. Kravchenko, and R. J. Ulevitch. 1997. Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386:296-299.
19. Han, J., J.-D. Lee, L. Bibbs, and R. J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265:808-811.
20. Han, J., J.-D. Lee, Y. Jiang, Z. Li, L. Feng, and R. J. Ulevitch. 1996. Characterization of the structure and function of a novel MAP kinases kinases (MKK6). J. Biol. Chem. 271:2886-2891.
21. + T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395:189-194.
22. Hockenbery, D. M., M. Zutter, W. Hickey, M. Nahm, and S. J. Korsmeyer. 1991. Bcl-2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc. Natl. Acad. Sci. USA 88:6961-6965.
23. Huang, S., Y. Jiang, Z. Li, E. Nishida, P. Mathias, S. Lin, R. J. Ulevitch, G. R. Nemerow, and J. Han. 1997. Apoptosis signaling pathway in T cells is composed of ICE/Ced-3 family proteases and MAP kinase kinase 6b. Immunity 6:739-749.
24. Johnson, B. W., and L. H. Boise. 1999. Bcl-2 and caspase inhibition cooperate to inhibit tumor necrosis factor-α-induced cell death in a Bcl-2 cleavage-independent fashion. J. Biol. Chem. 274:18552-18558.
25. Kamogawa, Y., L-A. E. Minasi, S. Carding, K. Bottomry, and R. A. Flavell. 1993. The relationship of IL-4 and IFNγ-producing T cells studied by lineage ablation of IL-4-producing cells. Cell 75:985-995.
26. Kasibhatla, S., T. Brunner, L. Genestier, F. Echeverri, A. Mahboubi, and D. R. Green. 1998. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol. Cell 1:543-541.
27. Kihara-Negishl, F., T. Yamada, Y. Kubota, N. Kondoh, H. Yamamoto, M. Abe, T. Shirai, Y. Hashimoto, and T. Oikawa. 1998. Down-regulation of c-myc and bcl-2 gene expression in PU.1-induced apoptosis in murine erythroleukemia cells. Int. J. Cancer 76:523-530.
28. Kirsch, D. G., A. Doseff, B. N. Chau, D.-S. Lim, N. C. de Souza-Pinto, R. Hansford, M. B. Kastan, Y. A. Lazebnik, and J. M. Hardwick. 1999. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochorme c. J. Biol. Chem. 274:21155-21161.
29. Lee, J. C., T. Laydon, P. C. McDonnell, T. F. Gallagher, S. Kumar, D. Gree, D. McNulty, M. J. Blumenthal, J. R. Heys, S. W. Landvatter, J. E. Strickler, M. M. McLaughlin, I. R. Siemens, S. M. Fisher, G. P. Livi, J. R. White, J. L. Adams, and P. R. Young. 1994. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372:739-746.
30. Los, M., S. Wesselborg, and K. Schulze-Osthoff. 1999. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10:629-639.
31. Lu, H. T., D. D. Yang, M. Wysk, E. Gatti, I. Mellman, R. J. Davis, and R. A. Flavell. 1999. Defective IL-12 production in mitogen-activated protein (MAP) kinase kinase 3 (Mkk3)-deficient mice. EMBO J. 18:1845-1857.
32. Ma, A., J. C. Pena, B. Chang, E. Margosian, L. Davidson, F. W. Alt, and C. B. Thompson. 1995. Bclx regulates the survival of double-positive thymocytes. Proc. Natl. Acad. Sci. USA 92:4763-4767.
33. Margolick, J. B., A. Muñoz, A. D. Donnenberg, L. P. Park, N. Galai, J. V. Giorgi, M. R. O'Gorman, and J. Ferbas. 1995. Failure of T-cell homeostasis preceding AIDS in HIV-1 infection. The Multicenter AIDS Cohort Study. Nat. Med. 1:674-680.
34. McLaughlin, M. M., S. Kurnar, P. C. McDonnell, S. Van Horn, J. C. Lee, G. P. Livi, and P. R. Young. 1996. Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J. Biol. Chem. 271:8488-8492.
35. Moriguchi, T., N. Kuroyanigi, K. Yamaguchi, Y. Gotoh, K. Irie, T. Kano, K. Shirakabe, Y. Muro, H. Shibuya, K. Matsumoto, B. Nishida, and M. Hagiwara. 1996. A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3. J. Biol. Chem. 271:13675-13679.
36. Makayama, K., I. Negishi, K. Kuida, H. Sawa, and D. Y. Loh. 1994. Targeted disruption of Bcl-2 αβ in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc. Natl. Acad. Sci. USA 91:3700-3704.
37. New, L., Y. Jiaag, M. Zhao, K. Liu, W. Zhu, L. J. Flood, Y. Kato, G. C. Parry, and J. Han. 1998. PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J. 17:3372-3384.
