ERK5 and the regulation of endothelial cell function

Biochemical Society Transactions

Volumn 37, Issue 6, 2009, Pages 1254-1259

  Roberts, Owain Llŷr ^a   Holmes, Katherine ^b   Müller, Jürgen ^c   Cross, Darren A E ^d   Cross, Michael J ^b  

^a BANGOR UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d ASTRAZENECA   (United Kingdom)

Author keywords

Angiogenesis; Big mitogen activated protein kinase 1 (BMK 1); Endothelial cell; Extracellular signal regulated kinase 5 (ERK5); Mitogen activated protein kinase (MAPK); Signal transduction

Indexed keywords

KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 5; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 3; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

APOPTOSIS; ARTICLE; CELL FUNCTION; CELL MIGRATION; DEPHOSPHORYLATION; ENDOTHELIUM CELL; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE STRUCTURE; GENE TARGETING; GENOTYPE; HUMAN; HYPOXIA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SHEAR STRESS;

ANIMALS; ANOXIA; CELL MOVEMENT; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION;

MUS;

EID: 70450182094     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0371254     Document Type: Article

References (67)

1. Abe, J., Kusuhara, M., Ulevitch, R.J., Berk, B.C. and Lee, J.D. (1996) Big mitogen-activated protein kinase 1 (BMK1) is a redox-sensitive kinase. J. Biol. Chem. 271, 16586-16590
2. Chang, L. and Karin, M. (2001) Mammalian MAP kinase signalling cascades. Nature 410, 37-40
3. Yang, S.H., Sharrocks, A.D. and Whitmarsh, A.J. (2003) Transcriptional regulation by the MAP kinase signaling cascades. Gene 320, 3-21
4. Zhou, G., Bao, Z.Q. and Dixon, J.E. (1995) Components of a new human protein kinase signal transduction pathway. J. Biol. Chem. 270, 12665-12669
5. Lee, J.D., Ulevitch, R.J. and Han, J. (1995) Primary structure of BMK1: a new mammalian MAP kinase. Biochem. Biophys. Res. Commun. 213, 715-724
6. Buschbeck, M. and Ullrich, A. (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
7. Kasler, H.G., Victoria, J., Duramad, O. and Winoto, A. (2000) ERK5 is a novel type of mitogen-activated protein kinase containing a transcriptional activation domain. Mol. Cell. Biol. 20, 8382-8389
8. Yan, C., Luo, H., Lee, J.D., Abe, J. and Berk, B.C. (2001) Molecular cloning of mouse ERK5/BMK1 splice variants and characterization of ERK5 functional domains. J. Biol. Chem. 276, 10870-10878
9. Kato, Y., Kravchenko, V.V., Tapping, R.I., Han, J., Ulevitch, R.J. and Lee, J.D. (1997) BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16, 7054-7066
10. Kato, Y., Tapping, R.I., Huang, S., Watson, M.H., Ulevitch, R.J. and Lee, J.D. (1998) Bmk1/Erk5 is required for cell proliferation induced by epidermal growth factor. Nature 395, 713-716
11. Kesavan, K., Lobel-Rice, K., Sun, W., Lapadat, R., Webb, S., Johnson, G.L. and Garrington, T.P. (2004) MEKK2 regulates the coordinate activation of ERK5 and JNK in response to FGF-2 in fibroblasts. J. Cell. Physiol. 199, 140-148
12. Hayashi, M., Kim, S.W., Imanaka-Yoshida, K., Yoshida, T., Abel, E.D., Eliceiri, B., Yang, Y., Ulevitch, R.J. and Lee, J.D. (2004) Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure. J. Clin. Invest. 113, 1138-1148
13. Nicol, R.L., Frey, N., Pearson, G., Cobb, M., Richardson, J. and Olson, E.N. (2001) Activated MEK5 induces serial assembly of sarcomeres and eccentric cardiac hypertrophy. EMBO J. 20, 2757-2767
14. Carvajal-Vergara, X., Tabera, S., Montero, J.C., Esparis-Ogando, A., Lopez-Perez, R., Mateo, G., Gutierrez, N., Parmo-Cabanas, M., Teixido, J. et al. (2005) Multifunctional role of Erk5 in multiple myeloma. Blood 105, 4492-4499
