ERK5 activates NF-κB in leukemic T cells and is essential for their growth in vivo

Journal of Immunology

Volumn 177, Issue 11, 2006, Pages 7607-7617

  Garaude, Johan ^a   Cherni, Seyma ^a   Kaminski, Sandra ^a   Delepine, Etienne ^a   Chable Bessia, Christine ^a   Benkirane, Monsef ^a   Borges, Joana ^c   Pandiella, Atanasio ^c   Iñiguez, Miguel Angel ^b   Fresno, Manuel ^b   Hipskind, Robert A ^a   Villalba, Martin ^a  

^a CNRS   (France)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR; FAS ANTIBODY; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 7; RNA; SMALL HAIRPIN RNA; SYNAPTOTAGMIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE ACTIVATION; HUMAN; HUMAN CELL; IN VIVO CULTURE; LEUKEMIA CELL; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SIGNAL TRANSDUCTION; STRESS; T LYMPHOCYTE;

EID: 33751576569     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.11.7607     Document Type: Article

References (60)

1. Garaude, J., S. Kaminski, S. Cherni, R. A. Hipskind, and M. Villalba. 2005. The role of ERK5 in T-cell signalling. Scand. J. Immunol. 62: 515-520.
2. Lee, J. D., R. J. Ulevitch, and J. Han. 1995. Primary structure of BMK1: a new mammalian MAP kinase. Biochem. Biophys. Res. Commun. 213: 715-724.
3. Buschbeck, M., and A. Ullrich. 2005. The unique C-terminal tail of the mitogen-activated protein kinase ERK5 regulates its activation and nuclear shuttling. J. Biol. Chem. 280: 2659-2667.
4. Kato, Y., R. I. Tapping, S. Huang, M. H. Watson, R. J. Ulevitch, and J. D. Lee. 1998. Bmk1/Erk5 is required for cell proliferation induced by epidermal growth factor. Nature 395: 713-716.
5. Sohn, S. J., D. Li, L. K. Lee, and A. Winoto. 2005. Transcriptional regulation of tissue-specific genes by the ERK5 mitogen-activated protein kinase. Mol. Cell. Biol. 25: 8553-8566.
6. Esparis-Ogando, A., E. Diaz-Rodriguez, J. C. Montero, L. Yuste, P. Crespo, and A. Pandiella. 2002. Erk5 participates in neuregulin signal transduction and is constitutively active in breast cancer cells overexpressing ErbB2. Mol. Cell. Biol. 22: 270-285.
7. Yuste, L., J. C. Montero, A. Esparis-Ogando, and A. Pandiella. 2005. Activation of ErbB2 by overexpression or by transmembrane neuregulin results in differential signaling and sensitivity to herceptin. Cancer Res. 65: 6801-6810.
8. English, J. M., G. Pearson, T. Hockenberry, L. Shivakumar, M. A. White, and M. H. Cobb. 1999. Contribution of the ERK5/MEK5 pathway to Ras/Raf signaling and growth control. J. Biol. Chem. 274: 31588-31592.
9. Mulloy, R., S. Salinas, A. Philips, and R. A. Hipskind. 2003. Activation of cyclin D1 expression by the ERK5 cascade. Oncogene 22: 5387-5398.
10. Linnerth, N. M., M. Baldwin, C. Campbell, M. Brown, H. McGowan, and R. A. Moorehead. 2005. IGF-II induces CREB phosphorylation and cell survival in human lung cancer cells. Oncogene 24: 7310-7319.
11. Buschbeck, M., S. Hofbauer, L. D. Croce, G. Keri, and A. Ullrich. 2005. Ab1-kinase-sensitive levels of ERK5 and its intrinsic basal activity contribute to leukemia cell survival. EMBO Rep. 6: 63-69.
12. Carvajal-Vergara, X., S. Tabera, J. C. Montero, A. Esparis-Ogando, R. Lopez-Perez, G. Mateo, N. Gutierrez, M. Parmo-Cabanas, J. Teixido, J. F. San Miguel, and A. Pandiella. 2005. Multifunctional role of Erk5 in multiple myeloma. Blood 105: 4492-4499.
