Multisite phosphorylation of Erk5 in mitosis

Journal of Cell Science

Volumn 123, Issue 18, 2010, Pages 3146-3156

  Díaz Rodríguez, Elena ^a   Pandiella, Atanasio ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Erk5; Mitosis; Phosphorylation

Indexed keywords

BETA TUBULIN; CYCLIN B; DOCETAXEL; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE 7; NOCODAZOLE;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PHASE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MITOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; TRANSCRIPTION REGULATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CDC2 PROTEIN KINASE; CELL LINE, TUMOR; CELL NUCLEUS; CYTOSOL; HUMANS; MAP KINASE KINASE 5; MITOGEN-ACTIVATED PROTEIN KINASE 7; MITOSIS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN TRANSPORT;

EID: 77956910145     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.070516     Document Type: Article

References (50)

1. Astuti, P., Pike, T., Widberg, C., Payne, E., Harding, A., Hancock, J. and Gabrielli, B. (2009). MAPK pathway activation delays G2/M progression by destabilizing Cdc25B. J. Biol. Chem. 284, 33781-33788.
2. Borges, J., Pandiella, A. and Esparis-Ogando, A. (2007). Erk5 nuclear location is independent on dual phosphorylation, and favours resistance to TRAIL-induced apoptosis. Cell. Signal. 19, 1473-1487. (Pubitemid 46818913)
3. 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.
4. Carvajal-Vergara, X., Tabera, S., Montero, J. C., Esparis-Ogando, A., Lopez-Perez, R., Mateo, G., Gutierrez, N., Parmo-Cabanas, M., Teixido, J., San Miguel, J. F. et al. (2005). Multifunctional role of Erk5 in multiple myeloma. Blood 105, 4492-4499.
5. Cha, H., Wang, X., Li, H. and Fornace, A. J., Jr (2007). A functional role for p38 MAPK in modulating mitotic transit in the absence of stress. J. Biol. Chem. 282, 22984-22992.
6. Cude, K., Wang, Y., Choi, H. J., Hsuan, S. L., Zhang, H., Wang, C. Y. and Xia, Z. (2007). Regulation of the G2-M cell cycle progression by the ERK5-NFkappaB signaling pathway. J. Cell Biol. 177, 253-264.
7. Dyson, M. H., Thomson, S., Inagaki, M., Goto, H., Arthur, S. J., Nightingale, K., Iborra, F. J. and Mahadevan, L. C. (2005). MAP kinase-mediated phosphorylation of distinct pools of histone H3 at S10 or S28 via mitogen- and stress-activated kinase 1/2. J. Cell Sci. 118, 2247-2259.
8. Elia, A. E., Cantley, L. C. and Yaffe, M. B. (2003). Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299, 1228-1231.
9. 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.
10. Esparis-Ogando, A., Diaz-Rodriguez, E., Montero, J. C., Yuste, L., Crespo, P. and 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.
11. Girio, A., Montero, J. C., Pandiella, A. and Chatterjee, S. (2007). Erk5 is activated and acts as a survival factor in mitosis. Cell. Signal. 19, 1964-1972. (Pubitemid 47081386)
12. Goto, H., Tomono, Y., Ajiro, K., Kosako, H., Fujita, M., Sakurai, M., Okawa, K., Iwamatsu, A., Okigaki, T., Takahashi, T. et al. (1999). Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274, 25543-25549.
13. 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.
14. Hendzel, M. J., Wei, Y., Mancini, M. A., Van Hooser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360.
15. 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.
16. 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.
17. 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.
18. 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.
19. Liu, X., Yan, S., Zhou, T., Terada, Y. and Erikson, R. L. (2004). The MAP kinase pathway is required for entry into mitosis and cell survival. Oncogene 23, 763-776.
20. McCracken, S. R., Ramsay, A., Heer, R., Mathers, M. E., Jenkins, B. L., Edwards, J., Robson, C. N., Marquez, R., Cohen, P. and Leung, H. Y. (2008). Aberrant expression of extracellular signal-regulated kinase 5 in human prostate cancer. Oncogene 27, 2978-2988.
