Activation of MEK kinase 1 by the c-Abl protein tyrosine kinase in response to DNA damage

Molecular and Cellular Biology

Volumn 20, Issue 14, 2000, Pages 4979-4989

  Kharbanda, Surender ^a   Pandey, Pramod ^a   Yamauchi, Teruo ^a   Kumar, Shailender ^a   Kaneki, Masao ^a   Kumar, Vijay ^a   Bharti, Ajit ^a   Yuan, Zhi Min ^a   Ghanem, Louis ^b   Rana, Ajay ^b   Weichselbaum, Ralph ^c   Johnson, Gary ^d   Kufe, Donald ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL CYCLE G1 PHASE; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE TARGETING; GENETIC TRANSFECTION; GENOTOXICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RECEPTOR BINDING;

ANIMALS; CELLS, CULTURED; CISPLATIN; DNA DAMAGE; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 4; MAP KINASE KINASE KINASE 1; MICE; MICE, MUTANT STRAINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-ABL; RADIATION, IONIZING; U937 CELLS;

EID: 0033935649     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.14.4979-4989.2000     Document Type: Article

References (81)

1. Angel, P., K. Hattori, T. Smeal, and M. Karin. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55:875-885.
2. Baskaran, R., L. D. Wood, L. L. Whitaker, Y. Xu, C. Barlow, C. E. Canman, S. E. Morgan, D. Baltimore, A. Wynshaw-Boris, M. B. Kastan, and J. Y. J. Wang. 1997. Ataxia telangiectasia mutant protein activates c-ab1 tyrosine kinase in response to ionizing radiation. Nature 387:516-519.
3. Ben-Neriah, Y., A. Bernards, M. Paskind, G. Q. Daley, and D. Baltimore. 1986. Alternative 5′ exons in c-ab1 mRNA. Cell 44:577-586.
4. Blank, J. L., P. Gerwins, E. M. Elliott, S. Sather, and G. Johnson. 1996. Molecular cloning of mitogen-activated protein/ERK kinase kinases (MEKK) 2 and 3. Regulation of sequential phosphorylation pathways involving mitogen-activated protein kinase and c-Jun kinase. J. Biol. Chem. 271:5361-5368.
5. Chen, R. H., C. Sarnecki, and J. Blenis. 1992. Nuclear localization and regulation of erk-and rsk-encoded protein kinases. Mol. Cell. Biol. 12:915-927.
6. Chen, Y.-H., C. F. Meyer, and T.-H. Tan. 1996. Persistent activation of c-Jun N-terminal kinase 1 (JNK1) in γ radiation-induced apoptosis. J. Biol. Chem. 271:631-634.
7. Chen, Y.-R., X. Wang, D. Templeton, R. J. Davis, and T.-H. Tan. 1996. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ radiation. J. Biol. Chem. 271:31929-31936.
8. Coso, O. A., M. Chiariello, J. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J. S. Gutkind 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137-1146.
9. Davis, R. J. 1994. MAPKs: new JNK expands the group. Trends Biochem. Sci. 19:470-473.
10. Derijard, B., M. Hibi, I. H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that hinds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
11. Derijard, B., J. Raingeaud, T. Barrett, 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 267:682-685.
12. Devary, Y., R. A. Gottlieb, T. Smeal, and M. Karin. 1992. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 71:1081-1091.
13. Dikic, I., G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383:547-550.
14. Errede, B., and D. E. Levin. 1993. A conserved kinase cascade for MAP kinase activation in yeast. Curr. Opin. Cell Biol. 5:254-260.
15. Fanger, G. R., N. L. Johnson, and G. L. Johnson. 1997. MEK kinases are regulated by EGF and selectively interact with Rac/Cdc42. EMBO J. 16: 4961-4972.
16. Feller, S., R. Ren, H. Hanafusa, and D. Baltimore. 1994. SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Ab1. Trends Biochem. Sci. 19:453-458.
17. Georgiev, O., J. P. Bourquin, M. Gstaiger, L. Knoepfel, Vl. Schaffner, and C. Hovens. 1996. Two versatile eukaryotic vectors permitting epitope tagging, radiolabelling and nuclear localisation of expressed proteins. Gene 168:165-167.
18. Goga, A., X. Liu, T. M. Hambuch, K. Senechal, E. Major, A. J. Berk, O. N. Witte, and C. L. Sawyers. 1995. p53 dependent growth suppression by the c-Ab1 nuclear tyrosine kinase. Oncogene 11:791-799.