15. Yan, C., Takahashi, M., Okuda, M., Lee, J.D. and Berk, B.C. (1999) Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells: dependence on tyrosine kinases and intracellular calcium. J. Biol. Chem. 274, 143-150
16. Sohn, S.J., Sarvis, B.K., Cado, D. and Winoto, A. (2002) ERK5 MAPK regulates embryonic angiogenesis and acts as a hypoxia-sensitive repressor of vascular endothelial growth factor expression. J. Biol. Chem. 277, 43344-43351
17. Takeishi, Y., Abe, J., Lee, J.D., Kawakatsu, H., Walsh, R.A. and Berk, B.C. (1999) Differential regulation of p90 ribosomal S6 kinase and big mitogen-activated protein kinase 1 by ischemia/reperfusion and oxidative stress in perfused guinea pig hearts. Circ. Res. 85, 1164-1172
18. Widmann, C., Gibson, S., Jarpe, M.B. and Johnson, G.L. (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180
19. Chao, T.H., Hayashi, M., Tapping, R.I., Kato, Y. and Lee, J.D. (1999) MEKK3 directly regulates MEK5 activity as part of the big mitogen-activated protein kinase 1 (BMK1) signaling pathway. J. Biol. Chem. 274, 36035-36038
20. English, J.M., Vanderbilt, C.A., Xu, S., Marcus, S. and Cobb, M.H. (1995) Isolation of MEK5 and differential expression of alternatively spliced forms. J. Biol. Chem. 270, 28897-28902
21. Mody, N., Campbell, D.G., Morrice, N., Peggie, M. and Cohen, P. (2003) An analysis of the phosphorylation and activation of extracellular-signal-regulated protein kinase 5 (ERK5) by mitogen-activated protein kinase kinase 5 (MKK5) in vitro. Biochem. J. 372, 567-575
22. Morimoto, H., Kondoh, K., Nishimoto, S., Terasawa, K. and Nishida, E. (2007) Activation of a C-terminal transcriptional activation domain of ERK5 by autophosphorylation. J. Biol. Chem. 282, 35449-35456
23. Dickinson, R.J. and Keyse, S.M. (2006) Diverse physiological functions for dual-specificity MAP kinase phosphatases. J. Cell Sci. 119, 4607-4615
24. Buschbeck, M., Eickhoff, J., Sommer, M.N. and Ullrich, A. (2002) Phosphotyrosine-specific phosphatase PTP-SL regulates the ERK5 signaling pathway. J. Biol. Chem. 277, 29503-29509
25. Woo, C.H., Shishido, T., McClain, C., Lim, J.H., Li, J.D., Yang, J., Yan, C. and Abe, J. (2008) Extracellular signal-regulated kinase 5 SUMOylation antagonizes shear stress-induced antiinflammatory response and endothelial nitric oxide synthase expression in endothelial cells. Circ. Res. 102, 538-545
26. Nishimoto, S. and Nishida, E. (2006) MAPK signalling: ERK5 versus ERK1/ 2. EMBO Rep. 7, 782-786
27. Yang, C.C., Ornatsky, O.I., McDermott, J.C., Cruz, T.F. and Prody, C.A. (1998) Interaction of myocyte enhancer factor 2 (MEF2) with a mitogen-activated protein kinase, ERK5/BMK1. Nucleic Acids Res. 26, 4771-4777
28. Kato, Y., Zhao, M., Morikawa, A., Sugiyama, T., Chakravortty, D., Koide, N., Yoshida, T., Tapping, R.I., Yang, Y., Yokochi, T. and Lee, J.D. (2000) Big mitogen-activated kinase regulates multiple members of the MEF2 protein family. J. Biol. Chem. 275, 18534-18540
29. Kamakura, S., Moriguchi, T. and Nishida, E. (1999) Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases: identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274, 26563-26571
30. English, J.M., Pearson, G., Baer, R. and Cobb, M.H. (1998) Identification of substrates and regulators of the mitogen-activated protein kinase ERK5 using chimeric protein kinases. J. Biol. Chem. 273, 3854-3860