13. Mehta, P. B., B. L. Jenkins, L. McCarthy, L. Thilak, C. N. Robson, D. E. Neal, and H. Y. Leung. 2003. MEK5 overexpression is associated with metastatic prostate cancer, and stimulates proliferation, MMP-9 expression and invasion. Oncogene 22: 1381-1389.
14. Weldon, C. B., A. B. Scandurro, K. W. Rolfe, J. L, Clayton, S. Elliott, N. N. Butler, L. I. Melnik, J. Alam, J. A. McLachlan, B. M. Jaffe, et al. 2002. Identification of mitogen-activated protein kinase kinase as a chemoresistant pathway in MCF-7 cells by using gene expression microarray. Surgery 132: 293-301.
15. Linnerth, N. M., M. Baldwin, C. Campbell, M. Brown, H. McGowan, and R. A. Moorehead. 2005. IGF-II induces CREB phosphorylation and cell survival in human lung cancer cells. Oncogene 24: 7310-7319.
16. Sohn, S. J., B. K. Sarvis, D. Cado, and A. Winoto. 2002. ERK5 MAPK regulates embryonic angiogenesis and acts as a hypoxia-sensitive represser of vascular endothelial growth factor expression. J. Biol. Chem. 277: 43344-43351.
17. Regan, C. P., W. Li, D. M. Boucher, S. Spatz, M. S. Su, and K. Kuida. 2002. Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects. Proc. Natl. Acad. Sci. USA 99: 9248-9253.
18. Wang, X., A. J. Merritt, J. Seyfried, C. Guo, E. S. Papadakis, K. G. Finegan, M. Kayahara, J. Dixon, R. P. Boot-Handford, E. J. Cartwright, et al. 2005. Targeted deletion of mek5 causes early embryonic death and defects in the extracellular signal-regulated kinase 5/myocyte enhancer factor 2 cell survival pathway. Mol. Cell. Biol. 25: 336-345.
19. Hayashi, M., S. W. Kim, K. Imanaka-Yoshida, T. Yoshida, E. D. Abel, B. Eliceiri, Y. Yang, R. J. Ulevitch, and J. D. Lee. 2004. Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure. J. Clin. Invest. 113: 1138-1148.
20. Cameron, S. J., S. Itoh, C. P. Baines, C. Zhang, S. Ohta, W. Che, M. Glassman, J. D. Lee, C. Yan, J. Yang, and J. Abe. 2004. Activation of big MAP kinase 1 (BMK1/ERK5) inhibits cardiac injury after myocardial ischemia and reperfusion. FEBS Lett. 566: 255-260.
21. Hayashi, M., C. Fearns, B. Eliceiri, Y. Yang, and J. D. Lee. 2005. Big mitogen-activated protein kinase I/extracellular signal-regulated kinase 5 signaling pathway is essential for tumor-associated angiogenesis. Cancer Res. 65: 7699-7706.
22. Barsyte-Lovejoy, D., A. Galanis, A. Clancy, and A. D. Sharrocks. 2004. ERK5 is targeted to myocyte enhancer factor 2A (MEF2A) through a MAPK docking motif. Biochem. J. 381: 693-699.
23. Pearson, G., J. M. English, M. A. White, and M. H. Cobb. 2001. ERK5 and ERK2 cooperate to regulate NF-κB and cell transformation. J. Biol. Chem. 276: 7927-7931.
24. Rayet, B., and C. Gelinas. 1999. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18: 6938-6947.
25. Villalba, M., S. Kasibhatla, L. Genestier, A. Mahboubi, D. R. Green, and A. Altman. 1999. PKCθ is a necessary component, and cooperates with calcineurin, to induce FasL expression during activation-induced T cell death. J. Immunol. 163: 5813-5819.
26. Villalba, M., K. Bi, J. Hu, Y. Altman, P. Bushway, E. Reits, J. Neefjes, G. Baier, R. T. Abraham, and A. Altman. 2002. Translocation of PKCθ in T cells is mediated by a nonconventional, P13-K- and Vav-dependent pathway, but does not absolutely require phospholipase C. J. Cell Biol. 157: 253-263.