38. Nosaka, T., J. M. van Deursen, R. A. Tripp, W. E. Thieifelder, B. A. Witthuhn, A. P. McMickle, P. C. Doherty, G. C. Grosveld, and J. N. Ihle. 1995. Defective lymphoid development in mice lacking Jak3. Science 270: 800-802.
39. Oltvai, Z. N., C. L. Milliman, and S. J. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619.
40. Park, S. Y., K. Saijo, T. Takahashi, M. Osawa, H. Arase, N. Hirayama, K. Miyake, H. Nakauchi, T. Shirasawa, and T. Saito. 1995. Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity 3:771-782.
41. 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.
42. Raingeaud, J., A. J. Whitmarsh, T. Barret, B. Dérijard, and R. J. Devis. 1996. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol. 16:1247-1255.
43. + T cells. J. Exp. Med. 185:461-469.
44. + T-cells into effector Th1 and Th2 cells. Genes Funct. 1:51-68.
45. 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 J. 17:2817-2829.
46. Robey, E., D. Chang, A. Itano, D. Cado, H. Alesander, D. Lans, G. Weinmaster, and P. Salmon. 1996. An activated form of Notch influences the choice between CD4 and CD8 T cell lineages. Cell 87:483-492.
47. Rouse, J., P. Cohen, S. Trigon, M. Morange, A. Alonso-Llamazares, D. Zamanillo, T. Hunt, and A. R. Nebreda. 1994. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78:1027-1037.
48. Schnittman, S. M., and A. S. Fauci. 1994. Human immunodeficiency virus and acquired immunodeficiency syndrome: an update. Adv. Intern. Med. 39:305-355.
49. 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.
50. + T cells proliferation and lead to the amplification in vivo of cytotoxic T cell responses. J. Exp. Med. 186:47-55.
51. Sohn, S. J., K. A. Forbush, N. Nguyen, B. Witthuhn, T. Nosoka, J. N. Ihle, and R. M. Perlmutter. 1998. Requirement for Jak3 in mature T cells: its role in regulation of T cell homeostasis. J. Immunol. 160:2130-2138.
52. Sugawara, T., T. Moriguchi, E. Nishida, and Y. Takahama. 1998 Differential roles of ERK and p38 MAP kinase pathways in positive and negative selection of T lymphocytes. Immunity 9:565-574.
53. Suzuki, I, and P. J. Fink. 1998. Maximal proliferation of cytotoxic T lymphocytes requires reverse signaling through Fas ligand. J. Exp. Med. 187: 123-128.
54. Thomis, D. C., C. B. Gurniak, E. Tivol, A. H. Sharpe, and L. J. Berg. 1995. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 270:794-797.
55. Tong, L., S. Pav, D. M. White, S. Rogers, K. M. Crane, C. L. Cywin, M. L. Brown, and C. A. Pargellis. 1997. A highly specific inhibitor of human p38 MAP kinase binds in the ATP pocket. Nat. Struct. Biol. 4:311-316.
56. Veis, D. J., C. L. Sentman, E. A. Bach, and S. J. Korsmeyer. 1993. Expression of the Bcl-2 protein in murine and human thymocytes and in peripheral T lymphocytes. J. Immunol. 151:2546-2554.
57. Wang, X.-Z., and D. Ron. 1996. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP kinase. Science 272:1347-1349.
58. Waskiewicz, A. J., A. Flynn, C. G. Proud, and J. A. Cooper. 1997. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J. 16:1909-1920.
59. Whitmarsh, A. J., S. H. Yang, M. S. Su, A. D. Sharrocks, and R. J. Davis. 1997. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol. Cell. Biol. 17:2360-2371.
60. 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.
61. Wilson, K. P., P. G. McCaffrey, K. Hsiao, S. Pazhanisamy, V. Galullo, G. W. Bemis, M. J. Fitzgibbon, P. R. Caron, M. A. Murcko, and M. S. Su. 1997. The structural basis for the specificity of pyridinylimidazole inhibitors of p38 MAP kinase. Chem. Biol. 4:423-431.
62. Wysk, M., D. D. Yang, H. T. Lu, R. A. Flavell, and R. J. Davis. 1999. Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for tumor necrosis factor-induced cytokine expression. Proc. Natl. Acad. Sci. USA 96:3763-3768.
63. 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.
64. 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 Jacking the Jnk3 gene. Nature 389: 865-870.
65. Young, P. R., M. M. McLaughlin, S. Kumar, S. Kassis, M. L. Doyle, D. McNulty, T. F. Gallagher, S. Fisher, P. C. McDonnell, S. A. Carr, M. J. Huddleston, G. Seibel, T. G. Porter, G. P. Livi, J. L. Adams, and J. C. Lee. 1997. Pyridinyl imidazole inhibitors of p38 mitogen-activated protein kinase bind in the ATP site. J. Biol. Chem. 272:12116-12121.