New role for hPar-1 kinases EMK and C-TAK1 in regulating localization and activity of class IIa histone deacetylases

Molecular and Cellular Biology

Volumn 26, Issue 19, 2006, Pages 7086-7102

  Dequiedt, Franck ^a   Martin, Maud ^a   Von Blume, Julia ^b   Vertommen, Didier ^c   Lecomte, Emily ^a   Mari, Nathalie ^a   Heinen, Marie France ^a   Bachmann, Malte ^d   Twizere, Jean Claude ^a   Huang, Mei Chris ^e   Rider, Mark H ^c   Piwnica Worms, Helen ^e   Seufferlein, Thomas ^b   Kettmann, Richard ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF ULM   (Germany)

^c DE DUVE INSTITUTE   (Belgium)

^d UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 9; MICROTUBULE AFFINITY REGULATING KINASE; PROTEIN 14 3 3; PROTEIN C TAK1; PROTEIN EMK; PROTEIN KINASE; SERINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENT; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN FAMILY; SIGNAL TRANSDUCTION;

14-3-3 PROTEINS; ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL NUCLEUS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASM; HELA CELLS; HISTONE DEACETYLASES; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SUBSTRATE SPECIFICITY;

EID: 33749161207     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00231-06     Document Type: Article

References (52)

