The Rad9A checkpoint protein is required for nuclear localization of the claspin adaptor protein

Cell Cycle

Volumn 9, Issue 3, 2010, Pages 548-556

  Sierant, Megan L ^a,b   Archer, Nicole E ^a   Davey, Scott K ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

911 complex; Cell cycle checkpoint control; Claspin; DNA repair; Nuclear localization; Rad9A

Indexed keywords

ADAPTOR PROTEIN; CHECKPOINT KINASE 1; CLASPIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN RAD9; PROTEIN RAD9A; PROTEIN RAD9B; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CLASPIN PROTEIN, MOUSE; CLSPN PROTEIN, HUMAN; MESSENGER RNA; RETINOIC ACID; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CYCLE; CELL LINE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NULL CELL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; WILD TYPE; ANIMAL; CELL FRACTIONATION; CELL NUCLEUS; CHEMISTRY; CYTOLOGY; DRUG EFFECT; EMBRYONIC STEM CELL; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HELA CELL; METABOLISM; MOUSE; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL NUCLEUS; DNA DAMAGE; EMBRYONIC STEM CELLS; GENE DELETION; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICE; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, MESSENGER; SUBCELLULAR FRACTIONS; TRETINOIN;

EID: 77951894248     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.3.10553     Document Type: Article

References (44)

