Role of the BMK1/ERK5 signaling pathway: Lessons from knockout mice

Journal of Molecular Medicine

Volumn 82, Issue 12, 2004, Pages 800-808

  Hayashi, Masaaki ^a,b   Lee, Jiing Dwan ^b,c  

^a MIE UNIVERSITY   (Japan)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

BMK 1; Cell signaling; Endothelial cell; ERK5; Gene targeting; MAP kinase

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 7;

ATHEROSCLEROSIS; CARCINOGENESIS; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; ENZYME ACTIVATION; GENE TARGETING; HEART HYPERTROPHY; HUMAN; KNOCKOUT MOUSE; NERVE CELL; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOVASCULAR DISEASES; CELL SURVIVAL; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEOPLASMS; NEURONS; SIGNAL TRANSDUCTION;

EID: 12444285810     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-004-0602-8     Document Type: Review

References (63)

1. Pearson G, Robinson F, Beers GT, Xu BE, Karandikar M, Berman K, Cobb MH (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22:153-183
2. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37-40
3. Lee JD, Ulevitch RJ, Han J (1995) Primary structure of BMK1: a new mammalian map kinase. Biochem Biophys Res Commun 213:715-724
4. Zhou G, Bao ZQ, Dixon JE (1995) Components of a new human protein kinase signal transduction pathway. J Biol Chem 270:12665-12669
5. English JM, Vanderbilt CA, Xu S, Marcus S, Cobb MH (1995) Isolation of MEK5 and differential expression of alternatively spliced forms. J Biol Chem 270:28897-28902
6. Yan C, Luo H, Lee JD, Abe J, Berk BC (2001) Molecular cloning of mouse ERK5/BMK1 splice variants and characterization of ERK5 functional domains. J Biol Chem 276:10870-10978
7. Kato Y, Tapping RI, Huang S, Watson MH, Ulevitch RJ, Lee JD (1998) Bmk1/Erk5 is required for cell proliferation induced by epidermal growth factor. Nature 395:713-716
8. Kato Y, Kravchenko W, Tapping RI, Han J, Ulevitch RJ, Lee JD (1997) BMK1/ERK5 regulates serum-induced early gene expression through the transcription factor MEF2C. EMBO J 16:7054-7066
9. Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ, Segal RA (2001) Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat Neurosci 4:981-988
10. Hayashi M, Kim SW, Imanaka-Yoshida K, Yoshida T, Abel ED, Eliceiri B, Yang Y, Ulevitch RJ, Lee JD (2004) Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure. J Clin Invest 113:1138-1148
11. Kesavan K, Lobel-Rice K, Sun W, Lapadat R, Webb S, Johnson GL, Garrington TP (2004) MEKK2 regulates the coordinate activation of ERK5 and JNK in response to FGF-2 in fibroblasts. J Cell Physiol 199:140-148
12. Abe J, Kusuhara M, Ulevitch RJ, Berk BC, Lee JD (1996) Big mitogen-activated protein kinase 1 (BMK1) is a redox-sensitive kinase. J. Biol Chem 271:16586-16590
13. Yan C, Takahashi M, Okuda M, Lee JD, Berk BC (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
14. Suzaki Y, Yoshizumi M, Kagami S, Koyama AH, Taketani Y, Houchi H, Tsuchiya K, Takeda E, Tamaki T (2002) Hydrogen peroxide stimulates c-Src-mediated big mitogen-activated protein kinase 1 (BMK1) and the MEF2C signaling pathway in PC12 cells: potential role in cell survival following oxidative insults. J Biol Chem 277:9614-9621
15. Sun W, Kesavan K, Schaefer BC, Garrington TP, Ware M, Johnson NL, Gelfand EW, Johnson GL (2001) MEKK2 associates with the adapter protein Lad/RIBP and regulates the MEK5-BMK1/ERK5 pathway. J Biol Chem 276:5093-5100
16. Chao TH, Hayashi M, Tapping RI, Kato Y, Lee JD (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
17. Kamakura S, Moriguchi T, 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
18. Mody N, Leitch J, Armstrong C, Dixon J, Cohen P (2001) Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway. FEBS Lett 502:21-24
19. Deacon K, Blank JL (1997) Characterization of the mitogen-activated protein kinase kinase 4 (MKK4)/c-Jun NH2-terminal kinase 1 and MKK3/p38 pathways regulated by MEK kinases 2 and 3. MEK kinase 3 activates MKK3 but does not cause activation of p38 kinase in vivo. J Biol Chem 272:14489-14496