1. Bachmann, M., H. Hennemann, P. X. Xing, I. Hoffmann, and T. Moroy. 2004. The oncogenic serine/threonine kinase Pim-1 phosphorylates and inhibits the activity of Cdc25C-associated kinase 1 (C-TAK1): a novel role for Pim-1 at the G2/M cell cycle checkpoint. J. Biol. Chem. 279:48319-48328.
2. Bakin, R. E., and M. O. Jung. 2004. Cytoplasmic sequestration of HDAC7 from mitochondrial and nuclear compartments upon initiation of apoptosis. J. Biol. Chem. 279:51218-51225.
3. Bolger, T. A., and T. P. Yao. 2005. Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J. Neurosci. 25:9544-9553.
4. Chang, S., S. Bezprozvannaya, S. Li, and E. N. Olson. 2005. An expression screen reveals modulators of class II histone deacetylase phosphorylation. Proc. Natl. Acad. Sci. USA 102:8120-8125.
5. Chang, S., T. A. McKinsey, C. L. Zhang, J. A. Richardson, J. A. Hill, and E. N. Olson. 2004. Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol. Cell. Biol. 24:8467-8476.
6. Chawla, S., P. Vanhoutte, F. J. Arnold, C. L. Huang, and H. Bading. 2003. Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J. Neurochem. 85:151-159.
7. Davis, F. J., M. Gupta, B. Camoretti-Mercado, R. J. Schwartz, and M. P. Gupta. 2003. Calcium/calmodulin-dependent protein kinase activates serum response factor transcription activity by its dissociation from histone deacetylase, HDAC4. Implications in cardiac muscle gene regulation during hypertrophy. J. Biol. Chem. 278:20047-20058.
8. Dequiedt, F., H. Kasler, W. Fischle, V. Kiermer, M. Weinstein, B. G. Herndier, and E. Verdin. 2003. HDAC7, a thymus-specific class II histone deacetylase, regulates Nur77 transcription and TCR-mediated apoptosis. Immunity 18:687-698.
9. Dequiedt, F., J. Van Lint, E. Lecomte, V. Van Duppen, T. Seufferlein, J. R. Vandenheede, R. Wattiez, and R. Kettmann. 2005. Phosphorylation of histone deacetylase 7 by protein kinase D mediates T cell receptor-induced Nur77 expression and apoptosis. J. Exp. Med. 201:793-804.
10. Drewes, G., A. Ebneth, U. Preuss, E. M. Mandelkow, and E. Mandelkow. 1997. MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297-308.
11. Fischle, W., F. Dequiedt, M. Fillion, M. J. Hendzel, W. Voelter, and E. Verdin. 2001. Human HDAC7 histone deacetylase activity is associated with HDAC3 in vivo. J. Biol. Chem. 276:35826-35835.
12. Fischle, W., F. Dequiedt, M. J. Hendzel, M. G. Guenther, M. A. Lazar, W. Voelter, and E. Verdin. 2002. Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol. Cell 9:45-57.
13. Grozinger, C. M., and S. L. Schreiber. 2000. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc. Natl. Acad. Sci. USA 97:7835-7840.
14. Hurov, J. B., T. S. Stappenbeck, C. M. Zmasek, L. S. White, S. H. Ranganath, J. H. Russell, A. C. Chan, K. M. Murphy, and H. Piwnica-Worms. 2001. Immune system dysfunction and autoimmune disease in mice lacking Emk (Par-1) protein kinase. Mol. Cell. Biol. 21:3206-3219.
15. Kao, H.-Y., A. Verdel, C.-C. Tsai, C. Simon, H. Juguilon, and S. Khochbin. 2001. Mechanism for nucleocytoplasmic shuttling of histone deacetylase 7. J. Biol. Chem. 276:47496-47507.
16. Kirsh, O., J. S. Seeler, A. Pichler, A. Gast, S. Muller, E. Miska, M. Mathieu, A. Harel-Bellan, T. Kouzarides, F. Melchior, and A. Dejean. 2002. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21:2682-2691.
17. Lemercier, C., A. Verdel, B. Galloo, S. Curtet, M.-P. Brocard, and S. Khochbin. 2000. mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity. J. Biol. Chem. 275:15594-15599.
18. Li, X., S. Song, Y. Liu, S.-H. Ko, and H.-Y. Kao. 2004. Phosphorylation of the histone deacetylase 7 modulates its stability and association with 14-3-3 proteins. J. Biol. Chem. 279:34201-34208.
19. +/ calmodulin-dependent kinase II promotes depolarization-mediated cerebellar granule neuron survival. J. Biol. Chem. 278:41472-41481.
20. Liu, F., M. Dowling, X.-J. Yang, and G. D. Kao. 2004. Caspase-mediated specific cleavage of human histone deacetylase 4. J. Biol. Chem. 279:34537-34546.
21. Liu, Y., W. R. Randall, and M. F. Schneider. 2005. Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle. J. Cell Biol. 168:887-897.
22. Lu, J., T. A. McKinsey, R. L. Nicol, and E. N. Olson. 2000. Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc. Natl. Acad. Sci. USA 97:4070-4075.
23. Manning, G., D. B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam. 2002. The protein kinase complement of the human genome. Science 298: 1912-1934.
24. McKinsey, T. A., C. L. Zhang, J. Lu, and E. N. Olson. 2000. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408:106-111.
25. McKinsey, T. A., C. L. Zhang, and E. N. Olson. 2000. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc. Natl. Acad. Sci. USA 97:14400-14405.
26. McKinsey, T. A., C. L. Zhang, and E. N. Olson. 2001. Identification of a signal-responsive nuclear export sequence in class II histone deacetylases. Mol. Cell. Biol. 21:6312-6321.
