Dephosphorylation at a conserved sp motif governs camp sensitivity and nuclear localization of class iia histone deacetylases

Journal of Biological Chemistry

Volumn 288, Issue 8, 2013, Pages 5591-5605

  Walkinshaw, Donald R ^a   Weist, Ryan ^a,b,c   Xiao, Lin ^a,b   Yan, Kezhi ^b,c   Kim, Go Woon ^d   Yang, Xiang Jiao ^a,b,c,d  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c Deparment of Anatomy and Cell Biology   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; CELLULAR SIGNALING; DEPHOSPHORYLATIONS; HISTONE DEACETYLASES; NUCLEAR LOCALIZATION; NUCLEOCYTOPLASMIC TRAFFICKING;

BIOCHEMISTRY;

BIOLOGY;

CORTICOTROPIN; CYCLIC AMP; HISTONE DEACETYLASE; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 9; LEPTOMYCIN B; UNCLASSIFIED DRUG;

ADIPOCYTE; ARTICLE; CELL DIFFERENTIATION; GENE MUTATION; HUMAN; HUMAN CELL; MYOBLAST; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION;

3T3 CELLS; ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; HEK293 CELLS; HELA CELLS; HISTONE DEACETYLASES; HUMANS; INSECTS; MICE; PHOSPHORYLATION; PLASMIDS; SIGNAL TRANSDUCTION;

EID: 84874334200     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445668     Document Type: Article

References (89)

1. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
2. Wang, Q., Zhang, Y., Yang, C., Xiong, H., Lin, Y., Yao, J., Li, H., Xie, L., Zhao, W., Yao, Y., Ning, Z. B., Zeng, R., Xiong, Y., Guan, K. L., Zhao, S., and Zhao, G. P. (2010) Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327, 1004-1007
3. Yang, X. J., and Seto, E. (2008) Lysine acetylation. Codified crosstalk with other posttranslational modifications. Mol. Cell 31, 449-461
4. Khochbin, S., Verdel, A., Lemercier, C., and Seigneurin-Berny, D. (2001) Functional significance of histone deacetylase diversity. Curr. Opin. Genet. Dev. 11, 162-166
5. McKinsey, T. A., Zhang, C. L., Lu, J., and Olson, E. N. (2000) Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408, 106-111
6. Kim, M. S., Fielitz, J., McAnally, J., Shelton, J. M., Lemon, D. D., McKinsey, T. A., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008) Protein kinase D1 stimulates MEF2 activity in skeletal muscle and enhances muscle performance. Mol. Cell Biol. 28, 3600-3609
7. Liu, Y., Contreras, M., Shen, T., Randall, W. R., and Schneider, M. F. (2009) α-Adrenergic signalling activates protein kinase D and causes nuclear efflux of the transcriptional repressor HDAC5 in cultured adult mouse soleus skeletal muscle fibres. J. Physiol. 587, 1101-1115
8. Zhang, C. L., McKinsey, T. A., Chang, S., Antos, C. L., Hill, J. A., and Olson, E. N. (2002) Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110, 479-488
9. Ha, C. H., Jhun, B. S., Kao, H. Y., and Jin, Z. G. (2008) VEGF stimulates HDAC7 phosphorylation and cytoplasmic accumulation modulating matrix metalloproteinase expression and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 28, 1782-1788
10. Martin, M., Potente, M., Janssens, V., Vertommen, D., Twizere, J. C., Rider, M. H., Goris, J., Dimmeler, S., Kettmann, R., and Dequiedt, F. (2008) Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 4727-4732
11. Wang, S., Li, X., Parra, M., Verdin, E., Bassel-Duby, R., and Olson, E. N. (2008) Control of endothelial cell proliferation and migration by VEGF signaling to histone deacetylase 7. Proc. Natl. Acad. Sci. U.S.A. 105, 7738-7743
12. Parra, M., and Verdin, E. (2010) Regulatory signal transduction pathways for class IIa histone deacetylases. Curr. Opin. Pharmacol. 10, 454-460
13. Majdzadeh, N., Morrison, B. E., and D'Mello, S. R. (2008) Class IIA HDACs in the regulation of neurodegeneration. Front Biosci. 13, 1072-1082
14. Vega, R. B., Matsuda, K., Oh, J., Barbosa, A. C., Yang, X., Meadows, E., McAnally, J., Pomajzl, C., Shelton, J. M., Richardson, J. A., Karsenty, G., and Olson, E. N. (2004) Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119, 555-566
15. Moresi, V., Williams, A. H., Meadows, E., Flynn, J. M., Potthoff, M. J., McAnally, J., Shelton, J. M., Backs, J., Klein, W. H., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2010) Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143, 35-45
16. Chang, S., McKinsey, T. A., Zhang, C. L., Richardson, J. A., Hill, J. A., and Olson, E. N. (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
17. Chang, S., Young, B. D., Li, S., Qi, X., Richardson, J. A., and Olson, E. N. (2006) Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126, 321-334
18. Renthal, W., Maze, I., Krishnan, V., Covington, H. E., 3rd, Xiao, G., Kumar, A., Russo, S. J., Graham, A., Tsankova, N., Kippin, T. E., Kerstetter, K. A., Neve, R. L., Haggarty, S. J., McKinsey, T. A., Bassel-Duby, R., Olson, E. N., and Nestler, E. J. (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56, 517-529
19. Rad, R., Rad, L., Wang, W., Cadinanos, J., Vassiliou, G., Rice, S., Campos, L. S., Yusa, K., Banerjee, R., Li, M. A., de la Rosa, J., Strong, A., Lu, D., Ellis, P., Conte, N., Yang, F. T., Liu, P., and Bradley, A. (2010) PiggyBac transposon mutagenesis. A tool for cancer gene discovery in mice. Science 330, 1104-1107
20. Hutt, D. M., Herman, D., Rodrigues, A. P., Noel, S., Pilewski, J. M., Matteson, J., Hoch, B., Kellner, W., Kelly, J. W., Schmidt, A., Thomas, P. J., Matsumura, Y., Skach, W. R., Gentzsch, M., Riordan, J. R., Sorscher, E. J., Okiyoneda, T., Yates, J. R., 3rd, Lukacs, G. L., Frizzell, R. A., Manning, G., Gottesfeld, J. M., and Balch, W. E. (2010) Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis. Nat. Chem. Biol. 6, 25-33
21. Williams, S. R., Aldred, M. A., Der Kaloustian, V. M., Halal, F., Gowans, G., McLeod, D. R., Zondag, S., Toriello, H. V., Magenis, R. E., and Elsea, S. H. (2010) Haploinsufficiency of HDAC4 causes brachydactyly mental retardation syndrome, with brachydactyly type E, developmental delays, and behavioral problems. Am. J. Hum. Genet. 87, 219-228