1. Kim SM, Kumagai A, Lee J, Dunphy WG. Phosphorylation of Chk1 by ATM- and Rad3-related (ATR) in Xenopus egg extracts requires binding of ATRIP to ATR but not the stable DNA-binding or coiled-coil domains of ATRIP. J Biol Chem 2005; 280:38355-64.
2. Kumagai A, Kim SM, Dunphy WG. Claspin and the activated form of ATR-ATRIP collaborate in the activation of Chk1. J Biol Chem 2004; 279:49599-608.
3. Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 2001; 21:4129-39.
4. Chini CC, Chen J. Human claspin is required for replication checkpoint control. J Biol Chem 2003; 278:30057-62.
5. Chini CC, Chen J. Claspin, a regulator of Chk1 in DNA replication stress pathway. DNA Repair (Amst) 2004; 3:1033-7.
6. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev 2007; 21:1472-7.
7. Bao S, Lu T, Wang X, Zheng H, Wang LE, Wei Q, et al. Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects. Oncogene 2004; 23:5586-93. (Pubitemid 39093036)
8. Dang T, Bao S, Wang XF. Human Rad9 is required for the activation of S-phase checkpoint and the maintenance of chromosomal stability. Genes Cells 2005; 10:287-95. (Pubitemid 40443681)
9. Roos-Mattjus P, Hopkins KM, Oestreich AJ, Vroman BT, Johnson KL, Naylor S, et al. Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J Biol Chem 2003; 278:24428-37.
10. Xu X, Vaithiyalingam S, Glick GG, Mordes DA, Chazin WJ, Cortez D. The basic cleft of RPA70N binds multiple checkpoint proteins including RAD9 to regulate ATR signaling. Mol Cell Biol 2008.
11. Wang X, Zou L, Lu T, Bao S, Hurov KE, Hittelman WN, et al. Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol Cell 2006; 23:331-41.
12. Greer DA, Besley BD, Kennedy KB, Davey S. hRad9 rapidly binds DNA containing double-strand breaks and is required for damage-dependent topoisomerase II beta binding protein 1 focus formation. Cancer Res 2003; 63:4829-35.
13. Lee J, Kumagai A, Dunphy WG. The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. J Biol Chem 2007; 282:28036-44.
14. Medhurst AL, Warmerdam DO, Akerman I, Verwayen EH, Kanaar R, Smits VA, et al. ATR and Rad17 collaborate in modulating Rad9 localisation at sites of DNA damage. J Cell Sci 2008; 121:3933-40.
15. Navadgi-Patil VM, Burgers PM. A tale of two tails: Activation of DNA damage checkpoint kinase Mec1/ ATR by the 9-1-1 clamp and by Dpb11/TopBP1. DNA Repair (Amst) 2009.
16. Liu S, Bekker-Jensen S, Mailand N, Lukas C, Bartek J, Lukas J. Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol Cell Biol 2006; 26:6056-64.
17. Bermudez VP, Lindsey-Boltz LA, Cesare AJ, Maniwa Y, Griffith JD, Hurwitz J, et al. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc Natl Acad Sci USA 2003; 100:1633-8.
18. Caspari T, Dahlen M, Kanter-Smoler G, Lindsay HD, Hofmann K, Papadimitriou K, et al. Characterization of Schizosaccharomyces pombe Hus1: a PCNA-related protein that associates with Rad1 and Rad9. Mol Cell Biol 2000; 20:1254-62.
19. Kostrub CF, Knudsen K, Subramani S, Enoch T. Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage. EMBO J 1998; 17:2055-66. (Pubitemid 28154534)
20. St. Onge RP, Udell CM, Casselman R, Davey S. The human G2 checkpoint control protein hRAD9 is a nuclear phosphoprotein that forms complexes with hRAD1 and hHUS1. Mol Biol Cell 1999; 10:1985-95. (Pubitemid 29272645)
21. Volkmer E, Karnitz LM. Human homologs of Schizosaccharomyces pombe rad1, hus1 and rad9 form a DNA damage-responsive protein complex. J Biol Chem 1999; 274:567-70.
22. Dore AS, Kilkenny ML, Rzechorzek NJ, Pearl LH. Crystal structure of the Rad9-Rad1-Hus1 DNA damage checkpoint complex-implications for clamp loading and regulation. Mol Cell 2009; 34:735-45.
23. Hirai I, Wang HG. A role of the C-terminal region of human Rad9 (hRad9) in nuclear transport of the hRad9 checkpoint complex. J Biol Chem 2002; 277:25722-7.
24. Komatsu K, Hopkins KM, Lieberman HB, Wang H. Schizosaccharomyces pombe Rad9 contains a BH3-like region and interacts with the anti-apoptotic protein Bcl-2. FEBS Lett 2000; 481:122-6.
25. St Onge RP, Besley BD, Pelley JL, Davey S. A role for the phosphorylation of hRad9 in checkpoint signaling. J Biol Chem 2003; 278:26620-8.
26. St. Onge RP, Besley BD, Park M, Casselman R, Davey S. DNA damage-dependent and -independent phosphorylation of the hRad9 checkpoint protein. J Biol Chem 2001; 276:41898-905.
27. Kumagai A, Dunphy WG. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol Cell 2000; 6:839-49.
28. Osborn AJ, Elledge SJ. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev 2003; 17:1755-67.
29. Scorah J, McGowan CH. Claspin and Chk1 regulate replication fork stability by different mechanisms. Cell Cycle 2009; 8:1036-43.
30. Dufault VM, Oestreich AJ, Vroman BT, Karnitz LM. Identification and characterization of RAD9B, a paralog of the RAD9 checkpoint gene. Genomics 2003; 82:644-51.
31. Hopkins KM, Wang X, Berlin A, Hang H, Thaker HM, Lieberman HB. Expression of mammalian paralogues of HRAD9 and Mrad9 checkpoint control genes in normal and cancerous testicular tissue. Cancer Res 2003; 63:5291-8.
32. Sorensen CS, Syljuasen RG, Lukas J, Bartek J. ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 2004; 3:941-5.
33. Sar F, Lindsey-Boltz LA, Subramanian D, Croteau DL, Hutsell SQ, Griffith JD, et al. Human claspin is a ring-shaped DNA-binding protein with high affinity to branched DNA structures. J Biol Chem 2004; 279:39289-95.
34. Venclovas C, Thelen MP. Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res 2000; 28:2481-93.
35. Kaur R, Kostrub CF, Enoch T. Structure-function analysis of fission yeast Hus1-Rad1-Rad9 checkpoint complex. Mol Biol Cell 2001; 12:3744-58.
36. Sohn SY, Cho Y. Crystal structure of the human Rad9-Hus1-Rad1 clamp. J Mol Biol 2009; 390:490-502.
37. Hopkins KM, Auerbach W, Wang XY, Hande MP, Hang H, Wolgemuth DJ, et al. Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol Cell Biol 2004; 24:7235-48.
38. Yoshizawa-Sugata N, Masai H. Human Tim/Timeless-interacting protein, Tipin, is required for efficient progression of S phase and DNA replication checkpoint. J Biol Chem 2007; 282:2729-40.
39. Unsal-Kacmaz K, Mullen TE, Kaufmann WK, Sancar A. Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol 2005; 25:3109-16.
40. Maniwa Y, Yoshimura M, Bermudez VP, Okada K, Kanomata N, Ohbayashi C, et al. His239Arg SNP of HRAD9 is associated with lung adenocarcinoma. Cancer 2006; 106:1117-22.
41. Maniwa Y, Yoshimura M, Bermudez VP, Yuki T, Okada K, Kanomata N, et al. Accumulation of hRad9 protein in the nuclei of nonsmall cell lung carcinoma cells. Cancer 2005; 103:126-32.
42. Rosa-Rosa JM, Pita G, Gonzalez-Neira A, Milne RL, Fernandez V, Ruivenkamp C, et al. A 7 Mb region within 11q13 may contain a high penetrance gene for breast cancer. Breast Cancer Res Treat 2009.
43. Cheng CK, Chow LW, Loo WT, Chan TK, Chan V. The cell cycle checkpoint gene Rad9 is a novel oncogene activated by 11q13 amplification and DNA methylation in breast cancer. Cancer Res 2005; 65:8646-54.
44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8.