27. Mejat, A., F. Ramond, R. Bassel-Duby, S. Khochbin, E. N. Olson, and L. Schaeffer. 2005. Histone deacetylase 9 couples neuronal activity to muscle chromatin acetylation and gene expression. Nat. Neurosci. 8:313-321.
28. Miska, E. A., C. Karlsson, E. Langley, S. J. Nielsen, J. Pines, and T. Kouzarides. 1999. HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J. 18:5099-5107.
29. Muller, J., S. Ory, T. Copeland, H. Piwnica-Worms, and D. K. Morrison. 2001. C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Mol. Cell 8:983-993.
30. Muller, J., D. A. Ritt, T. D. Copeland, and D. K. Morrison. 2003. Functional analysis of C-TAK1 substrate binding and identification of PKP2 as a new C-TAK1 substrate. EMBO J. 22:4431-4442.
31. Ng, H. H., and A. Bird. 2000. Histone deacetylases: silencers for hire. Trends Biochem. Sci. 25:121-126.
32. Ogg, S., B. Gabrielli, and H. Piwnica-Worms. 1994. Purification of a serine kinase that associates with and phosphorylates human Cdc25C on serine 216. J. Biol. Chem. 269:30461-30469.
33. Paroni, G., M. Mizzau, C. Henderson, G. Del Sal, C. Schneider, and C. Brancolini. 2004. Caspase-dependent regulation of histone deacetylase 4 nuclear-cytoplasmic shuttling promotes apoptosis. Mol. Biol. Cell 15:2804-2818.
34. Parra, M., H. Kasler, T. A. McKinsey, E. N. Olson, and E. Verdin. 2005. Protein dinase D1 phosphorylates HDAC7 and induces its nuclear export after T-cell receptor activation. J. Biol. Chem. 280:13762-13770.
35. Peng, C. Y., P. R. Graves, S. Ogg, R. S. Thomas, M. J. Byrnes, 3rd, Z. Wu, M. T. Stephenson, and H. Piwnica-Worms. 1998. C-TAK1 protein kinase phosphorylates human Cdc25C on serine 216 and promotes 14-3-3 protein binding. Cell Growth Differ. 9:197-208.
36. Petrie, K., F. Guidez, L. Howell, L. Healy, S. Waxman, M. Greaves, and A. Zelent. 2003. The histone deacetylase 9 gene encodes multiple protein isoforms. J. Biol. Chem. 278:16059-16072.
37. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
38. Shi, H., C. Asher, Y. Yung, L. Kligman, E. Reuveny, R. Seger, and H. Garty. 2002. Casein kinase 2 specifically binds to and phosphorylates the carboxy termini of ENaC subunits. Eur. J. Biochem. 269:4551-4558.
39. Tassan, J. P., and X. Le Goff. 2004. An overview of the KIN1/PAR-1/MARK kinase family. Biol. Cell. 96:193-199.
40. Thiel, G., M. Lietz, and M. Hohl. 2004. How mammalian transcriptional repressers work. Eur. J. Biochem. 271:2855-2862.
41. Trinczek, B., M. Brajenovic, A. Ebneth, and G. Drewes. 2004. MARK4 is a novel microtubule-associated proteins/microtubule affinity-regulating kinase that binds to the cellular microtubule network and to centrosomes. J. Biol. Chem. 279:5915-5923.
42. Vega, R. B., B. C. Harrison, E. Meadows, C. R. Roberts, P. J. Papst, E. N. Olson, and T. A. McKinsey. 2004. Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol. Cell. Biol. 24:8374-8385.
43. Vega, R. B., K. Matsuda, J. Oh, A. C. Barbosa, X. Yang, E. Meadows, J. McAnally, C. Pomajzl, J. M. Shelton, J. A. Richardson, G. Karsenty, and E. N. Olson. 2004. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119:555-566.
44. Vertommen, D., M. Rider, Y. Ni, E. Waelkens, W. Merlevede, J. R. Vandenheede, and J. Van Lint. 2000. Regulation of protein kinase D by multisite phosphorylation. Identification of phosphorylation sites by mass spectrometry and characterization by site-directed mutagenesis. J. Biol. Chem. 275:19567-19576.
45. Wang, A. H., N. R. Bertos, M. Vezmar, N. Pelletier, M. Crosato, H. H. Heng, J. Th'ng, J. Han, and X.-J. Yang. 1999. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol. Cell. Biol. 19:7816-7827.
46. Wang, A. H., M. J. Kruhlak, J. Wu, N. R. Bertos, M. Vezmar, B. I. Posner, D. P. Bazett-Jones, and X. J. Yang. 2000. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell. Biol. 20:6904-6912.
47. White, J., K. Haskins, P. Marrack, and J. Kappler. 1983. Use of I region-restricted, antigen-specific T cell hybridomas to produce idiotypically specific anti-receptor antibodies. J. Immunol. 130:1033-1037.
48. Yaffe, M. B. 2002. How do 14-3-3 proteins work? Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513:53-57.
49. Yang, X.-J., and S. Gregoire. 2005. Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol. Cell. Biol. 25:2873-2884.
50. Zhang, C. L., T. A. McKinsey, S. Chang, C. L. Antos, J. A. Hill, and E. N. Olson. 2002. Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110:479-488.
51. Zhang, S.-H., R. Kobayashi, P. R. Graves, H. Piwnica-Worms, and N. K. Tonks. 1997. Serine phosphorylation-dependent association of the band 4.1-related protein-tyrosine phosphatase PTPH1 with 14-3-3beta protein. J. Biol. Chem. 272:27281-27287.
52. Zhao, X., A. Ito, C. D. Kane, T.-S. Liao, T. A. Bolger, S. M. Lemrow, A. R. Means, and T.-P. Yao. 2001. The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J. Biol. Chem. 276:35042-35048.