31. Watson, F.L., Heerssen, H.M., Bhattacharyya, A., Klesse, L., Lin, M.Z. and Segal, R.A. (2001) Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat. Neurosci. 4, 981-988
32. Hayashi, M. and Lee, J.D. (2004) Role of the BMK1/ERK5 signaling pathway: lessons from knockout mice. J. Mol. Med. 82, 800-808
33. Regan, C.P., Li, W., Boucher, D.M., Spatz, S., Su, M.S. and Kuida, K. (2002) Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects. Proc. Natl. Acad. Sci. U.S.A. 99, 9248-9253
34. Yan, L., Carr, J., Ashby, P.R., Murry-Tait, V., Thompson, C. and Arthur, J.S. (2003) Knockout of ERK5 causes multiple defects in placental and embryonic development. BMC Dev. Biol. 3, 11
35. Wang, X., Merritt, A.J., Seyfried, J., Guo, C., Papadakis, E.S., Finegan, K.G., Kayahara, M., Dixon, J., Boot-Handford, R.P., Cartwright, E.J. 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
36. Yang, J., Boerm, M., McCarty, M., Bucana, C., Fidler, I.J., Zhuang, Y. and Su, B. (2000) Mekk3 is essential for early embryonic cardiovascular development. Nat. Genet. 24, 309-313
37. Traub, O. and Berk, B.C. (1998) Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler. Thromb. Vasc. Biol. 18, 677-685
38. Pi, X., Yan, C. and Berk, B.C. (2004) Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis. Circ. Res. 94, 362-369
39. Wang, X., Finegan, K.G., Robinson, A.C., Knowles, L., Khosravi-Far, R., Hinchliffe, K.A., Boot-Handford, R.P. and Tournier, C. (2006) Activation of extracellular signal-regulated protein kinase 5 downregulates FasL upon osmotic stress. Cell Death Differ. 13, 2099-2108
40. Akaike, M., Che, W., Marmarosh, N.L., Ohta, S., Osawa, M., Ding, B., Berk, B.C., Yan, C. and Abe, J. (2004) The hinge-helix 1 region of peroxisome proliferator-activated receptor γ 1 (PPARγ 1) mediates interaction with extracellular signal-regulated kinase 5 and PPARγ 1 transcriptional activation: involvement in flow-induced PPARγ activation in endothelial cells. Mol. Cell. Biol. 24, 8691-8704
41. Li, L., Tatake, R.J., Natarajan, K., Taba, Y., Garin, G., Tai, C., Leung, E., Surapisitchat, J., Yoshizumi, M., Yan, C. et al. (2008) Fluid shear stress inhibits TNF-mediated JNK activation via MEK5-BMK1 in endothelial cells. Biochem. Biophys. Res. Commun. 370, 159-163
42. ppel-like factor (KLF2). Blood 100, 1689-1698
43. SenBanerjee, S., Lin, Z., Atkins, G.B., Greif, D.M., Rao, R.M., Kumar, A., Feinberg, M.W., Chen, Z., Simon, D.I., Luscinskas, F.W. et al. (2004) KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J. Exp. Med. 199, 1305-1315
44. Boon, R.A. and Horrevoets, A.J. (2009) Key transcriptional regulators of the vasoprotective effects of shear stress. Hamostaseologie 29, 39-43
45. Dekker, R.J., Boon, R.A., Rondaij, M.G., Kragt, A., Volger, O.L., Elderkamp, Y.W., Meijers, J.C., Voorberg, J., Pannekoek, H. and Horrevoets, A.J. (2006) KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 107, 4354-4363
46. Sohn, S.J., Li, D., Lee, L.K. and Winoto, A. (2005) Transcriptional regulation of tissue-specific genes by the ERK5 mitogen-activated protein kinase. Mol. Cell. Biol. 25, 8553-8566
47. ppel-like factor 2. J. Clin. Invest. 116, 49-58
48. Kinderlerer, A.R., Ali, F., Johns, M., Lidington, E.A., Leung, V., Boyle, J.J., Hamdulay, S.S., Evans, P.C., Haskard, D.O. and Mason, J.C. (2008) KLF2-dependent, shear stress-induced expression of CD59: a novel cytoprotective mechanism against complement-mediated injury in the vasculature. J. Biol. Chem. 283, 14636-14644
49. Holmes, K., Roberts, O.L., Thomas, A.M. and Cross, M.J. (2007) Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell. Signalling 19, 2003-2012
