DNA-PK-dependent RPA2 hyperphosphorylation facilitates DNA repair and suppresses sister chromatid exchange

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Liaw, Hungjiun ^a   Lee, Deokjae ^a   Myung, Kyungjae ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; DNA DEPENDENT PROTEIN KINASE; RAD51 PROTEIN; REPLICATION FACTOR A; 4 NITROQUINOLINE 1 OXIDE; CYCLIN DEPENDENT KINASE; H2AFX PROTEIN, HUMAN; HISTONE; MUTANT PROTEIN; RPA2 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MITOSIS; PROTEIN PHOSPHORYLATION; SISTER CHROMATID EXCHANGE; CELL LINE; CELL STRAIN HEK293; DNA REPLICATION; DRUG EFFECT; METABOLISM; PHOSPHORYLATION; RADIATION EXPOSURE; ULTRAVIOLET RADIATION;

4-NITROQUINOLINE-1-OXIDE; CELL LINE; CYCLIN-DEPENDENT KINASES; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; DNA-ACTIVATED PROTEIN KINASE; HEK293 CELLS; HISTONES; HUMANS; MITOSIS; MUTANT PROTEINS; PHOSPHORYLATION; RAD51 RECOMBINASE; REPLICATION PROTEIN A; SISTER CHROMATID EXCHANGE; ULTRAVIOLET RAYS;

EID: 79959488298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021424     Document Type: Article

References (36)

1. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S, (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85.
2. Sogo JM, Lopes M, Foiani M, (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
3. Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, et al. (2005) Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 25: 3553-3562.
4. Brown EJ, Baltimore D, (2003) Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev 17: 615-628.
5. Branzei D, Foiani M, (2009) The checkpoint response to replication stress. DNA Repair (Amst) 8: 1038-1046.
6. Branzei D, Foiani M, (2010) Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 11: 208-219.
7. Din S, Brill SJ, Fairman MP, Stillman B, (1990) Cell-cycle-regulated phosphorylation of DNA replication factor A from human and yeast cells. Genes Dev 4: 968-977.
8. Zernik-Kobak M, Vasunia K, Connelly M, Anderson CW, Dixon K, (1997) Sites of UV-induced phosphorylation of the p34 subunit of replication protein A from HeLa cells. J Biol Chem 272: 23896-23904.
9. Carty MP, Zernik-Kobak M, McGrath S, Dixon K, (1994) UV light-induced DNA synthesis arrest in HeLa cells is associated with changes in phosphorylation of human single-stranded DNA-binding protein. EMBO J 13: 2114-2123.
10. Olson E, Nievera CJ, Klimovich V, Fanning E, Wu X, (2006) RPA2 is a direct downstream target for ATR to regulate the S-phase checkpoint. J Biol Chem 281: 39517-39533.
11. Manthey KC, Opiyo S, Glanzer JG, Dimitrova D, Elliott J, et al. (2007) NBS1 mediates ATR-dependent RPA hyperphosphorylation following replication-fork stall and collapse. J Cell Sci 120: 4221-4229.
12. Shao RG, Cao CX, Zhang H, Kohn KW, Wold MS, et al. (1999) Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA:DNA-PK complexes. EMBO J 18: 1397-1406.
13. Pan ZQ, Amin AA, Gibbs E, Niu H, Hurwitz J, (1994) Phosphorylation of the p34 subunit of human single-stranded-DNA-binding protein in cyclin A-activated G1 extracts is catalyzed by cdk-cyclin A complex and DNA-dependent protein kinase. Proc Natl Acad Sci U S A 91: 8343-8347.
14. Brush GS, Anderson CW, Kelly TJ, (1994) The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication. Proc Natl Acad Sci U S A 91: 12520-12524.
15. Gately DP, Hittle JC, Chan GK, Yen TJ, (1998) Characterization of ATM expression, localization, and associated DNA-dependent protein kinase activity. Mol Biol Cell 9: 2361-2374.
16. Morgan SE, Kastan MB, (1997) Dissociation of radiation-induced phosphorylation of replication protein A from the S-phase checkpoint. Cancer Res 57: 3386-3389.
17. Boubnov NV, Weaver DT, (1995) scid cells are deficient in Ku and replication protein A phosphorylation by the DNA-dependent protein kinase. Mol Cell Biol 15: 5700-5706.
18. Anantha RW, Sokolova E, Borowiec JA, (2008) RPA phosphorylation facilitates mitotic exit in response to mitotic DNA damage. Proc Natl Acad Sci U S A 105: 12903-12908.
19. Anantha RW, Vassin VM, Borowiec JA, (2007) Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J Biol Chem 282: 35910-35923.
20. Motegi A, Liaw HJ, Lee KY, Roest HP, Maas A, et al. (2008) Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc Natl Acad Sci U S A 105: 12411-12416.
21. Solomon DA, Cardoso MC, Knudsen ES, (2004) Dynamic targeting of the replication machinery to sites of DNA damage. J Cell Biol 166: 455-463.
22. Stephan H, Concannon C, Kremmer E, Carty MP, Nasheuer HP, (2009) Ionizing radiation-dependent and independent phosphorylation of the 32-kDa subunit of replication protein A during mitosis. Nucleic Acids Res 37: 6028-6041.
23. Niu H, Erdjument-Bromage H, Pan ZQ, Lee SH, Tempst P, et al. (1997) Mapping of amino acid residues in the p34 subunit of human single-stranded DNA-binding protein phosphorylated by DNA-dependent protein kinase and Cdc2 kinase in vitro. J Biol Chem 272: 12634-12641.
24. Oakley GG, Patrick SM, Yao J, Carty MP, Turchi JJ, et al. (2003) RPA phosphorylation in mitosis alters DNA binding and protein-protein interactions. Biochemistry 42: 3255-3264.
25. Cheng X, Cheong N, Wang Y, Iliakis G, (1996) Ionizing radiation-induced phosphorylation of RPA p34 is deficient in ataxia telangiectasia and reduced in aged normal fibroblasts. Radiother Oncol 39: 43-52.
26. Ruis BL, Fattah KR, Hendrickson EA, (2008) The catalytic subunit of DNA-dependent protein kinase regulates proliferation, telomere length, and genomic stability in human somatic cells. Mol Cell Biol 28: 6182-6195.
27. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, et al. (2002) DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 4: 993-997.
28. Kannouche P, Broughton BC, Volker M, Hanaoka F, Mullenders LH, et al. (2001) Domain structure, localization, and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev 15: 158-172.
29. San Filippo J, Sung P, Klein H, (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77: 229-257.
30. Block WD, Yu Y, Lees-Miller SP, (2004) Phosphatidyl inositol 3-kinase-like serine/threonine protein kinases (PIKKs) are required for DNA damage-induced phosphorylation of the 32 kDa subunit of replication protein A at threonine 21. Nucleic Acids Res 32: 997-1005.
31. Liu VF, Weaver DT, (1993) The ionizing radiation-induced replication protein A phosphorylation response differs between ataxia telangiectasia and normal human cells. Mol Cell Biol 13: 7222-7231.
32. Wang H, Guan J, Perrault AR, Wang Y, Iliakis G, (2001) Replication protein A2 phosphorylation after DNA damage by the coordinated action of ataxia telangiectasia-mutated and DNA-dependent protein kinase. Cancer Res 61: 8554-8563.
33. Lee KY, Myung K, (2008) PCNA modifications for regulation of post-replication repair pathways. Mol Cells 26: 5-11.
34. Cruet-Hennequart S, Glynn MT, Murillo LS, Coyne S, Carty MP, (2008) Enhanced DNA-PK-mediated RPA2 hyperphosphorylation in DNA polymerase eta-deficient human cells treated with cisplatin and oxaliplatin. DNA Repair (Amst) 7: 582-596.
35. Lee DH, Pan Y, Kanner S, Sung P, Borowiec JA, et al. (2010) A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination. Nat Struct Mol Biol 17: 365-372.
36. Nakanishi K, Yang YG, Pierce AJ, Taniguchi T, Digweed M, et al. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc Natl Acad Sci U S A 102: 1110-1115.