19. Herskowitz, I. 1995. MAP kinase pathways in yeast: for mating and more. Cell 80:187-197.
20. Hirai, S., M. Izawa, S. Osada, G. Spyrou, and S. Ohno. 1996. Activation of the JNK pathway by distantly related protein kinases, MEKK and MLK. Oncogene 12:641-650.
21. Hirano, M., S.-I. Osada, T. Aoki, S.-I. Hirai, M. Hosaka, J.-I. Inoue, and S. Ohno, 1996. MEK kinase is involved in tumor necrosis factor α-induced NF-κB activation and degradation of IkBα. J. Biol. Chem. 271:13234-13238.
22. Ichijo, H., E. Nishida, K. Irie, P. ten Dijke, T. Moriguchi, M. Takagi, K. Matsumoto, K. Miyazono, and Y. Gotoh. 1997. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90-94.
23. Johnson, N. L., A. M. Gardner, K. M. Diener, C. A. Lange-Carter, J. Gleavy, M. B. Jarpe, A. Minden, M. Karin, L. I. Zon, and G. L. Johnson. 1996. Signal transduction pathways regulated by mitogen-activated/extracurricular response kinase kinase kinase induce cell death. J. Biol. Chem. 271:3229-3237.
24. Kaneki, M., S. Kharbanda, P. Pandey, J.-R. Liou, R. Stone, and D. Kufe. 1999. Functional role for protein kinase Cβ as a regulator of stress-activated protein kinase activation and monocytic differentiation of myeloid leukemia cells. Mol. Cell. Biol. 19:461-470.
25. Karin, M. 1995. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270:16483-16486.
26. Katz, P., G. Whalen, and J. H. Kehrl. 1994. Differential expression of a novel protein kinase in human B lymphocytes. Preferential localization in the germinal center. J. Biol. Chem. 269:16802-16809.
27. Kharbanda, S., A. Bharti, D. Pei, J. Wang, P. Pandey, R. Ren, R. Weichselbaum, C. T. Walsh, and D. Kufe. 1996. The stress response to ionizing radiation involves c-Ab1-dependent phosphorylation of SHPTP1. Proc. Natl. Acad. Sci. USA 93:6898-6901.
28. Kharbanda, S., P. Pandey, S. Jin, S. Inoue, A. Bharti, Z.-M. Yuan, R. Weichselbaum, D. Weaver, and D. Kufe. 1997. Functional interaction of DNA-PK and c-Ab1 in response to DNA damage. Nature 386:732-735.
29. Kharbanda, S., P. Pandey, R. Ren, S. Feller, B. Mayer, L. Zon, and D. Kufe. 1995. c-Ab1 activation regulates induction of the SEK1/stress activated protein kinase pathway in the cellular response to 1-β-D-arabinofuranosylcytosine. J. Biol. Chem. 270:30278-30281.
30. Kharbanda, S., R. Ren, P. Pandey, T. D. Shafman, S. M. Feller, R. R. Weichselbaum, and D. W. Kufe. 1995. Activation of the c-Ab1 tyrosine kinase in the stress response to DNA-damaging agents. Nature 376:785-788.
31. Kharbanda, S., A. Saleem, T. Shafman, Y. Emoto, R. Weichselbaum, J. Woodgett, J. Avruch, J. Kyriakis, and D. Kufe. 1995. Ionizing radiation stimulates a Grb2-mediated association of the stress activated protein kinase with phosphatidylinositol 3-kinase. J. Biol. Chem. 270:18871-18874.
32. Kharbanda, S., M. L. Sherman, and D. W. Kufe. 1990. Transcriptional regulation of c-jun gene expression by arabinofuranosylcytosine in human myeloid leukemia cells. J. Clin. Investig. 86:1517-1523.
33. Kiefer, F., L. A. Tibbles, M. Anafi, A. Janssen, B. W. Zanke, N. Lassam, T. Pawson, J. R. Woodgett, and N. N. Iscove. 1996. HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J. 15:7013-7025.
34. Kyriakis, J. M., and J. Avruch. 1996. Sounding the alarm: protein kinase cascades activated by stress and inflammation. J. Biol. Chem. 271:24313-24316.
35. Kyriakis, J. M., P. Banerjee, E. Nikolakaki, T. Dai, E. A. Rubie, M. F. Ahmad, J. Avruch, and J. R. Woodgett. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369:156-160.
36. Lallemand, D., J. Ham, S. Garbay, L. Bakiri, F. Traincard, O. Jeannequin, C. M. Pfarr, and M. Yaniv. 1998. Stress-activated protein kinases are negatively regulated by cell density. EMBO J. 17:5615-5626.
37. Lange-Carter, C. A., and G. L. Johnson. 1994. Ras-dependent growth factor regulation of MEK kinase in PC12 cells. Science 265:1458-1461.
38. Lange-Carter, C. A., C. M. Pleiman, A. M. Gardner, K. J. Blumer, and G. J. Johnson. 1994. A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf. Science 260:315-319.
