Mitogen-activated protein kinase phosphatase 2 regulates histone H3 phosphorylation via interaction with vaccinia-related kinase 1

Molecular Biology of the Cell

Volumn 24, Issue 3, 2013, Pages 373-384

  Jeong, Min Woo ^a   Kang, Tae Hong ^a   Kim, Wanil ^b   Choi, Yoon Ha ^a   Kim, Kyong Tai ^a,b  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b Dong A University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 2; PHOSPHATASE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; VACCINIA RELATED KINASE 1;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CHROMATIN; DOWN REGULATION; ENZYME ACTIVITY; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL;

CELL DIVISION; CHROMATIN; DUAL-SPECIFICITY PHOSPHATASES; HELA CELLS; HISTONES; HUMANS; HYDROGEN PEROXIDE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES;

EID: 84873394986     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-06-0456     Document Type: Article

References (54)

1. Ajiro K, Yasuda H, Tsuji H (1996a). Vanadate triggers the transition from chromosome condensation to decondensation in a mitotic mutant (tsTM13) inactivation of p34cdc2/H1 kinase and dephosphorylation of mitosis-specific histone H3. Eur J Biochem 241, 923-930.
2. Ajiro K, Yoda K, Utsumi K, Nishikawa Y (1996b). Alteration of cell cycle-dependent histone phosphorylations by okadaic acid. Induction of mitosis-specific H3 phosphorylation and chromatin condensation in mammalian interphase cells. J Biol Chem 271, 13197-13201.
3. Baek SH (2011). When signaling kinases meet histones and histone modifiers in the nucleus. Mol Cell 42, 274-284.
4. Banerjee T, Chakravarti D (2011). A peek into the complex realm of histone phosphorylation. Mol Cell Biol 31, 4858-4872.
5. Boutros T, Chevet E, Metrakos P (2008). Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol Rev 60, 261-310.
6. Britson JS, Barton F, Balko JM, Black EP (2009). Deregulation of DUSP activity in EGFR-mutant lung cancer cell lines contributes to sustained ERK1/2 signaling. Biochem Biophys Res Commun 390, 849-854.
7. Brondello JM, Brunet A, Pouyssegur J, McKenzie FR (1997). The dual specificity mitogen-activated protein kinase phosphatase-1 and -2 are induced by the p42/p44MAPK cascade. J Biol Chem 272, 1368-1376.
8. Cadalbert L, Sloss CM, Cameron P, Plevin R (2005). Conditional expression of MAP kinase phosphatase-2 protects against genotoxic stress-induced apoptosis by binding and selective dephosphorylation of nuclear activated c-jun N-terminal kinase. Cell Signal 17, 1254-1264.
9. Choi YH, Park CH, Kim W, Ling H, Kang A, Chang MW, Im SK, Jeong HW, Kong YY, Kim KT (2010). Vaccinia-related kinase 1 is required for the maintenance of undifferentiated spermatogonia in mouse male germ cells. PLoS One 5, e15254.
10. Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, Sen S, Allis CD, Sassone-Corsi P (2002). Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 22, 874-885.
11. Dai J, Higgins JM (2005). Haspin: a mitotic histone kinase required for metaphase chromosome alignment. Cell Cycle 4, 665-668.
12. Dai J, Sultan S, Taylor SS, Higgins JM (2005). The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev 19, 472-488.
13. Dickinson RJ, Keyse SM (2006). Diverse physiological functions for dual-specificity MAP kinase phosphatases. J Cell Sci 119, 4607-4615.
14. Emanuele MJ, Lan W, Jwa M, Miller SA, Chan CS, Stukenberg PT (2008). Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J Cell Biol 181, 241-254.
15. Farooq A, Zhou MM (2004). Structure and regulation of MAPK phosphatases. Cell Signal 16, 769-779.
16. Girdler F, Sessa F, Patercoli S, Villa F, Musacchio A, Taylor S (2008). Molecular basis of drug resistance in Aurora kinases. Chem Biol 15, 552-562.
17. Gorjanacz M, Klerkx EP, Galy V, Santarella R, Lopez-Iglesias C, Askjaer P, Mattaj IW (2007). Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J 26, 132-142.
18. Guan KL, Butch E (1995). Isolation and characterization of a novel dual specific phosphatase, HVH2, which selectively dephosphorylates the mitogen-activated protein kinase. J Biol Chem 270, 7197-7202.
19. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (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.
20. Hsu JY et al. (2000). Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102, 279-291.
21. Jeffrey KL, Camps M, Rommel C, Mackay CR (2007). Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat Rev Drug Discov 6, 391-402.
22. Johnson GL, Lapadat R (2002). Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298, 1911-1912.
23. Kang TH, Kim KT (2006). Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat Cell Biol 8, 863-869.
24. Kang TH, Park DY, Choi YH, Kim KJ, Yoon HS, Kim KT (2007). Mitotic histone H3 phosphorylation by vaccinia-related kinase 1 in mammalian cells. Mol Cell Biol 27, 8533-8546.
25. Kang TH, Park DY, Kim W, Kim KT (2008). VRK1 phosphorylates CREB and mediates CCND1 expression. J Cell Sci 121, 3035-3041.
26. Keyse SM (2008). Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev 27, 253-261.
