Phosphatase 1 nuclear targeting subunit is an essential regulator of M-phase entry, maintenance, and exit

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23745-23752

  Fisher, Laura A ^a   Wang, Ling ^a   Wu, Lan ^b   Peng, Aimin ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MAINTENANCE; PROTEINS;

ANAPHASE-PROMOTING COMPLEX/CYCLOSOME; IMMUNODEPLETION; MASTER REGULATORS; MITOTIC PROGRESSION; NUCLEAR TARGETING; OVER-EXPRESSION; PROTEIN PHOSPHATASE-1; PROTEIN PHOSPHORYLATION;

PHOSPHATASES;

PHOSPHATASE 1 NUCLEAR TARGETING SUBUNIT; REGULATOR PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; NUCLEAR PROTEIN; PPP1R10 PROTEIN, HUMAN; PRIMER DNA; RNA BINDING PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CONTROLLED STUDY; MEIOSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; UBIQUITINATION; XENOPUS; ANIMAL; CELL DIVISION; METABOLISM; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; CELL DIVISION; DNA PRIMERS; DNA-BINDING PROTEINS; MEIOSIS; MITOSIS; NUCLEAR PROTEINS; PROTEOLYSIS; RNA-BINDING PROTEINS; UBIQUITINATION; XENOPUS;

EID: 84906569790     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.572149     Document Type: Article

References (47)