20. Deacon K, Blank JL (1999) MEK kinase 3 directly activates MKK6 and MKK7, specific activators of the p38 and c-Jun NH2-terminal kinases. J Biol Chem 274:16604-16610
21. Marinissen MJ, Chiariello M, Pallante M, Gutkind JS (1999) A network of mitogen-activated protein kinases links G protein-coupled receptors to the c-jun promoter: a role for c-Jun NH2-terminal kinase, p38s, and extracellular signal-regulated kinase 5. Mol Cell Biol 19:4289-4301
22. Kato Y, Zhao M, Morikawa A, Sugiyama T, Chakravortty D, Koide N, Yoshida T, Tapping RI, Yang Y, Yokochi T, Lee JD (2000) Big mitogen-activated kinase regulates multiple members of the MEF2 protein family. J Biol Chem 275:18534-18540
23. Hayashi M, Tapping RI, Chao TH, Lo JF, King CC, Yang Y, Lee JD (2001) BMK1 mediates growth factor-induced cell proliferation through direct cellular activation of serum and glucocorticoid-inducible kinase. J Biol Chem 276:8631-8634
24. Cameron SJ, Malik S, Akaike M, Lerner-Marmarosh N, Yan C, Lee JD, Abe J, Yang J (2003) Regulation of epidermal growth factor-induced connexin 43 gap junction communication by big mitogen-activated protein kinase1/ERK5 but not ERK1/2 kinase activation. J Biol Chem 278:18682-18688
25. Pi X, Yan C, Berk BC (2004) Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis. Circ Res 94:362-369
26. English JM, Pearson G, Hockenberry T, Shivakumar L, White MA, Cobb MH (1999) Contribution of the ERK5/MEK5 pathway to Ras/Raf signaling and growth control. J Biol Chem 274:31588-31592
27. Pearson G, English JM, White MA, Cobb MH (2001) ERK5 and ERK2 cooperate to regulate NF-kappaB and cell transformation. J Biol Chem 276:7927-7931
28. Mehta PB, Jenkins BL, McCarthy L, Thilak L, Robson CN, Neal DE, Leung HY (2003) MEK5 overexpression is associated with metastatic prostate cancer, and stimulates proliferation, MMP-9 expression and invasion. Oncogene 22:1381-1389
29. Weldon CB, Scandurro AB, Rolfe KW, Clayton JL, Elliott S, Butler NN, Melnik LI, Alam J, McLachlan JA, Jaffe BM, Beckman BS, Burow ME (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
30. Esparis-Ogando A, Diaz-Rodriguez E, Montero JC, Yuste L, Crespo P, Pandiella A (2002) Erk5 participates in neuregulin signal transduction and is constitutively active in breast cancer cells overexpressing ErbB2. Mol Cell Biol 22:270-285
31. Mulloy R, Salinas S, Philips A, Hipskind RA (2003) Activation of cyclin D1 expression by the ERK5 cascade. Oncogene 22:5387-5398
32. Francis GS (2001) Pathophysiology of chronic heart failure. Am J Med 110 [Suppl 7A]:37S-46S
33. Takeishi Y, Huang Q, Abe J, Classman M, Che W, Lee JD, Kawakatsu H, Lawrence EG, Hoit BD, Berk BC, Walsh RA (2001) Src and multiple MAP kinase activation in cardiac hypertrophy and congestive heart failure under chronic pressure-overload: comparison with acute mechanical stretch. J Mol Cell Cardiol 33:1637-1648
34. Nicol RL, Frey N, Olson EN (2000) From the sarcomere to the nucleus: role of genetics and signaling in structural heart disease. Annu Rev Genomics Hum Genet 1:179-223
35. Kacimi R, Gerdes AM (2003) Alterations in G protein and MAP kinase signaling pathways during cardiac remodeling in hypertension and heart failure. Hypertension 41:968-977
36. Nicol RL, Frey N, Pearson G, Cobb M, Richardson J, Olson EN (2001) Activated MEK5 induces serial assembly of sarcomeres and eccentric cardiac hypertrophy. EMBO J 20:2757-2767
37. Nakaoka Y, Nishida K, Fujio Y, Izumi M, Terai K, Oshima Y, Sugiyama S, Matsuda S, Koyasu S, Yamauchi-Takihara K, Hirano T, Kawase I, Hirota H (2003) Activation of gp130 transduces hypertrophic signal through interaction of scaffolding/docking protein Gab1 with tyrosine phosphatase SHP2 in cardiomyocytes. Circ Res 93:221-229
38. Thusen JH der, Kuiper J, Van Berkel TJ, Biessen EA (2003) Interleukins in atherosclerosis: molecular pathways and therapeutic potential. Pharmacol Rev 55:133-166