27. Brockman, J. A., D. C. Scherer, T. A. McKinsey, S. M. Hall, X. Qi, W. Y. Lee, and D. W. Ballard. 1995. Coupling of a signal response domain in IκBα to multiple pathways for NF-κB activation. Mol. Cell. Biol. 15: 2809-2818.
28. Villalba, M., N. Coudronniere, M. Deckert, E. Teixeiro, P. Mas, and A. Altman. 2000. A novel functional interaction between Vav and PKCθ is required for TCR-induced T cell activation. Immunity 12: 151-160.
29. Villalba, M., J. Hernandez, M. Deckert, and A. Altman. 2000. Vav modulation of the Ras/MEK/ERK signaling pathway plays a role in NFAT activation and CD69 up-regulation. Eur. J. Immunol. 30: 1587-1596.
30. Coudronniere, N., M. Villalba, N. Englund, and A. Altman. 2000. NF-κB activation induced by CD28 costimulation is mediated by PKCθ. Proc. Natl. Acad. Sci. USA 97: 3394-3399.
31. Martin, A. G., and M. Fresno. 2000. Tumor necrosis factor-α activation of NF-κB requires the phosphorylation of Ser-471 in the transactivation domain of C-Rel. J. Biol. Chem. 275: 24383-24391.
32. Yano, O., J. Kanellopoulos, M. Kieran, O. Le Bail, A. Israel, and P. Kourilsky. 1987. Purification of KBF1, a common factor binding to both H-2 and β2-microglobulin enhancers. EMBO J. 6: 3317-3324.
33. Schmitz, M. L., and P. A. Baeuerle. 1991. The p65 subunit is responsible for the strong transcription activating potential of NF-κB. EMBO J. 10: 3805-3817.
34. Busuttil, V., V. Bottero, C. Frelin, V. Imbert, J. E. Ricci, P. Auberger, and J. F. Peyron. 2002. Blocking NF-κB activation in Jurkat leukemic T cells converts the survival agent and tumor promoter PMA into an apoptotic effector. Oncogene 21: 3213-3224.
35. Villalba, M., P. Bushway, and A. Altman. 2001. PKCθ mediates a selective T cell survival signal via phosphorylation of BAD. J. Immunol. 166: 5955-5963.
36. Ashkenazi, A., and V. M. Dixit. 1999. Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 11: 255-260.
37. Engedal, N., and H. K. Blomhoff. 2003. Combined action of ERK and NFκB mediates the protective effect of phorbol ester on Fas-induced apoptosis in Jurkat cells. J. Biol. Chem. 278: 10934-10941.
38. Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-α-induced apoptosis by NF-κB. Science 274: 787-789.
39. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α-induced cell death. Science 274: 782-784.
40. Nencioni, A., L. Wille, G. Dal Bello, D. Boy, G. Cirmena, S. Wesselborg, C. Belka, P. Brossart, F. Patrone, and A. Ballestrero. 2005. Cooperative cytotoxicity of proteasome inhibitors and tumor necrosis factor-related apoptosis-inducing ligand in chemoresistant Bcl-2-overexpressing cells. Clin. Cancer Res. 11: 4259-4265.
41. Sabatini, N., R. Di Pietro, M. Rapino, S. Sancilio, S. Comani, and A. Cataldi. 2004. PI-3-kinase/NF-κB mediated response of Jurkat T leukemic cells to two different chemotherapeutic drugs, etoposide and TRAIL. J. Cell. Biochem. 93: 301-311.
42. Bellarosa, D., M. Binaschi, C. A. Maggi, and C. Goso. 2005. Sabarubicin- (MEN 10755) and paclitaxel show different kinetics in nuclear factor-κB (NF-κB) activation: effect of parthenolide on their cytotoxicity. Anticancer Res. 25: 2119-2128.
43. Dudley, E., F. Hornung, L. Zheng, D. Scherer, D. Ballard, and M. Lenardo. 1999. NF-κB regulates Fas/APO-1/CD95- and TCR-mediated apoptosis of T lymphocytes. Eur. J. Immunol. 29: 878-886.