50. Miquerol, L., Langille, B.L. and Nagy, A. (2000) Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127, 3941-3946
51. Pi, X., Garin, G., Xie, L., Zheng, Q., Wei, H., Abe, J., Yan, C. and Berk, B.C. (2005) BMK1/ERK5 is a novel regulator of angiogenesis by destabilizing hypoxia inducible factor 1α. Circ. Res. 96, 1145-1151
52. Richard, D.E., Berra, E., Gothie, E., Roux, D. and Pouyssegur, J. (1999) p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1α (HIF-1α) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274, 32631-32637
53. Sodhi, A., Montaner, S., Miyazaki, H. and Gutkind, J.S. (2001) MAPK and Akt act cooperatively but independently on hypoxia inducible factor-1α in rasV12 upregulation of VEGF. Biochem. Biophys. Res. Commun. 287, 292-300
54. Folkman, J. (2007) Angiogenesis: an organizing principle for drug discovery? Nat. Rev. 6, 273-286
55. Hayashi, M., Fearns, C., Eliceiri, B., Yang, Y. and Lee, J.D. (2005) Big mitogen-activated protein kinase 1/extracellular signal-regulated kinase 5 signaling pathway is essential for tumor-associated angiogenesis. Cancer Res. 65, 7699-7706
56. Spiering, D., Schmolke, M., Ohnesorge, N., Schmidt, M., Goebler, M., Wegener, J., Wixler, V. and Ludwig, S. (2009) MEK5/ERK5 signaling modulates endothelial cell migration and focal contact turnover. J. Biol. Chem. 284, 24972-24980
57. Sawhney, R.S., Liu, W. and Brattain, M.G. (2009) A novel role of ERK5 in integrin-mediated cell adhesion and motility in cancer cells via Fak signaling. J. Cell. Physiol. 219, 152-161
58. Cavanaugh, J.E. (2004) Role of extracellular signal regulated kinase 5 in neuronal survival. Eur. J. Biochem. 271, 2056-2059
59. Wang, X. and Tournier, C. (2006) Regulation of cellular functions by the ERK5 signalling pathway. Cell. Signalling 18, 753-760
60. Finegan, K.G., Wang, X., Lee, E.J., Robinson, A.C. and Tournier, C. (2009) Regulation of neuronal survival by the extracellular signal-regulated protein kinase 5. Cell Death Differ. 16, 674-683
61. Montero, J.C., Ocana, A., Abad, M., Ortiz-Ruiz, M.J., Pandiella, A. and Esparis-Ogando, A. (2009) Expression of Erk5 in early stage breast cancer and association with disease free survival identifies this kinase as a potential therapeutic target. PLoS One 4, e5565
62. Tatake, R.J., O'Neill, M.M., Kennedy, C.A., Wayne, A.L., Jakes, S., Wu, D., Kugler, Jr, S.Z., Kashem, M.A., Kaplita, P. and Snow, R.J. (2008) Identification of pharmacological inhibitors of the MEK5/ERK5 pathway. Biochem. Biophys. Res. Commun. 377, 120-125
63. Guo, Z., Clydesdale, G., Cheng, J., Kim, K., Gan, L., McConkey, D.J., Ullrich, S.E., Zhuang, Y. and Su, B. (2002) Disruption of Mekk2 in mice reveals an unexpected role for MEKK2 in modulating T-cell receptor signal transduction. Mol. Cell. Biol. 22, 5761-5768
64. Garrington, T.P., Ishizuka, T., Papst, P.J., Chayama, K., Webb, S., Yujiri, T., Sun, W., Sather, S., Russell, D.M., Gibson, S.B. et al. (2000) MEKK2 gene disruption causes loss of cytokine production in response to IgE and c-Kit ligand stimulation of ES cell-derived mast cells. EMBO J. 19, 5387-5395
65. Lin, Q., Schwarz, J., Bucana, C. and Olson, E.N. (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276, 1404-1407
66. Lin, Q., Lu, J., Yanagisawa, H., Webb, R., Lyons, G.E., Richardson, J.A. and Olson, E.N. (1998) Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125, 4565-4574
67. Bi, W., Drake, C.J. and Schwarz, J.J. (1999) The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev. Biol. 211, 255-267