22. Verdin, E., Dequiedt, F., and Kasler, H. G. (2003) Class II histone deacetylases. Versatile regulators. Trends Genet. 19, 286-293
23. Yang, X. J., and Seto, E. (2008) The Rpd3/Hda1 family of lysine deacetylases. From bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206-218
24. Backs, J., Song, K., Bezprozvannaya, S., Chang, S., and Olson, E. N. (2006) CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J. Clin. Invest. 116, 1853-1864
25. Kao, H. Y., Verdel, A., Tsai, C. C., Simon, C., Juguilon, H., and Khochbin, S. (2001) Mechanism for nucleocytoplasmic shuttling of histone deacetylase 7. J. Biol. Chem. 276, 47496-47507
26. Little, G. H., Bai, Y., Williams, T., and Poizat, C. (2007) Nuclear calcium/ calmodulin-dependent protein kinase II-preferentially transmits signals to histone deacetylase 4 in cardiac cells. J. Biol. Chem. 282, 7219-7231
27. Zhao, X., Ito, A., Kane, C. D., Liao, T. S., Bolger, T. A., Lemrow, S. M., Means, A. R., and Yao, T. P. (2001) The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J. Biol. Chem. 276, 35042-35048
28. Dequiedt, F., Van Lint, J., Lecomte, E., Van Duppen, V., Seufferlein, T., Vandenheede, J. R., Wattiez, R., and Kettmann, R. (2005) Phosphorylation of histone deacetylase 7 by protein kinase D mediates T cell receptorinduced Nur77 expression and apoptosis. J. Exp. Med. 201, 793-804
29. Harrison, B. C., Kim, M. S., van Rooij, E., Plato, C. F., Papst, P. J., Vega, R. B., McAnally, J. A., Richardson, J. A., Bassel-Duby, R., Olson, E. N., and McKinsey, T. A. (2006) Regulation of cardiac stress signaling by protein kinase d1. Mol. Cell Biol. 26, 3875-3888
30. Vega, R. B., Harrison, B. C., Meadows, E., Roberts, C. R., Papst, P. J., Olson, E. N., and McKinsey, T. A. (2004) Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol. Cell Biol. 24, 8374-8385
31. Carnegie, G. K., Soughayer, J., Smith, F. D., Pedroja, B. S., Zhang, F., Diviani, D., Bristow, M. R., Kunkel, M. T., Newton, A. C., Langeberg, L. K., and Scott, J. D. (2008) AKAP-Lbc mobilizes a cardiac hypertrophy signaling pathway. Mol. Cell 32, 169-179
32. Chawla, S., Vanhoutte, P., Arnold, F. J., Huang, C. L., and Bading, H. (2003) Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J. Neurochem. 85, 151-159
33. 2+ signaling in cardiac myocyte excitation-transcription coupling. J. Clin. Invest. 116, 675-682
34. Ha, C. H., Wang, W., Jhun, B. S., Wong, C., Hausser, A., Pfizenmaier, K., McKinsey, T. A., Olson, E. N., and Jin, Z. G. (2008) Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J. Biol. Chem. 283, 14590-14599
35. Illi, B., Dello Russo, C., Colussi, C., Rosati, J., Pallaoro, M., Spallotta, F., Rotili, D., Valente, S., Ragone, G., Martelli, F., Biglioli, P., Steinkuhler, C., Gallinari, P., Mai, A., Capogrossi, M. C., and Gaetano, C. (2008) Nitric oxide modulates chromatin folding in human endothelial cells via protein phosphatase 2A activation and class II histone deacetylases nuclear shuttling. Circ. Res. 102, 51-58
36. Paroni, G., Cernotta, N., Dello Russo, C., Gallinari, P., Pallaoro, M., Foti, C., Talamo, F., Orsatti, L., Steinkuhler, C., and Brancolini, C. (2008) PP2A regulates HDAC4 nuclear import. Mol. Biol. Cell 19, 655-667
37. Parra, M., Mahmoudi, T., and Verdin, E. (2007) Myosin phosphatase dephosphorylates HDAC7, controls its nucleocytoplasmic shuttling, and inhibits apoptosis in thymocytes. Genes Dev. 21, 638-643
38. Francis, S. H., and Corbin, J. D. (1994) Structure and function of cyclic nucleotide-dependent protein kinases. Annu. Rev. Physiol. 56, 237-272
39. Baillie, G. S., Scott, J. D., and Houslay, M. D. (2005) Compartmentalisation of phosphodiesterases and protein kinase A. Opposites attract. FEBS Lett. 579, 3264-3270
40. Wong, W., and Scott, J. D. (2004) AKAP signalling complexes. Focal points in space and time. Nat. Rev. Mol. Cell Biol. 5, 959-970
41. Daniel, P. B., Walker, W. H., and Habener, J. F. (1998) Cyclic AMP signaling and gene regulation. Annu. Rev. Nutr. 18, 353-383
42. Montminy, M. (1997) Transcriptional regulation by cyclic AMP. Annu. Rev. Biochem. 66, 807-822
43. Shaywitz, A. J., and Greenberg, M. E. (1999) CREB. A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861
44. 2+ and cAMP on transcription mediated by MEF2D and cAMP-response element-binding protein in hippocampal neurons. J. Biol. Chem. 281, 27724-27732
45. Du, M., Perry, R. L., Nowacki, N. B., Gordon, J. W., Salma, J., Zhao, J., Aziz, A., Chan, J., Siu, K. W., and McDermott, J. C. (2008) Protein kinase A represses skeletal myogenesis by targeting myocyte enhancer factor 2D. Mol. Cell Biol. 28, 2952-2970