1. Janssen, A., and Medema, R. H. (2011) Mitosis as an anti-cancer target. Oncogene 30, 2799-2809
2. Nigg, E. A. (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32
3. Malumbres, M., Harlow, E., Hunt, T., Hunter, T., Lahti, J. M., Manning, G., Morgan, D. O., Tsai, L. H., and Wolgemuth, D. J. (2009) Cyclin-dependent kinases: a family portrait. Nat. Cell Biol. 11, 1275-1276
4. Lens, S. M., Voest, E. E., and Medema, R. H. (2010) Shared and separate functions of Polo-like kinases and Aurora kinases in cancer. Nat. Rev. Cancer 10, 825-841
5. Mochida, S., and Hunt, T. (2012) Protein phosphatases and their regulation in the control of mitosis. EMBO Rep. 13, 197-203
6. Bollen, M., Gerlich, D. W., and Lesage, B. (2009) Mitotic phosphatases: from entry guards to exit guides. Trends Cell Biol. 19, 531-541
7. Wurzenberger, C., and Gerlich, D. W. (2011) Phosphatases:providing safe passage through mitotic exit. Nat. Rev. Mol. Cell Biol. 12, 469-482
8. Stegmeier, F., and Amon, A. (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38, 203-232
9. Mocciaro, A., and Schiebel, E. (2010) Cdc14: a highly conserved family of phosphatases with non-conserved functions? J. Cell Sci. 123, 2867-2876
10. Moorhead, G. B., Trinkle-Mulcahy, L., and Ulke-Lemée, A. (2007) Emerging roles of nuclear protein phosphatases. Nat. Rev. Mol. Cell Biol. 8, 234-244
11. Peng, A., and Maller, J. L. (2010) Serine/threonine phosphatases in the DNA damage response and cancer. Oncogene 29, 5977-5988
12. Castilho, P. V., Williams, B. C., Mochida, S., Zhao, Y., and Goldberg, M. L. (2009) The M phase kinase Greatwall (Gwl) promotes inactivation of PP2A/B55δ, a phosphatase directed against CDK phosphosites. Mol. Biol. Cell 20, 4777-4789
13. Mochida, S., Ikeo, S., Gannon, J., and Hunt, T. (2009) Regulated activity of PP2A-B55δ is crucial for controlling entry into and exit from mitosis in Xenopus egg extracts. EMBO J. 28, 2777-2785
14. Manchado, E., Guillamot, M., de Cárcer, G., Eguren, M., Trickey, M., García-Higuera, I., Moreno, S., Yamano, H., Cañamero, M., and Malumbres, M. (2010) Targeting mitotic exit leads to tumor regression in vivo: modulation by Cdk1, Mastl, and the PP2A/B55α,δ phosphatase. Cancer Cell 18, 641-654
15. Gharbi-Ayachi, A., Labbé, J. C., Burgess, A., Vigneron, S., Strub, J. M., Brioudes, E., Van-Dorsselaer, A., Castro, A., and Lorca, T. (2010) The substrate of Greatwall kinase, Arpp19, controls mitosis by inhibiting protein phosphatase 2A. Science 330, 1673-1677
16. Mochida, S., Maslen, S. L., Skehel, M., and Hunt, T. (2010) Greatwall phosphorylates an inhibitor of protein phosphatase 2A that is essential for mitosis. Science 330, 1670-1673
17. Emanuele, M. J., Lan, W., Jwa, M., Miller, S. A., Chan, C. S., and Stukenberg, P. T. (2008) Aurora B kinase and protein phosphatase 1 have opposing roles in modulating kinetochore assembly. J. Cell Biol. 181, 241-254
18. Fuller, B. G., Lampson, M. A., Foley, E. A., Rosasco-Nitcher, S., Le, K. V., Tobelmann, P., Brautigan, D. L., Stukenberg, P. T., and Kapoor, T. M. (2008) Midzone activation of Aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 453, 1132-1136
19. Tsai, M. Y., Wiese, C., Cao, K., Martin, O., Donovan, P., Ruderman, J., Prigent, C., and Zheng, Y. (2003) A Ran signalling pathway mediated by the mitotic kinase AuroraAin spindle assembly. Nat. Cell Biol. 5, 242-248
20. Allen, P. B., Kwon, Y. G., Nairn, A. C., and Greengard, P. (1998) Isolation and characterization of PNUTS, a putative protein phosphatase 1 nuclear targeting subunit. J. Biol. Chem. 273, 4089-4095
21. Kim, Y. M., Watanabe, T., Allen, P. B., Kim, Y. M., Lee, S. J., Greengard, P., Nairn, A. C., and Kwon, Y. G. (2003) PNUTS, a protein phosphatase 1 (PP1) nuclear targeting subunit: characterization of its PP1-And RNAbinding domains and regulation by phosphorylation. J. Biol. Chem. 278, 13819-13828
22. Lee, J. H., You, J., Dobrota, E., and Skalnik, D. G. (2010) Identification and characterization of a novel human PP1 phosphatase complex. J. Biol. Chem. 285, 24466-24476
23. Bounaix Morand du Puch, C., Barbier, E., Kraut, A., Couté, Y., Fuchs, J., Buhot, A., Livache, T., Sève, M., Favier, A., Douki, T., Gasparutto, D., Sauvaigo, S., and Breton, J. (2011) TOX4 and its binding partners recognize DNA adducts generated by platinum anticancer drugs. Arch. Biochem. Biophys. 507, 296-303
24. Landsverk, H. B., Mora-Bermúdez, F., Landsverk, O. J., Hasvold, G., Naderi, S., Bakke, O., Ellenberg, J., Collas, P., Syljuåsen, R. G., and Küntziger, T. (2010) The protein phosphatase 1 regulator PNUTS is a new component of the DNA damage response. EMBO Rep. 11, 868-875