21. Mehta, P. B., Jenkins, B. L., McCarthy, L., Thilak, L., Robson, C. N., Neal, D. E. and Leung, H. Y. (2003). MEK5 overexpression is associated with metastatic prostate cancer, and stimulates proliferation, MMP-9 expression and invasion. Oncogene 22, 1381-1389.
22. 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.
23. 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. (Pubitemid 350277147)
24. Nebreda, A. R. and Porras, A. (2000). p38 MAP kinases: beyond the stress response. Trends Biochem. Sci. 25, 257-260.
25. Nishimoto, S. and Nishida, E. (2006). MAPK signalling: ERK5 versus ERK1/2. EMBO Rep. 7, 782-786.
26. Norbury, C. and Nurse, P. (1992). Animal cell cycles and their control. Annu. Rev. Biochem. 61, 441-470.
27. Palmer, A., Gavin, A. C. and Nebreda, A. R. (1998). A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. EMBO J. 17, 5037-5047.
28. 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 1alpha. Circ. Res. 96, 1145-1151.
29. Pines, J. and Hunter, T. (1991). Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115, 1-17.
30. Preuss, U., Landsberg, G. and Scheidtmann, K. H. (2003). Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res. 31, 878-885.
31. 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. USA 99, 9248-9253.
32. Robinson, M. J. and Cobb, M. H. (1997). Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9, 180-186.
33. Santamaria, D., Barriere, C., Cerqueira, A., Hunt, S., Tardy, C., Newton, K., Caceres, J. F., Dubus, P., Malumbres, M. and Barbacid, M. (2007). Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448, 811-815.
34. Shaul, Y. D. and Seger, R. (2006). ERK1c regulates Golgi fragmentation during mitosis. J. Cell Biol. 172, 885-897.
35. Sif, S., Stukenberg, P. T., Kirschner, M. W. and Kingston, R. E. (1998). Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12, 2842-2851.
36. 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. (Pubitemid 35285722)
37. Vander Haar, E., Lee, S. I., Bandhakavi, S., Griffin, T. J. and Kim, D. H. (2007). Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 9, 316-323.
38. Vassilev, L. T., Tovar, C., Chen, S., Knezevic, D., Zhao, X., Sun, H., Heimbrook, D. C. and Chen, L. (2006). Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc. Natl. Acad. Sci. USA 103, 10660-10665.
39. Wang, X. and Tournier, C. (2006). Regulation of cellular functions by the ERK5 signalling pathway. Cell. Signal. 18, 753-760.
40. 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.
41. 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.
42. Weston, C. R. and Davis, R. J. (2002). The JNK signal transduction pathway. Curr. Opin. Genet. Dev. 12, 14-21.
43. 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.
44. Woronicz, J. D., Lina, A., Calnan, B. J., Szychowski, S., Cheng, L. and Winoto, A. (1995). Regulation of the Nur77 orphan steroid receptor in activation-induced apoptosis. Mol. Cell. Biol. 15, 6364-6376.
45. Wright, J. H., Munar, E., Jameson, D. R., Andreassen, P. R., Margolis, R. L., Seger, R. and Krebs, E. G. (1999). Mitogen-activated protein kinase kinase activity is required for the G(2)/M transition of the cell cycle in mammalian fibroblasts. Proc. Natl. Acad. Sci. USA 96, 11335-11340.
46. Xie, S., Wang, Q., Ruan, Q., Liu, T., Jhanwar-Uniyal, M., Guan, K. and Dai, W. (2004). MEK1-induced Golgi dynamics during cell cycle progression is partly mediated by Polo-like kinase-3. Oncogene 23, 3822-3829.
47. 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.
48. Zecevic, M., Catling, A. D., Eblen, S. T., Renzi, L., Hittle, J. C., Yen, T. J., Gorbsky, G. J. and Weber, M. J. (1998). Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J. Cell Biol. 142, 1547-1558.
49. Zhao, Y. and Chen, R. H. (2006). Mps1 phosphorylation by MAP kinase is required for kinetochore localization of spindle-checkpoint proteins. Curr. Biol. 16, 1764-1769.
50. 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.