39. 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.
40. Liu, Z.-G., R. Baskaran, E. T. Lea-Chou, L. Wood, V. Chen, M. Karin, and J. Y. J. Wang. 1996. Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 384:273-276.
41. Liu, Z.-G., R. Baskaran, E. T. Lea-Chou, L. Wood, Y. Chen, M. Karin, and J. Y. J. Wang. 1996. Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 384:273-276.
42. Manser, E., T. Leung, H. Salihuddin, Z. S. Zhao, and L. Lim. 1994. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367: 40-46.
43. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
44. Mattioni, T., P. K. Jackson, O. Bchini-Hooft van Huijsduijnen, and D. Picard. 1995. Cell cycle arrest by tyrosine kinase Ab1 involves altered early mitogenic response. Oncogene 10:1325-1333.
45. Minden, A., and M. Karin. 1997. Regulation and function of the JNK subgroup of MAP kinases. Biochim. Biophys. Acta 1333:F85-104.
46. Minden, A., A. Lin, M. McMahon, C. Lange-Carter, B. Derijard, R. J. Davis, G. L. Johnson, and M. Karin. 1994. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719-1723.
47. L blocks activation of related adhesion focal tyrosine kinase/proline-rich tyrosine kinase 2 and stress-activated protein kinase/c-Jun N-terminal protein kinase in the cellular response to methylmethane sulfonate. J. Biol. Chem. 274:8618-8623.
48. Pandey, P., J. Raingeaud, M. Kaneki, R. Weichselbaum, R. Davis, D. Kufe, and S. Kharbanda. 1996. Activation of p38 MAP kinase by c-Ab1-dependent and -independent mechanisms. J. Biol. Chem. 271:23775-23779.
49. Pombo, C. M., J. H. Kehrl, I. Sanchez, P. Kate, J. Avruch, L. I. Zon, J. R. Woodgett, T. Force, and J. M. Kyriakis. 1995. Activation of the SAPK pathway by the human STE20 homologue germinal centre kinase. Nature 377:750-754.
50. Raitano, A. B., J. R. Halpern, T. M. Hambuch, and C. L. Sawyers. 1995. The Bcr-Ab1 leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc. Natl. Acad. Sci. USA 92:11746-11750.
51. Rana, A., K. Gallo, P. Godowski, S.-I. Hirai, S. Ohno, L. Zon, J. M. Kyriakis, and J. Avruch. 1996. The mixed lineage kinase SPRK phosphorylates and activates the stress-activated protein kinase activator, SEK-1. J. Biol. Chem. 271:19025-19028.
52. Ren, R., Z.-S. Ye, and D. Baltimore. 1994. Ab1 protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes Dev. 8:783-795.
53. Renshaw, M. W., E. Lea-Chou, and J. Y. J. Wang. 1996. Rac is required for v-Ab1 tyrosine kinase to activate mitogenesis. Curr. Biol. 6:76-83.
54. Rubin, E., S. Kharbanda, H. Gunji, and D. Kufe. 1991. Activation of the c-jun protooncogene in human myeloid leukemia cells treated with etoposide. Mol. Pharmacol. 39:697-701.
55. Russell, M., C. A. Lange-Carter, and G. L. Johnson. 1995. Direct interaction between Ras and the kinase domain of mitogen-activated protein kinase kinase kinase (MEKK1). J. Biol. Chem. 270:11757-11760.
56. Salmeron, A., T. B. Ahmad, G. W. Carlile, D. Pappin, R. P. Narsimhan, and S. C. Ley. 1996. Activation of MEK-1 and SEK-1 by Tpl-2 proto-oncoprotein, a novel MAP kinase kinase kinase. EMBO J. 15:817-826.
57. Sanchez, 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.
58. Sawyers, C. L., J. McLaughlin, A. Goga, M. Havilik, and O. Witte. 1994. The nuclear tyrosine kinase c-Ab1 negatively regulates cell growth. Cell 77:121-131.
59. m1 mutation show poor viability and depletion of selected B and T cell populations. Cell 65:1165-1175.
60. Shafman, T., K. K. Khanna, P. Kedar, K. Spring, S. Kozlov, T. Yen, K. Hobson, M. Gatei, N. Zhang, D. Watters, M. Egerton, Y. Shiloh, S. Kharbanda, D. Kufe, and M. F. Lavin. 1997. Interaction between ATM protein and c-Ab1 in response to DNA damage. Nature 387:520-523.
61. Sherman, M., R. Stone, R. Datta, S. Bernstein, and D. Kufe. 1990. Transcriptional and post-transcriptional regulation of c-Jun expression during monocytic differentiation of human myeloid leukemic cells. J. Biol. Chem. 265:3320-3323.