44. 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)-κB. J. Exp. Med. 185: 1897-1907.
45. Jones, R. G., S. D. Saibil, J. M. Pun, A. R. Elford, M. Bonnard, M. Pellegrini, S. Arya, M. E. Parsons, C. M. Krawczyk, S. Gerondakis, et al. 2005. NF-κB couples protein kinase B/Akt signaling to distinct survival pathways and the regulation of lymphocyte homeostasis in vivo. J. Immunol. 175: 3790-3799.
46. Fluhmann, B., U. Zimmermann, R. Muff, G. Bilbe, J. A. Fischer, and W. Born. 1998. Parathyroid hormone responses of cyclic AMP-, serum- and phorbol esterresponsive reporter genes in osteoblast-like UMR-106 cells. Mol. Cell. Endocrinol. 139: 89-98.
47. Claret, F. X., M. Hibi, S. Dhut, T. Toda, and M. Karin. 1996. A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383: 453-457.
48. Li, Z. W., R. C. Rickert, and M. Karin. 2004. Genetic dissection of antigen receptor-induced NF-κB activation. Mol. Immunol. 41: 701-714.
49. Caamano, J., and C. A. Hunter. 2002. NF-κB family of transcription factors: central regulators of innate and adaptive immune functions. Clin. Microbiol. Rev. 15: 414-429.
50. Tam, W. F., and R. Sen. 2001. IκB family members function by different mechanisms. J. Biol. Chem. 276: 7701-7704.
51. Dyall, R., L. V. Vasovic, R. A. Clynes, and J. Nikolic-Zugic. 1999. Cellular requirements for the monoclonal antibody-mediated eradication of an established solid tumor. Eur. J. Immunol. 29: 30-37.
52. + organs. Blood 95: 2111-2117.
53. Jeremias, I., C. Kupatt, B. Baumann, I. Herr, T. Wirth, and K. M. Debatin. 1998. Inhibition of nuclear factor κB activation attenuates apoptosis resistance in lymphoid cells. Blood 91: 4624-4631.
54. Aza-Blanc, P., C. L. Cooper, K. Wagner, S. Batalov, Q. L. Deveraux, and M. P. Cooke. 2003. Identification of modulators of TRAIL-induced apoptosis via RNAi-based phenotypic screening. Mol. Cell 12: 627-637.
55. Ranganathan, A., G. W. Pearson, C. A. Chrestensen, T. W. Sturgill, and M. H. Cobb. 2006. The MAP kinase ERK5 binds to and phosphorylates p90 RSK. Arch. Biochem. Biophys. 449: 8-16.
56. Bohuslav, J., L. F. Chen, H. Kwon, Y. Mu, and W. C. Greene. 2004. p53 induces NF-κB activation by an IκB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1. J. Biol. Chem. 279: 26115-26125.
57. Lafont, V., E. Astoul, A. Laurence, J. Liautard, and D. Cantrell. 2000. The T cell antigen receptor activates phosphatidylinositol 3-kinase-regulated serine kinases protein kinase B and ribosomal S6 kinase 1. FEBS Lett. 486: 38-42.
58. Franklin, R. A., A. Tordai, H. Patel, A. M. Gardner, G. L. Johnson, and E. W. Gelfand. 1994. Ligation of the T cell receptor complex results in activation of the Ras/Raf-1/MEK/MAPK cascade in human T lymphocytes. J. Clin. Invest. 93: 2134-2140.
59. Kasler, H. G., J. Victoria, O. Duramad, and A. Winoto. 2000. ERK5 is a novel type of mitogen-activated protein kinase containing a transcriptional activation domain. Mol. Cell. Biol. 20: 8382-8389.
60. Liu, W., Y. Liu, and W. L. Lowe, Jr. 2001. The role of phosphatidylinositol 3-kinase and the mitogen-activated protein kinases in insulin-like growth factor-I-mediated effects in vascular endothelial cells. Endocrinology 142: 1710-1719.