A chromatin-bound kinase, ERK8, protects genomic integrity by inhibiting HDM2-mediated degradation of the DNA clamp PCNA

Journal of Cell Biology

Volumn 190, Issue 4, 2010, Pages 575-586

  Groehler, Angela L ^a,b   Lannigan, Deborah A ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; PROTEIN MDM2; STRESS ACTIVATED PROTEIN KINASE 1; CHROMATIN; DNA; ERK8 PROTEIN, HUMAN; MDM2 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BINDING; RAN PROTEIN; SMALL INTERFERING RNA;

ARTICLE; BREAST EPITHELIUM; CELL CYCLE REGULATION; CELL TRANSFORMATION; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA DEGRADATION; DNA METABOLISM; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN METABOLISM; PROTEIN MOTIF; PROTEIN STABILITY; CELL CYCLE; CELL LINE; CYTOLOGY; DNA REPAIR; EPITHELIUM CELL; GENETICS; MAMMARY GLAND; METABOLISM; PHYSIOLOGY;

CELL CYCLE; CELL LINE; CHROMATIN; DNA; DNA DAMAGE; DNA REPAIR; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENOMIC INSTABILITY; HUMANS; MAMMARY GLANDS, HUMAN; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MDM2; RAN GTP-BINDING PROTEIN; RNA, SMALL INTERFERING;

EID: 77955904679     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201002124     Document Type: Article

References (51)