39. Zhao M, Liu Y, Bao M, Kato Y, Han J, Eaton JW (2002) Vascular smooth muscle cell proliferation requires both p38 and BMK1 MAP kinases. Arch Biochem Biophys 400:199-207
40. Luo H, Reidy MA (2002) Activation of big mitogen-activated protein kinase-1 regulates smooth muscle cell replication. Arterioscler Thromb Vasc Biol 22:394-399
41. Cavanaugh JE (2004) Role of extracellular signal regulated kinase 5 in neuronal survival. Eur J Biochem 271:2056-2059
42. Liu L, Cavanaugh JE, Wang Y, Sakagami H, Mao Z, Xia Z (2003) ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc Natl Acad Sci USA 100:8532-8537
43. Shalizi A, Lehtinen M, Gaudilliere B, Donovan N, Han J, Konishi Y, Bonni A (2003) Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J Neurosci 23:7326-7336
44. Regan CP, Li W, Boucher DM, Spatz S, Su MS, Kuida K (2002) Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects. Proc Natl Acad Sci USA 99:9248-9253
45. Sohn SJ, Sarvis BK, Cado D, 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
46. Yan L, Carr J, Ashby PR, Murry-Tait V, Thompson C, Arthur JS (2003) Knockout of ERK5 causes multiple defects in placental and embryonic development. BMC Dev Biol 3:11
47. Yang J, Boerm M, McCarty M, Bucana C, Fidler IJ, Zhuang Y, Su B (2000) Mekk3 is essential for early embryonic cardiovascular development. Nat Genet 24:309-313
48. Lin Q, Schwarz J, Bucana C, Olson EN (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276:1404-1407
49. Lin Q, Lu J, Yanagisawa H, Webb R, Lyons GE, Richardson JA, Olson EN (1998) Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125:4565-4574
50. Bi W, Drake CJ, Schwarz JJ (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
51. Han J, Jiang Y, Li Z, Kravchenko VV, Ulevitch RJ (1997) Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386:296-299
52. Tamura K, Sudo T, Senftleben U, Dadak AM, Johnson R, Karin M (2000) Requirement for p38alpha in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 102:221-231
53. Adams RH, Porras A, Alonso G, Jones M, Vintersten K, Panelli S, Valladares A, Perez L, Klein R, Nebreda AR (2000) Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol Cell 6:109-116
54. Tallquist MD, Soriano P (2000) Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function. Genesis 26:113-115
55. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99-103
56. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, Marth JD, Parada LF (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15:859-876
57. Postic C, Shiota M, Niswender KD, Jetton TL, Chen Y, Moates JM, Shelton KD, Lindner J, Cherrington AD, Magnuson MA (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J Biol Chem 274:305-315
58. Wagner KU, Wall RJ, St Onge L, Gruss P, Wynshaw-Boris A, Garrett L, Li M, Furth PA, Hennighausen L (1997) Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 25:4323-4330
59. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, Cunha GR, Donjacour AA, Matusik RJ, Rosen JM (1995) Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 92:3439-3443
60. Muller WJ, Sinn E, Pattengale PK, Wallace R, Leder P (1988) Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54:105-115
61. Chayama K, Papst PJ, Garrington TP, Pratt JC, Ishizuka T, Webb S, Ganiatsas S, Zon LI, Sun W, Johnson GL, Gelfand EW (2001) Role of MEKK2-MEK5 in the regulation of TNF-alpha gene expression and MEKK2-MKK7 in the activation of c-Jun N-terminal kinase in mast cells. Proc Natl Acad Sci USA 98:4599-4604
62. Wei X, Sun W, Fan R, Hahn J, Joetham A, Li G, Webb S, Garrington T, Dakhama A, Lucas J, Johnson GL, Gelfand EW (2003) MEF2C regulates c-Jun but not TNF-alpha gene expression in stimulated mast cells. Eur J Immunol 33:2903-2909
63. Dinev D, Jordan BW, Neufeld B, Lee JD, Lindemann D, Rapp UR, Ludwig S (2001) Extracellular signal regulated kinase 5 (ERK5) is required for the differentiation of muscle cells. EMBO Rep 2:829-834