Thymocyte negative selection is mediated by protein kinase C- and Ca 2+-dependent transcriptional induction of Bim of cell death

Journal of Immunology

Volumn 176, Issue 4, 2006, Pages 2299-2306

  Canté Barrett, Kirsten ^a   Gallo, Elena M ^a   Winslow, Monte M ^a   Crabtree, Gerald R ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; BIM PROTEIN; CALCINEURIN; CALCIUM; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; IONOMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN BCL 2; PROTEIN KINASE C; STRESS ACTIVATED PROTEIN KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL SURVIVAL; CONTROLLED STUDY; FLOW CYTOMETRY; IC 50; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RIBONUCLEASE PROTECTION ASSAY; T LYMPHOCYTE; THYMOCYTE; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 32044471627     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.4.2299     Document Type: Article

References (64)

1. Jessell, T. M. 2000. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1: 20-29.
2. Muller, B., B. Hartmann, G. Pyrowolakis, M. Afflolter, and K. Basler. 2003. Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113: 221-233.
3. Bouillet, P., J. F. Purton, D. I. Godfrey, L. C. Zhang, L. Coultas, H. Puthalakath, M. Pellegrini, S. Cory, J. M. Adams, and A. Strasser. 2002. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 415: 922-926.
4. O'Connor, L., A. Strasser, L. A. O'Reilly, G. Hausmann, J. M. Adams, S. Cory, and D. C. Huang. 1998. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17: 384-395.
5. Bouillet, P., S. Cory, L. C. Zhang, A. Strasser, and J. M. Adams. 2001. Degenerative disorders caused by Bcl-2 deficiency prevented by loss of its BH3-only antagonist Bim. Dev. Cell 1: 645-653.
6. Bouillet, P., D. Metcalf, D. C. Huang, D. M. Tarlinton, T. W. Kay, F. Kontgen, J. M. Adams, and A. Strasser. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286: 1735-1738.
7. Starr, T. K., S. C. Jameson, and K. A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21: 139-176.
8. Mombaerts, P., S. J. Anderson, R. M. Perlmutter, T. W. Mak, and S. Tonegawa. 1994. An activated lck transgene promotes thymocyte development in RAG-1 mutant mice. Immunity 1: 261-267.
9. Negishi, I., N. Motoyama, K. Nakayama, S. Senju, S. Hatakeyama, Q. Zhang, A. C. Chan, and D. Y. Loh. 1995. Essential role for ZAP-70 in both positive and negative selection of thymocytes. Nature 376: 435-438.
10. Schaeffer, E. M., C. Broussard, J. Debnath, S. Anderson, D. W. McVicar, and P. L. Schwartzberg. 2000. Tec family kinases modulate thresholds for thymocyte development and selection. J. Exp. Med. 192: 987-1000.
11. Pivniouk, V., E. Tsitsikov, P. Swinton, G. Rathbun, F. W. Alt, and R. S. Geha. 1998. Impaired viability and profound block in thymocyte development in mice lacking the adaptor protein SLP-76. Cell 94: 229-238.
12. Sommers, C. L., J. Lee, K. L. Steiner, J. M. Gurson, C. L. Depersis, D. El-Khoury, C. L. Fuller, E. W. Shores, P. E. Love, and L. E. Samelson. 2005. Mutation of the phospholipase C-γ1-binding site of LAT affects both positive and negative thymocyte selection. J. Exp. Med. 201: 1125-1134.
13. Turner, M., P. J. Mee, A. E. Walters, M. E. Quinn, A. L. Mellor, R. Zamoyska, and V. L. Tybulewicz. 1997. A requirement for the Rho-family GTP exchange factor Vav in positive and negative selection of thymocytes. Immunity 7: 451-460.
14. Neilson, J. R., M. M. Winslow, E. M. Hur, and G. R. Crabtree. 2004. Calcineurin B1 is essential for positive but not negative selection during thymocyte development. Immunity 20: 255-266.
15. Costello, P. S., R. H. Nicolas, Y. Watanabe, I. Rosewell, and R. Treisman. 2004. Ternary complex factor SAP-1 is required for Erk-mediated thymocyte positive selection. Nat. Immunol. 5: 289-298.
16. 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 1: 609-618.
17. Pages, G., S. Guerin, D. Grall, F. Bonino, A. Smith, F. Anjuere, P. Auberger, and J. Pouyssegur. 1999. Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice. Science 286: 1374-1377.
18. 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.