1. Abe, M.K., M.P. Saelzler, R. Espinosa III, K.T. Kahle, M.B. Hershenson, M.M. Le Beau, and M.R. Rosner. 2002. ERK8, a new member of the mitogen-activated protein kinase family. J. Biol. Chem. 277:16733-16743. doi:10.1074/jbc. M112483200
2. Andersen, P.L., F. Xu, and W. Xiao. 2008. Eukaryotic DNA damage tolerance and translesion synthesis through covalent modifications of PCNA. Cell Res. 18:162-173. doi:10.1038/cr.2007.114
3. Avkin, S., Z. Sevilya, L. Toube, N. Geacintov, S.G. Chaney, M. Oren, and Z. Livneh. 2006. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol. Cell. 22:407-413. doi:10.1016/j.molcel.2006.03.022
4. Azam, N., M. Vairapandi, W. Zhang, B. Hoffman, and D.A. Liebermann. 2001. Interaction of CR6 (GADD45gamma ) with proliferating cell nuclear antigen impedes negative growth control. J. Biol. Chem. 276:2766-2774. doi:10.1074/jbc.M005626200
5. Banks, D., M. Wu, L.A. Higa, N. Gavrilova, J. Quan, T. Ye, R. Kobayashi, H. Sun, and H. Zhang. 2006. L2DTL/CDT2 and PCNA interact with p53 and regulate p53 polyubiquitination and protein stability through MDM2 and CUL4A/DDB1 complexes. Cell Cycle. 5:1719-1729.
6. Black, E.P., T. Hallstrom, H.K. Dressman, M. West, and J.R. Nevins. 2005. Distinctions in the specificity of E2F function revealed by gene expression signatures. Proc. Natl. Acad. Sci. USA. 102:15948-15953. doi:10.1073/pnas. 0504300102
7. Coulombe, P., and S. Meloche. 2007. Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochim. Biophys. Acta. 1773:1376-1387. doi:10.1016/j.bbamcr.2006.11.001 (Pubitemid 47125971)
8. Das-Bradoo, S., H.D. Nguyen, J.L. Wood, R.M. Ricke, J.C. Haworth, and A.K. Bielinsky. 2010. Defects in DNA ligase I trigger PCNA ubiquitylation at Lys 107. Nat. Cell Biol. 12:74-79. doi:10.1038/ncb2007
9. Eisinger-Mathason, T.S., J. Andrade, A.L. Groehler, D.E. Clark, T.L. Muratore- Schroeder, L. Pasic, J.A. Smith, J. Shabanowitz, D.F. Hunt, I.G. Macara, and D.A. Lannigan. 2008. Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol. Cell. 31:722-736. doi:10.1016/j.molcel.2008.06.025
10. Essers, J., A.F. Theil, C. Baldeyron, W.A. van Cappellen, A.B. Houtsmuller, R. Kanaar, and W. Vermeulen. 2005. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25:9350-9359. doi:10 .1128/MCB.25.21.9350-9359.2005
11. Gary, R., D.L. Ludwig, H.L. Cornelius, M.A. MacInnes, and M.S. Park. 1997. The DNA repair endonuclease XPG binds to proliferating cell nuclear antigen (PCNA) and shares sequence elements with the PCNA-binding regions of FEN-1 and cyclin-dependent kinase inhibitor p21. J. Biol. Chem. 272:24522-24529. doi:10.1074/jbc.272.39.24522
12. Gilljam, K.M., E. Feyzi, P.A. Aas, M.M. Sousa, R. Müller, C.B. Vågbø, T.C. Catterall, N.B. Liabakk, G. Slupphaug, F. Drabløs, et al. 2009. Identification of a novel, widespread, and functionally important PCNA-binding motif. J. Cell Biol. 186:645-654. doi:10.1083/jcb.200903138
13. Gomes, X.V., and P.M. Burgers. 2000. Two modes of FEN1 binding to PCNA regulated by DNA. EMBO J. 19:3811-3821. doi:10.1093/emboj/19.14.3811
14. Halazonetis, T.D., V.G. Gorgoulis, and J. Bartek. 2008. An oncogene-induced DNA damage model for cancer development. Science. 319:1352-1355. doi:10.1126/science.1140735
15. Havens, C.G., and J.C. Walter. 2009. Docking of a specialized PIP Box onto chromatin-bound PCNA creates a degron for the ubiquitin ligase CRL4Cdt2. Mol. Cell. 35:93-104. doi:10.1016/j.molcel.2009.05.012
16. Henderson, D.S., S.S. Banga, T.A. Grigliatti, and J.B. Boyd. 1994. Mutagen sensitivity and suppression of position-effect variegation result from mutations in mus209, the Drosophila gene encoding PCNA. EMBO J. 13:1450-1459.
17. Her, J.H., S. Lakhani, K. Zu, J. Vila, P. Dent, T.W. Sturgill, and M.J. Weber. 1993. Dual phosphorylation and autophosphorylation in mitogen-activated protein (MAP) kinase activation. Biochem. J. 296:25-31.
18. Hoege, C., B. Pfander, G.L. Moldovan, G. Pyrowolakis, and S. Jentsch. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature. 419:135-141. doi:10.1038/nature00991 (Pubitemid 35025438)
19. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature. 411:366-374. doi:10.1038/35077232
20. Izumi, M., F. Yatagai, and F. Hanaoka. 2001. Cell cycle-dependent proteolysis and phosphorylation of human Mcm10. J. Biol. Chem. 276:48526-48531. doi:10.1074/jbc.M101463200
21. Jaskulski, D., J.K. deRiel, W.E. Mercer, B. Calabretta, and R. Baserga. 1988. Inhibition of cellular proliferation by antisense oligodeoxynucleotides to PCNA cyclin. Science. 240:1544-1546. doi:10.1126/science.2897717
22. Jørgensen, S., I. Elvers, M.B. Trelle, T. Menzel, M. Eskildsen, O.N. Jensen, T. Helleday, K. Helin, and C.S. Sørensen. 2007. The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 179:1337-1345. doi:10.1083/jcb.200706150
23. Kedar, P.S., S.J. Kim, A. Robertson, E. Hou, R. Prasad, J.K. Horton, and S.H. Wilson. 2002. Direct interaction between mammalian DNA polymerase beta and proliferating cell nuclear antigen. J. Biol. Chem. 277:31115-31123. doi:10.1074/jbc.M201497200
24. Klevernic, I.V., M.J. Stafford, N. Morrice, M. Peggie, S. Morton, and P. Cohen. 2006. Characterization of the reversible phosphorylation and activation of ERK8. Biochem. J. 394:365-373. doi:10.1042/BJ20051288
25. Klevernic, I.V., N.M. Martin, and P. Cohen. 2009. Regulation of the activity and expression of ERK8 by DNA damage. FEBS Lett. 583:680-684. doi:10.1016/j.febslet.2009.01.011