46. Kozhemyakina, E., Cohen, T., Yao, T. P., and Lassar, A. B. (2009) Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/MEF2 pathway. Mol. Cell Biol. 29, 5751-5762
47. Mihaylova, M. M., Vasquez, D. S., Ravnskjaer, K., Denechaud, P. D., Yu, R. T., Alvarez, J. G., Downes, M., Evans, R. M., Montminy, M., and Shaw, R. J. (2011) Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145, 607-621
48. Wang, B., Moya, N., Niessen, S., Hoover, H., Mihaylova, M. M., Shaw, R. J., Yates, J. R., 3rd, Fischer, W. H., Thomas, J. B., and Montminy, M. (2011) A hormone-dependent module regulating energy balance. Cell 145, 596-606
49. Collins, S. P., Reoma, J. L., Gamm, D. M., and Uhler, M. D. (2000) LKB1, a novel serine/threonine protein kinase and potential tumour suppressor, is phosphorylated by cAMP-dependent protein kinase (PKA) and prenylated in vivo. Biochem. J. 345, 673-680
50. Sapkota, G. P., Kieloch, A., Lizcano, J. M., Lain, S., Arthur, J. S., Williams, M. R., Morrice, N., Deak, M., and Alessi, D. R. (2001) Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/ STK11, at Ser431 by p90RSK and cAMP-dependent protein kinase, but not its farnesylation at Cys433, is essential for LKB1 to suppress cell growth. J. Biol. Chem. 276, 19469-19482
51. Screaton, R. A., Conkright, M. D., Katoh, Y., Best, J. L., Canettieri, G., Jeffries, S., Guzman, E., Niessen, S., Yates, J. R., 3rd, Takemori, H., Okamoto, M., and Montminy, M. (2004) The CREB coactivator TORC2 functions as a calcium-and cAMP-sensitive coincidence detector. Cell 119, 61-74
52. Wang, A. H., Kruhlak, M. J., Wu, J., Bertos, N. R., Vezmar, M., Posner, B. I., Bazett-Jones, D. P., and Yang, X. J. (2000) Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell Biol. 20, 6904-6912
53. Verdel, A., and Khochbin, S. (1999) Identification of a new family of higher eukaryotic histone deacetylases. Coordinate expression of differentiationdependent chromatin modifiers. J. Biol. Chem. 274, 2440-2445
54. Zhou, X., Marks, P. A., Rifkind, R. A., and Richon, V. M. (2001) Cloning and characterization of a histone deacetylase, HDAC9. Proc. Natl. Acad. Sci. U.S.A. 98, 10572-10577
55. Petrie, K., Guidez, F., Howell, L., Healy, L., Waxman, S., Greaves, M., and Zelent, A. (2003) The histone deacetylase 9 gene encodes multiple protein isoforms. J. Biol. Chem. 278, 16059-16072
56. Yuan, Z., Peng, L., Radhakrishnan, R., and Seto, E. (2010) Histone deacetylase 9 (HDAC9) regulates the functions of the ATDC (TRIM29) protein. J. Biol. Chem. 285, 39329-39338
57. Szyf, M., and Slack, A. D. (2000) Mechanisms of epigenetic silencing of the c21 gene in Y1 adrenocortical tumor cells. Endocr. Res. 26, 921-930
58. Magun, R., Boone, D. L., Tsang, B. K., and Sorisky, A. (1998) The effect of adipocyte differentiation on the capacity of 3T3-L1 cells to undergo apoptosis in response to growth factor deprivation. Int. J. Obes. Relat. Metab. Disord. 22, 567-571
59. Wang, A. H., Bertos, N. R., Vezmar, M., Pelletier, N., Crosato, M., Heng, H. H., Th'ng, J., Han, J., and Yang, X. J. (1999) HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol. Cell Biol. 19, 7816-7827
60. Katoh, Y., Takemori, H., Lin, X. Z., Tamura, M., Muraoka, M., Satoh, T., Tsuchiya, Y., Min, L., Doi, J., Miyauchi, A., Witters, L. A., Nakamura, H., and Okamoto, M. (2006) Silencing the constitutive active transcription factor CREB by the LKB1-SIK signaling cascade. FEBS J. 273, 2730-2748
61. Tiainen, M., Ylikorkala, A., and Makela, T. P. (1999) Growth suppression by Lkb1 is mediated by a G1 cell cycle arrest. Proc. Natl. Acad. Sci. U.S.A. 96, 9248-9251
62. Kudo, N., Matsumori, N., Taoka, H., Fujiwara, D., Schreiner, E. P., Wolff, B., Yoshida, M., and Horinouchi, S. (1999) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. U.S.A. 96, 9112-9117
63. McKinsey, T. A., Zhang, C. L., and Olson, E. N. (2000) Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulindependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc. Natl. Acad. Sci. U.S.A. 97, 14400-14405
64. Miska, E. A., Karlsson, C., Langley, E., Nielsen, S. J., Pines, J., and Kouzarides, T. (1999) HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J. 18, 5099-5107
65. Lemercier, C., Verdel, A., Galloo, B., Curtet, S., Brocard, M. P., and Khochbin, S. (2000) mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity. J. Biol. Chem. 275, 15594-15599