19. 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.
20. Fischer, A. M., C. D. Katayama, G. Pages, J. Pouyssegur, and S. M. Hedrick. 2005. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 23: 431-443.
21. Rathmell, J. C., T. Lindsten, W. X. Zong, R. M. Cinalli, and C. B. Thompson. 2002. Deficiency in Bak and Bax perturbs thymic selection and lymphoid homeostasis. Nat. Immunol. 3: 932-939.
22. Strasser, A. 2005. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5: 189-200.
23. Enders, A., P. Bouillet, H. Puthalakath, Y. Xu, D. M. Tarlinton, and A. Strasser. 2003. Loss of the pro-apoptotic BH3-only Bcl-2 family member Bim inhibits BCR stimulation-induced apoptosis and deletion of autoreactive B cells. J. Exp. Med. 198: 1119-1126.
24. Hildeman, D. A., Y. Zhu, T. C. Mitchell, P. Bouillet, A. Strasser, J. Kappler, and P. Marrack. 2002. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity 16: 759-767.
25. Dijkers, P. F., R. H. Medema, J. W. Lammers, L. Koenderman, and P. J. Coffer. 2000. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr. Biol. 10: 1201-1204.
26. Gilley, J., P. J. Coffer, and J. Ham. 2003. FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol. 162: 613-622.
27. Puthalakath, H., D. C. Huang, L. A. O'Reilly, S. M. King, and A. Strasser. 1999. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3: 287-296.
28. Seward, R. J., P. D. von Haller, R. Aebersold, and B. T. Huber. 2003. Phosphorylation of the pro-apoptotic protein Bim in lymphocytes is associated with protection from apoptosis. Mol. Immunol. 39: 983-993.
29. + thymocyte negative selection. J. Immunol. 156: 4594-4601.
30. McConkey, D. J., P. Hartzell, J. F. Amador-Perez, S. Orrenius, and M. Jondal. 1989. Calcium-dependent killing of immature thymocytes by stimulation via the CD3/T cell receptor complex. J. Immunol. 143: 1801-1806.
31. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
32. Purbhoo, M. A., D. J. Irvine, J. B. Huppa, and M. M. Davis. 2004. T cell killing does not require the formation of a stable mature immunological synapse. Nat. Immunol. 5: 524-530.
33. U. M., T. Miyashita, Y. Shikama, K. Tadokoro, and M. Yamada. 2001. Molecular cloning and characterization of six novel isoforms of human Bim, a member of the proapoptotic Bcl-2 family. FEBS Lett. 509: 135-141.
34. Marani, M., T. Tenev, D. Hancock, J. Downward, and N. R. Lemoine. 2002. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol. Cell. Biol. 22: 3577-3589.
35. Wang, Z., M. H. Malone, H. He, K. S. McColl, and C. W. Distelhorst. 2003. Microarray analysis uncovers the induction of the proapoptotic BH3-only protein Bim in multiple models of glucocorticoid-induced apoptosis. J. Biol. Chem. 278: 23861-23867.
36. Bunin, A., F. W. Khwaja, and G. J. Kersh. 2005. Regulation of Bim by TCR signals in CD4/CD8 double-positive thymocytes. J. Immunol. 175: 1532-1539.
37. Biswas, S. C., and L. A. Greene. 2002. Nerve growth factor (NGF) down-regulates the Bcl-2 homology 3 (BH3) domain-only protein Bim and suppresses its proapoptotic activity by phosphorylation. J. Biol. Chem. 277: 49511-49516.
38. Basson, M. A., T. J. Wilson, G. A. Legname, N. Sarner, P. D. Tomlinson, V. L. Tybulewicz, and R. Zamoyska. 2000. Early growth response (Egr)-1 gene induction in the thymus in response to TCR ligation during early steps in positive selection is not required for CD8 lineage commitment. J. Immunol. 165: 2444-2450.
39. Sharp, L. L., and S. M. Hedrick. 1999. Commitment to the CD4 lineage mediated by extracellular signal-related kinase mitogen-activated protein kinase and lck signaling. J. Immunol. 163: 6598-6605.
40. 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.
41. Truneh, A., F. Albert, P. Golstein, and A. M. Schmitt-Verhulst. 1985. Early steps of lymphocyte activation bypassed by synergy between calcium ionophores and phorbol ester. Nature 313: 318-320.
42. Toullec, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Boursier, F. Loriolle, et al. 1991. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C J. Biol. Chem. 266: 15771-15781.