26. Malliri, A., S. van Es, S. Huveneers, and J.G. Collard. 2004. The Rac exchange factor Tiam1 is required for the establishment and maintenance of cadherin-based adhesions. J. Biol. Chem. 279:30092-30098. doi:10.1074/jbc. M401192200 (Pubitemid 38937931)
27. Martin, K., D. Trouche, C. Hagemeier, T.S. Sørensen, N.B. La Thangue, and T. Kouzarides. 1995. Stimulation of E2F1/DP1 transcriptional activity by MDM2 oncoprotein. Nature. 375:691-694. doi:10.1038/375691a0
28. McCaffrey, L.M., and I.G. Macara. 2009. The Par3/aPKC interaction is essential for end bud remodeling and progenitor differentiation during mammary gland morphogenesis. Genes Dev. 23:1450-1460. doi:10.1101/gad.1795909
29. Moldovan, G.L., B. Pfander, and S. Jentsch. 2007. PCNA, the maestro of the replication fork. Cell. 129:665-679. doi:10.1016/j.cell.2007.05.003
30. Mortusewicz, O., and H. Leonhardt. 2007. XRCC1 and PCNA are loading platforms with distinct kinetic properties and different capacities to respond to multiple DNA lesions. BMC Mol. Biol. 8:81. doi:10.1186/1471-2199-8-81
31. Naryzhny, S.N., and H. Lee. 2001. Protein profiles of the Chinese hamster ovary cells in the resting and proliferating stages. Electrophoresis. 22: 1764-1775. doi:10.1002/1522-2683(200105)22:9〈1764::AID-ELPS1764〉 3.0.CO;2-V
32. Naryzhny, S.N., and H. Lee. 2004. The post-translational modifications of proliferating cell nuclear antigen: acetylation, not phosphorylation, plays an important role in the regulation of its function. J. Biol. Chem. 279:20194-20199. doi:10.1074/jbc.M312850200
33. Rogakou, E.P., C. Boon, C. Redon, and W.M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905-916. doi:10.1083/jcb.146.5.905
34. Saal, L.H., S.K. Gruvberger-Saal, C. Persson, K. Lövgren, M. Jumppanen, J. Staaf, G. Jönsson, M.M. Pires, M. Maurer, K. Holm, et al. 2008. Recurrent gross mutations of the PTEN tumor suppressor gene in breast cancers with deficient DSB repair. Nat. Genet. 40:102-107. doi:10.1038/ng.2007. 39
35. Scorah, J., M.Q. Dong, J.R. Yates III, M. Scott, D. Gillespie, and C.H. McGowan. 2008. A conserved proliferating cell nuclear antigen-interacting protein sequence in Chk1 is required for checkpoint function. J. Biol. Chem. 283:17250-17259. doi:10.1074/jbc.M800369200
36. Sedelnikova, O.A., D.R. Pilch, C. Redon, and W.M. Bonner. 2003. Histone H2AX in DNA damage and repair. Cancer Biol. Ther. 2:233-235.
37. Sporbert, A., A. Gahl, R. Ankerhold, H. Leonhardt, and M.C. Cardoso. 2002. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol. Cell. 10:1355-1365. doi:10.1016/S1097-2765(02)00729-3
38. St Onge, R.P., C.M. Udell, R. Casselman, and S. Davey. 1999. The human G2 checkpoint control protein hRAD9 is a nuclear phosphoprotein that forms complexes with hRAD1 and hHUS1. Mol. Biol. Cell. 10:1985-1995.
39. Stevens, C., and N.B. La Thangue. 2003. E2F and cell cycle control: a double-edged sword. Arch. Biochem. Biophys. 412:157-169. doi:10.1016/S0003- 9861(03)00054-7 (Pubitemid 36344139)
40. Tanoue, T., M. Adachi, T. Moriguchi, and E. Nishida. 2000. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2:110-116. doi:10.1038/35000065
41. Tanoue, T., R. Maeda, M. Adachi, and E. Nishida. 2001. Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions. EMBO J. 20:466-479. doi:10.1093/emboj/20.3.466
42. Umar, A., A.B. Buermeyer, J.A. Simon, D.C. Thomas, A.B. Clark, R.M. Liskay, and T.A. Kunkel. 1996. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell. 87:65-73. doi:10.1016/S0092-8674(00)81323- 9
43. Unk, I., L. Haracska, X.V. Gomes, P.M. Burgers, L. Prakash, and S. Prakash. 2002. Stimulation of 3′→5′ exonuclease and 3′-phosphodiesterase activities of yeast apn2 by proliferating cell nuclear antigen. Mol. Cell. Biol. 22:6480-6486. doi:10.1128/MCB.22.18.6480-6486. 2002
44. Vassilev, L.T., B.T. Vu, B. Graves, D. Carvajal, F. Podlaski, Z. Filipovic, N. Kong, U. Kammlott, C. Lukacs, C. Klein, et al. 2004. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science. 303:844-848. doi:10.1126/science.1092472
45. Waga, S., and B. Stillman. 1998. The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem. 67:721-751. doi:10.1146/annurev.biochem.67.1.721 (Pubitemid 28411143)
46. Wang, S.C., Y. Nakajima, Y.L. Yu, W. Xia, C.T. Chen, C.C. Yang, E.W. McIntush, L.Y. Li, D.H. Hawke, R. Kobayashi, and M.C. Hung. 2006. Tyrosine phosphorylation controls PCNA function through protein stability. Nat. Cell Biol. 8:1359-1368. doi:10.1038/ncb1501
47. Warbrick, E. 1998. PCNA binding through a conserved motif. Bioessays. 20:195-199. doi:10.1002/(SICI)1521-1878(199803)20:3〈195::AIDBIES2〉 3.0.CO;2-R (Pubitemid 28174030)
48. Xia, L., L. Zheng, H.W. Lee, S.E. Bates, L. Federico, B. Shen, and T.R. O'Connor. 2005. Human 3-methyladenine-DNA glycosylase: effect of sequence context on excision, association with PCNA, and stimulation by AP endonuclease. J. Mol. Biol. 346:1259-1274. doi:10.1016/j.jmb.2005.01.014 (Pubitemid 40248827)
49. Yu, Y., J.P. Cai, B. Tu, L. Wu, Y. Zhao, X. Liu, L. Li, M.A. McNutt, J. Feng, Q. He, et al. 2009. Proliferating cell nuclear antigen is protected from degradation by forming a complex with MutT Homolog2. J. Biol. Chem. 284:19310-19320. doi:10.1074/jbc.M109.015289
50. Zhang, J., B. Zhou, C.F. Zheng, and Z.Y. Zhang. 2003. A bipartite mechanism for ERK2 recognition by its cognate regulators and substrates. J. Biol. Chem. 278:29901-29912. doi:10.1074/jbc.M303909200 (Pubitemid 36962378)
51. Zufferey, R., D. Nagy, R.J. Mandel, L. Naldini, and D. Trono. 1997. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15:871-875. doi:10.1038/nbt0997-871 (Pubitemid 27391780) (Pubitemid 127747819)