66. Borghi, S., Molinari, S., Razzini, G., Parise, F., Battini, R., and Ferrari, S. (2001) The nuclear localization domain of the MEF2 family of transcription factors shows member-specific features and mediates the nuclear import of histone deacetylase 4. J. Cell Sci. 114, 4477-4483
67. Wang, A. H., and Yang, X. J. (2001) Histone deacetylase 4 possesses intrinsic nuclear import and export signals. Mol. Cell Biol. 21, 5992-6005
68. Winter, B., Braun, T., and Arnold, H. H. (1993) cAMP-dependent protein kinase represses myogenic differentiation and the activity of the musclespecific helix-loop-helix transcription factors Myf-5 and MyoD. J. Biol. Chem. 268, 9869-9878
69. Choi, R. C., Siow, N. L., Zhu, S. Q., and Tsim, K. W. (2000) The cAMPdependent protein kinase mediates the expression of AChE in chick myotubes. Neuroreport 11, 801-806
70. Haberland, M., Montgomery, R. L., and Olson, E. N. (2009) The many roles of histone deacetylases in development and physiology. Implications for disease and therapy. Nat. Rev. Genet. 10, 32-42
71. Garren, L. D., Gill, G. N., Masui, H., and Walton, G. M. (1971) On the mechanism of action of ACTH. Recent Prog. Horm. Res. 27, 433-478
72. Wood, H. N., and Braun, A. C. (1973) 8-Bromoadenosine 3 :5-cyclic monophosphate as a promoter of cell division in excised tobacco pith parenchyma tissue. Proc. Natl. Acad. Sci. U.S.A. 70, 447-450
73. Taniguchi, M., Carreira, M. B., Smith, L. N., Zirlin, B. C., Neve, R. L., and Cowan, C. W. (2012) Histone deacetylase 5 limits cocaine reward through cAMP-induced nuclear import. Neuron 73, 108-120
74. 2+, calcineurin, and NF-AT. Cell 96, 611-614
75. Gwack, Y., Sharma, S., Nardone, J., Tanasa, B., Iuga, A., Srikanth, S., Okamura, H., Bolton, D., Feske, S., Hogan, P. G., and Rao, A. (2006)Agenomewide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441, 646-650
76. Shabb, J. B. (2001) Physiological substrates of cAMP-dependent protein kinase. Chem. Rev. 101, 2381-2411
77. Zhu, G., Fujii, K., Belkina, N., Liu, Y., James, M., Herrero, J., and Shaw, S. (2005) Exceptional disfavor for proline at the P-1 position among AGC and CAMK kinases establishes reciprocal specificity between them and the proline-directed kinases. J. Biol. Chem. 280, 10743-10748
78. Deng, X., Ewton, D. Z., Mercer, S. E., and Friedman, E. (2005) Mirk/dyrk1B decreases the nuclear accumulation of class II histone deacetylases during skeletal muscle differentiation. J. Biol. Chem. 280, 4894-4905
79. Greco, T. M., Yu, F., Guise, A. J., and Cristea, I. M. (2011) Nuclear import of histone deacetylase 5 by requisite nuclear localization signal phosphorylation. Mol. Cell Proteomics 10, M110.004317
80. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A., Brunak, S., and Mann, M. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3
81. Ha, C. H., Kim, J. Y., Zhao, J., Wang, W., Jhun, B. S., Wong, C., and Jin, Z. G. (2010) PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 107, 15467-15472
82. Harrison, B. C., Huynh, K., Lundgaard, G. L., Helmke, S. M., Perryman, M. B., and McKinsey, T. A. (2010) Protein kinase C-related kinase targets nuclear localization signals in a subset of class IIa histone deacetylases. FEBS Lett. 584, 1103-1110
83. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 10762-10767
84. Sui, S., Wang, J., Yang, B., Song, L., Zhang, J., Chen, M., Liu, J., Lu, Z., Cai, Y., Chen, S., Bi, W., Zhu, Y., He, F., and Qian, X. (2008) Phosphoproteome analysis of the human Chang liver cells using SCX and a complementary mass spectrometric strategy. Proteomics 8, 2024-2034
85. Li, X., Song, S., Liu, Y., Ko, S. H., and Kao, H. Y. (2004) Phosphorylation of the histone deacetylase 7 modulates its stability and association with 14-3-3 proteins. J. Biol. Chem. 279, 34201-34208
86. Potthoff, M. J., Wu, H., Arnold, M. A., Shelton, J. M., Backs, J., McAnally, J., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2007) Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J. Clin. Invest. 117, 2459-2467
87. Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H., and Hay, R. T. (2001) Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276, 35368-35674
88. Kirsh, O., Seeler, J. S., Pichler, A., Gast, A., Muller, S., Miska, E., Mathieu, M., Harel-Bellan, A., Kouzarides, T., Melchior, F., and Dejean, A. (2002) The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21, 2682-2691
89. Walkinshaw, D. R., Weist, R., Kim, G.-W., You, L., Xiao, L., Nie, J., Li, C. S., Zhao, S., and Yang, X. J. (February 7, 2013) The tumor suppressor kinase LKB1 activates SIK2 and SIK3 to stimulate nuclear export of class IIa histone deacetylases. J. Biol. Chem. 10.1074/jbc.M113.456996