25. Kim, H., Lee, O. H., Xin, H., Chen, L. Y., Qin, J., Chae, H. K., Lin, S. Y., Safari, A., Liu, D., and Songyang, Z. (2009) TRF2 functions as a protein hub and regulates telomere maintenance by recognizing specific peptide motifs. Nat. Struct. Mol. Biol. 16, 372-379
26. Boon, R. A., Iekushi, K., Lechner, S., Seeger, T., Fischer, A., Heydt, S., Kaluza, D., Tréguer, K., Carmona, G., Bonauer, A., Horrevoets, A. J., Didier, N., Girmatsion, Z., Biliczki, P., Ehrlich, J. R., Katus, H. A., Müller, O. J., Potente, M., Zeiher, A. M., Hermeking, H., and Dimmeler, S. (2013) MicroRNA-34a regulates cardiac ageing and function. Nature 495, 107-110
27. Udho, E., Tedesco, V. C., Zygmunt, A., and Krucher, N. A. (2002) PNUTS (phosphatase nuclear targeting subunit) inhibits retinoblastoma-directed PP1 activity. Biochem. Biophys. Res. Commun. 297, 463-467
28. Krucher, N. A., Rubin, E., Tedesco, V. C., Roberts, M. H., Sherry, T. C., and De Leon, G. (2006) Dephosphorylation of Rb (Thr-821) in response to cell stress. Exp. Cell Res. 312, 2757-2763
29. Kavela, S., Shinde, S. R., Ratheesh, R., Viswakalyan, K., Bashyam, M. D., Gowrishankar, S., Vamsy, M., Pattnaik, S., Rao, S., Sastry, R. A., Srinivasulu, M., Chen, J., and Maddika, S. (2013) PNUTS functions as a protooncogene by sequestering PTEN. Cancer Res. 73, 205-214
30. Landsverk, H. B., Kirkhus, M., Bollen, M., Küntziger, T., and Collas, P. (2005) PNUTS enhances in vitro chromosome decondensation in a PP1-dependent manner. Biochem. J. 390, 709-717
31. Peng, A., Wang, L., and Fisher, L. A. (2011) Greatwall and Polo-like kinase 1 coordinate to promote checkpoint recovery. J Biol. Chem. 286, 28996-29004
32. Peng, A., Lewellyn, A. L., Schiemann, W. P., and Maller, J. L. (2010) Repo-Man controls a protein phosphatase 1-dependent threshold for DNA damage checkpoint activation. Curr. Biol. 20, 387-396
33. Crane, R. F., and Ruderman, J. V. (2006) Using Xenopus oocyte extracts to study signal transduction. Methods Mol. Biol. 322, 435-443
34. Philpott, A., and Yew, P. R. (2005) The Xenopus cell cycle: an overview. Methods Mol. Biol. 296, 95-112
35. Lee, S. J., Lee, J. K., Maeng, Y. S., Kim, Y. M., and Kwon, Y. G. (2009) Langerhans cell protein 1 (LCP1) binds to PNUTS in the nucleus: implications for this complex in transcriptional regulation. Exp. Mol. Med. 41, 189-200
36. Jerebtsova, M., Klotchenko, S. A., Artamonova, T. O., Ammosova, T., Washington, K., Egorov, V. V., Shaldzhyan, A. A., Sergeeva, M. V., Zatulovskiy, E. A., Temkina, O. A., Petukhov, M. G., Vasin, A. V., Khodorkovskii, M. A., Orlov, Y. N., and Nekhai, S. (2011) Mass spectrometry and biochemical analysis of RNA polymerase II: targeting by protein phosphatase-1. Mol. Cell. Biochem. 347, 79-87
37. Tunquist, B. J., and Maller, J. L. (2003) Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev. 17, 683-710
38. Wu, J. Q., Guo, J. Y., Tang, W., Yang, C. S., Freel, C. D., Chen, C., Nairn, A. C., and Kornbluth, S. (2009) PP1-mediated dephosphorylation of phosphoproteins at mitotic exit is controlled by inhibitor-1 and PP1 phosphorylation. Nat. Cell Biol. 11, 644-651
39. Margolis, S. S., Walsh, S., Weiser, D. C., Yoshida, M., Shenolikar, S., and Kornbluth, S. (2003) PP1 control ofMphase entry exerted through 14-3-3-regulated Cdc25 dephosphorylation. Embo J. 22, 5734-5745
40. Torres, J. Z., Ban K. H., and Jackson, P. K. (2010) A specific form of phospho protein phosphatase 2 regulates anaphase-promoting complex/cyclosome association with spindle poles. Mol. Biol. Cell 21, 897-904
41. Sullivan, M., and Morgan, D. O. (2007) Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8, 894-903
42. Castro, A., Bernis, C., Vigneron, S., Labbé, J. C., and Lorca, T. (2005) The anaphase-promoting complex: a key factor in the regulation of cell cycle. Oncogene 24, 314-325
43. Liu, J., Grimison, B., and Maller, J. L. (2007) New insight into metaphase arrest by cytostatic factor: from establishment to release. Oncogene 26, 1286-1289
44. Araki, M., Yu, H., and Asano, M. (2005) A novel motif governs APC-dependent degradation of Drosophila ORC1 in vivo. Genes Dev. 19, 2458-2465
45. Mochida, S., and Hunt, T. (2007) Calcineurin is required to release Xenopus egg extracts from meiotic M phase. Nature 449, 336-340
46. Voets, E., and Wolthuis R. M. (2010) MASTL is the human orthologue of Greatwall kinase that facilitates mitotic entry, anaphase and cytokinesis. Cell Cycle 9, 3591-3601
47. Burgess, A., Vigneron, S., Brioudes, E., Labbé, J. C., Lorca, T., and Castro, A. (2010) Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance. Proc. Natl. Acad. Sci. U. S. A. 107, 12564-12569