62. Sherman, S. E., and S. J. Lippard. 1987. Structural aspects of platinum anticancer drug interaction with DNA. J. Chem. Rev. 87:1153-1181.
63. Takekawa, M., F. Posas, and H. Saito. 1997. A human homolog of the yeast Ssk2/Ssk22 MAP kinase kinase kinases, MTK1, mediates stress-induced activation of the p38 and JNK pathways. EMBO J. 16:4973-4982.
64. Takekawa, M., and H. Saito. 1998. A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell 95:521-530.
65. Tibbles, L. A., Y. L. Ing, F. Kiefer, J. Chan, N. Iscove, J. R. Woodgett, and N. J. Lassam. 1996. MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. EMBO J. 15:7026-7035.
66. Tokiwa, G., I. Dikic, S. Lev, and J. Schlessinger. 1996. Activation of Pyk2 by stress signals and coupling with JNK signaling pathway. Science 273:792-794.
67. Tournier, C., A. J. Whitmarsh, J. Cavanagh, T. Barrett, and R. J. Davis. 1997. Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proc. Natl. Acad. Sci. USA 94:7337-7342.
68. Tybulewicz, V. L. J., C. E. Crawford, P. K. Jackson, R. T. Bronson, and R. C. Mulligan. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-ab1 proto-oncogene. Cell 65:1153-1163.
69. Verheij, M., R. Bose, X. H. Lin, B. Yhao, W. D. Jarvis, S. Grant, M. J. Birrer, E. Szabo, L. I. Zon, J. M. Kyriakis, A. Haimovitz-Friedman, Z. Fuks, and R. N. Kolesnick. 1996. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380:75-79.
70. Widmann, C., P. Gerwins, N. L. Johnson, M. B. Jarpe, and G. L. Johnson. 1998. MEK kinase 1, a substrate for DEVD-directed caspases, is involved in genotoxin-induced apoptosis. Mol. Cell. Biol. 18:2416-2429.
71. Widmann, C., S. Gibson, and G. L. Johnson. 1998. Caspase-dependent cleavage of signaling proteins during apoptosis. A turn-off mechanism for anti-apoptotic signals. J. Biol. Chem. 273:7141-7147.
72. Wilhelm, D., K. Bender, A. Knebel, and P. Angel. 1997. The level of intracellular glutathione is a key regulator for the induction of stress-activated signal transduction pathways including Jun N-terminal protein kinases and p38 kinase by alkylating agents. Mol. Cell. Biol. 17:4792-4800.
73. Xia, Z., M. Dickens, J. Raingeaud, R. J. Davis, and M. E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
74. Xu, S., and M. H. Cobb. 1997. MEKK1 binds directly to the c-Jun N-terminal kinases/stress-activated protein kinases. J. Biol. Chem. 272:32056-32060.
75. Xu, S., D. J. Robbins, L. B. Christerson, J. M. English, C. A. Vanderbilt, and M. H. Cobb. 1996. Cloning of rat MEK kinase 1 cDNA reveals an endogenous membrane-associated 195-kDa protein with a large regulatory domain. Proc. Natl. Acad. Sci. USA 93:5291-5295.
76. Yan, M., T. Dai, J. C. Deak, J. M. Kyriakis, L. I. Zon, J. R. Woodgett, and D. J. Templeton. 1994. Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature 372:798-800.
77. Yuan, Z. M., Y. Huang, T. Ishiko, S. Nakada, T. Utsugisawa, S. Kharbanda, P. Sung, A. Shinohara, R. Weichselbaum, and D. Kufe. 1998. Regulation of Rad51 function by c-Ab1 in response to DNA damage. J. Biol. Chem. 273: 3799-3802.
78. Yuan, Z. M., Y. Huang, Y. Whang, C. Sawyers, R. Weichselbaum, S. Kharbanda, and D. Kufe. 1996. Role for the c-Ab1 tyrosine kinase in the growth arrest response to DNA damage. Nature 382:272-274.
79. Yuasa, T., S. Ohno, J. H. Kehrl, and J. M. Kyriakis. 1998. Tumor necrosis factor signaling to stress-activated protein kinase (SAPK)/Jun NH2-terminal kinase (JNK) and p38. Germinal center kinase couples TRAF2 to mitogen-activated protein kinase/ERK kinase kinase 1 and SAPK while receptor interacting protein associates with a mitogen-activated protein kinase kinase kinase upstream of MKK6 and p38. J. Biol. Chem. 273:22681-22692.
80. Zanke, B. W., K. Boudreau, E. Rubie, E. Winnett, L. A. Tibbles, L. Zon, J. Kyriakis, F.-F. Liu, and J. R. Woodgett. 1996. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol. 6:606-613.
81. Zhang, S., J. Han, M. A. Sells, J. Chernoff, U. G. Knaus, R. J. Ulevitch, and G. M. Bokoch. 1995. Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. J. Biol. Chem. 270: 23934-23936.