43. Gschwendt, M., S. Dieterich, J. Rennecke, W. Kittstein, H. J. Mueller, and F. J. Johannes. 1996. Inhibition of protein kinase C mu by various inhibitors: differentiation from protein kinase c isoenzymes. FEBS Lett. 392: 77-80.
44. Martiny-Baron, G., M. G. Kazanietz, H. Mischak, P. M. Blumberg, G. Kochs, H. Hug, D. Marme, and C. Schachtele. 1993. Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J. Biol. Chem. 268: 9194-9197.
45. Ley, R., K. Balmanno, K. Hadfield, C. Weston, and S. J. Cook. 2003. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J. Biol. Chem. 278: 18811-18816.
46. Luciano, F., A. Jacquel, P. Colosetti, M. Herrant, S. Cagnol, G. Pages, and P. Auberger. 2003. Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22: 6785-6793.
47. Liston, A., S. Lesage, D. H. Gray, L. A. O'Reilly, A. Strasser, A. M. Fahrer, R. L. Boyd, J. Wilson, A. G. Baxter, E. M. Gallo, et al. 2004. Generalized resistance to thymic deletion in the NOD mouse; a polygenic trait characterized by defective induction of Bim. Immunity 21: 817-830.
48. Zucchelli, S., P. Holler, T. Yamagata, M. Roy, C. Benoist, and D. Mathis. 2005. Defective central tolerance induction in NOD mice: genomics and genetics. Immunity 22: 385-396.
49. Bouillet, P., L. C. Zhang, D. C. Huang, G. C. Webb, C. D. Bottema, P. Shore, H. J. Eyre, G. R. Sutherland, and J. M. Adams. 2001. Gene structure alternative splicing, and chromosomal localization of pro-apoptotic Bcl-2 relative Bim. Mamm. Genome 12: 163-168.
50. Asada, A., Y. Zhao, H. Komano, T. Kuwata, M. Mukai, K. Fujita, Y. Tozawa, R. Iseki, H. Tian, K. Sato, et al. 2000. The calcium-independent protein kinase C participates in an early process of CD3/CD28-mediated induction of thymocyte apoptosis. Immunology 101: 309-315.
51. Thuille, N., T. Gruber, G. Bock, M. Leitges, and G. Baier. 2004. Protein kinase C β is dispensable for TCR-signaling. Mol. Immunol. 41: 385-390.
52. Gruber, T., N. Thuille, N. Hermann-Kleiter, M. Leitges, and G. Baier. 2005. Protein kinase Cε is dispensable for TCR/CD3-signaling. Mol. Immunol. 42: 305-310.
53. 2+ mobilization and NFAT cell activation in primary mouse T cells. J. Exp. Med. 197: 1525-1535.
54. Sun, Z., C. W. Arendt, W. Ellmeier, E. M. Schaeffer, M. J. Sunshine, L. Gandhi, J. Annes, D. Petrzilka, A. Kupfer, P. L. Schwartzberg, and D. R. Littman. 2000. PKC-θ is required for TCR-induced NF-κB activation in mature but not immature T lymphocytes. Nature 404: 402-407.
55. + thymocytes. J. Exp. Med. 190: 943-952.
56. 2+ flux correlates with thymocyte selection. J. Immunol. 161: 6030-6037.
57. Nakayama, T., Y. Ueda, H. Yamada, E. W. Shores, A. Singer, and C. H. June. 1992. In vivo calcium elevations in thymocytes with T cell receptors that are specific for self ligands. Science 257: 96-99.
58. Werlen, G., B. Hausmann, and E. Palmer. 2000. A motif in the αβ T-cell receptor controls positive selection by modulating ERK activity. Nature 406: 422-426.
59. Gil, D., W. W. Schamel, M. Montoya, F. Sanchez-Madrid, and B. Alarcon. 2002. Recruitment of Nck by CD3 ε reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 109: 901-912.
60. Szymczak, A. L., C. J. Workman, D. Gil, S. Dilioglou, K. M. Vignali, E. Palmer, and D. A. Vignali. 2005. The CD3ε proline-rich sequence, and its interaction with Nck, is not required for T cell development and function. J. Immunol. 175: 270-275.
61. Ding, Y. H., B. M. Baker, D. N. Garboczi, W. E. Biddison, and D. C. Wiley. 1999. Four A6-TCR/peptide/HLA-A2 structures that generate very different T cell signals are nearly identical. Immunity 11: 45-56.
62. Gil, D., A. G. Schrum, B. Alarcon, and E. Palmer. 2005. T cell receptor engagement by peptide-MHC ligands induces a conformational change in the CD3 complex of thymocytes. J. Exp. Med. 201: 517-522.
63. McCarty, N., S. Paust, K. Ikizawa, I. Dan, X. Li, and H. Cantor. 2005. Signaling by the kinase MINK is essential in the negative selection of autoreactive thymocytes. Nat. Immunol. 6: 65-72.
64. Gong, Q., A. M. Cheng, A. M. Akk, J. Alberola-Ila, G. Gong, T. Pawson, and A. C. Chan. 2001. Disruption of T cell signaling networks and development by Grb2 haploid insufficiency. Nat. Immunol. 2: 29-36.