27. Kim W, Chakraborty G, Kim S, Shin J, Park CH, Jeong MW, Bharatham N, Yoon HS, Kim KT (2012). Macro histone H2A1.2 (MacroH2A1) protein suppresses mitotic kinase VRK1 during interphase. J Biol Chem 287, 5278-5289.
28. Kinney CM, Chandrasekharan UM, Yang L, Shen J, Kinter M, McDermott MS, DiCorleto PE (2009). Histone H3 as a novel substrate for MAP kinase phosphatase-1. Am J Physiol Cell Physiol 296, C242-C249.
29. Lawan A, Al-Harthi S, Cadalbert L, McCluskey AG, Shweash M, Grassia G, Grant A, Boyd M, Currie S, Plevin R (2011). Deletion of the dual specific phosphatase-4 (DUSP-4) gene reveals an essential non-redundant role for MAP kinase phosphatase-2 (MKP-2) in proliferation and cell survival. J Biol Chem 286, 12933-12942.
30. Lee JH, Jeong MW, Kim W, Choi YH, Kim KT (2008). Cooperative roles of c-Abl and Cdk5 in regulation of p53 in response to oxidative stress. J Biol Chem 283, 19826-19835.
31. Murnion ME, Adams RR, Callister DM, Allis CD, Earnshaw WC, Swedlow JR (2001). Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J Biol Chem 276, 26656-26665.
32. Nichols RJ, Traktman P (2004). Characterization of three paralogous members of the mammalian vaccinia related kinase family. J Biol Chem 279, 7934-7946.
33. Nichols RJ, Wiebe MS, Traktman P (2006). The vaccinia-related kinases phosphorylate the N′ terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol Biol Cell 17, 2451-2464.
34. Ozawa K (2008). Reduction of phosphorylated histone H3 serine 10 and serine 28 cell cycle marker intensities after DNA damage. Cytometry A 73, 517-527.
35. Prigent C, Dimitrov S (2003). Phosphorylation of serine 10 in histone H3, what for. J Cell Sci 116, 3677-3685.
36. Robinson CJ, Sloss CM, Plevin R (2001). Inactivation of JNK activity by mitogen-activated protein kinase phosphatase-2 in EAhy926 endothelial cells is dependent upon agonist-specific JNK translocation to the nucleus. Cell Signal 13, 29-41.
37. Russell P, Hennessy BT, Li J, Carey MS, Bast RC, Freeman T, Venkitaraman AR (2012). Cyclin G1 regulates the outcome of taxane-induced mitotic checkpoint arrest. Oncogene 31, 2450-2460.
38. Sanz-Garcia M, Lopez-Sanchez I, Lazo PA (2008). Proteomics identification of nuclear Ran GTPase as an inhibitor of human VRK1 and VRK2 (vaccinia-related kinase) activities. Mol Cell Proteomics 7, 2199-2214.
39. Sauve DM, Anderson HJ, Ray JM, James WM, Roberge M (1999). Phosphorylation-induced rearrangement of the histone H3 NH2-terminal domain during mitotic chromosome condensation. J Cell Biol 145, 225-235.
40. Schober CS, Aydiner F, Booth CJ, Seli E, Reinke V (2011). The kinase VRK1 is required for normal meiotic progression in mammalian oogenesis. Mech Dev 128, 178-190.
41. Sevilla A, Santos CR, Barcia R, Vega FM, Lazo PA (2004a). c-Jun phosphorylation by the human vaccinia-related kinase 1 (VRK1) and its cooperation with the N-terminal kinase of c-Jun (JNK). Oncogene 23, 8950-8958.
42. Sevilla A, Santos CR, Vega FM, Lazo PA (2004b). Human vaccinia-related kinase 1 (VRK1) activates the ATF2 transcriptional activity by novel phosphorylation on Thr-73 and Ser-62 and cooperates with JNK. J Biol Chem 279, 27458-27465.
43. Shen WH, Wang J, Wu J, Zhurkin VB, Yin Y (2006). Mitogen-activated protein kinase phosphatase 2: a novel transcription target of p53 in apoptosis. Cancer Res 66, 6033-6039.
44. Sloss CM, Cadalbert L, Finn SG, Fuller SJ, Plevin R (2005). Disruption of two putative nuclear localization sequences is required for cytosolic localization of mitogen-activated protein kinase phosphatase-2. Cell Signal 17, 709-716.
45. Sugiyama K, Sugiura K, Hara T, Sugimoto K, Shima H, Honda K, Furukawa K, Yamashita S, Urano T (2002). Aurora-B associated protein phosphatases as negative regulators of kinase activation. Oncogene 21, 3103-3111.
46. Theodosiou A, Ashworth A (2002). MAP kinase phosphatases. Genome Biol 3, reviews3009-1-10.
47. Torres C, Francis MK, Lorenzini A, Tresini M, Cristofalo VJ (2003). Metabolic stabilization of MAP kinase phosphatase-2 in senescence of human fibroblasts. Exp Cell Res 290, 195-206.
48. Tresini M, Lorenzini A, Torres C, Cristofalo VJ (2007). Modulation of replicative senescence of diploid human cells by nuclear ERK signaling. J Biol Chem 282, 4136-4151.
49. Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA (1998). Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci 111, 3497-3506.
50. Vega FM, Sevilla A, Lazo PA (2004). p53 Stabilization and accumulation induced by human vaccinia-related kinase 1. Mol Cell Biol 24, 10366-10380.
51. Wang F, Ulyanova NP, van der Waal MS, Patnaik D, Lens SM, Higgins JM (2011). A positive feedback loop involving Haspin and Aurora B promotes CPC accumulation at centromeres in mitosis. Curr Biol 21, 1061-1069.
52. Wang J, Shen WH, Jin YJ, Brandt-Rauf PW, Yin Y (2007). A molecular link between E2F-1 and the MAPK cascade. J Biol Chem 282, 18521-18531.
53. Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD (1999). Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99-109.
54. Wiebe MS, Nichols RJ, Molitor TP, Lindgren JK, Traktman P (2010). Mice deficient in the serine/threonine protein kinase VRK1 are infertile due to a progressive loss of spermatogonia. Biol Reprod 82, 182-192.