HARPing on about the DNA damage response during replication

Genes and Development

Volumn 23, Issue 20, 2009, Pages 2359-2365

  Driscoll, Robert ^a   Cimprich, Karlene A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Annealing helicase; DNA damage response; DNA replication; HARP; RPA; SMARCAL1

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; DNA; DNA BINDING PROTEIN; HELICASE; HEPA RELATED PROTEIN; PROTEIN; REPLICATION FACTOR A; UNCLASSIFIED DRUG;

CELL CYCLE S PHASE; CHROMATIN; DNA DAMAGE; DNA REPLICATION; DNA RESPONSIVE ELEMENT; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STABILITY; REVIEW; STRESS;

DNA DAMAGE; DNA HELICASES; DNA REPLICATION; S PHASE;

EID: 70350124025     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1860609     Document Type: Review

References (63)

1. Admire A, Shanks L, Danzl N, Wang M, Weier U, Stevens W, Hunt E, Weinert T. 2006. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes & Dev 20: 159-173. (Pubitemid 43112935)
2. Atkinson J, McGlynn P. 2009. Replication fork reversal and the maintenance of genome stability. Nucleic Acids Res 37: 3475-3492.
3. Bansbach CE, Bétous R, Lovejoy CA, Glick GG, Cortez D. 2009. The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes & Dev (this issue). doi: 10.1101/gad.1839909.
4. Barbour L, Xiao W. 2003. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: A yeast model. Mutat Res 532: 137-155. (Pubitemid 37487851)
5. Blastyak A, Pinter L, Unk I, Prakash L, Prakash S, Haracska L. 2007. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol Cell 28: 167-175. (Pubitemid 47542303)
6. Blow JJ, Dutta A. 2005. Preventing re-replication of chromosomal DNA. Nat Rev Mol Cell Biol 6: 476-486.
7. Boerkoel CF, O'Neill S, Andre JL, Benke PJ, Bogdanovic R, Bulla M, Burguet A, Cockfield S, Cordeiro I, Ehrich JH, et al. 2000. Manifestations and treatment of Schimke immuno-osseous dysplasia: 14 new cases and a review of the literature. Eur J Pediatr 159: 1-7. (Pubitemid 30120118)
8. Branzei D, Foiani M. 2005. The DNA damage response during DNA replication. Curr Opin Cell Biol 17: 568-575.
9. Branzei D, Foiani M. 2007. Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 6: 994-1003. (Pubitemid 46880479)
10. Branzei D, Foiani M. 2009. The checkpoint response to replication stress. DNA Repair (Amst) 8: 1038-1046.
11. Chang DJ, Cimprich KA. 2009. DNA damage tolerance: When it's OK to make mistakes. Nat Chem Biol 5: 82-90.
12. Ciccia A, McDonald N, West SC. 2008. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77: 259-287.
13. Ciccia A, Bredemeyer AL, Sowa ME, Terret M-E, Jallepalli PV, Harper JW, Elledge SJ. 2009. The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes & Dev (this issue). doi: 10.1101/gad.1832309.
14. Cimprich KA, Cortez D. 2008. ATR: An essential regulator of genome integrity. Nat Rev Mol Cell Biol 9: 616-627. (Pubitemid 352032926)
15. Cobb JA, Bjergbaek L, Shimada K, Frei C, Gasser SM. 2003. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J 22: 4325-4336. (Pubitemid 37021759)
16. Cortez D, Glick G, Elledge SJ. 2004. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci 101: 10078-10083. (Pubitemid 38891197)
17. Deguchi K, Clewing JM, Elizondo LI, Hirano R, Huang C, Choi K, Sloan EA, Lucke T, Marwedel KM, Powell RD Jr, et al. 2008. Neurologic phenotype of Schimke immuno-osseous dysplasia and neurodevelopmental expression of SMARCAL1. J Neuropathol Exp Neurol 67: 565-577. (Pubitemid 351787083)
18. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM. 2007. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes & Dev 21: 1472-1477. (Pubitemid 46955719)
19. Driscoll R, Hudson A, Jackson SP. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649-652. (Pubitemid 46214709)
20. Durr H, Flaus A, Owen-Hughes T, Hopfner KP. 2006. Snf2 family ATPases and DExx box helicases: Differences and unifying concepts from high-resolution crystal structures. Nucleic Acids Res 34: 4160-4167. (Pubitemid 44542195)
21. Ellison V, Stillman B. 2003. Biochemical characterization of DNA damage checkpoint complexes: Clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol 1: E33. doi: 10.1371/journal.pbio.0000033.
22. Flaus A, Martin DM, Barton GJ, Owen-Hughes T. 2006. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34: 2887-2905. (Pubitemid 44540417)
23. Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, Almouzni G. 2007. Regulation of replication fork progression through histone supply and demand. Science 318: 1928-1931.
24. Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z. 2007a. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315: 653-655. (Pubitemid 46214710)
25. Han J, Zhou H, Li Z, Xu RM, Zhang Z. 2007b. Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Biol Chem 282: 28587-28596. (Pubitemid 47606001)
26. Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, Maas A, Essers J, Hickson ID, Kanaar R. 2007. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 14: 1096-1104. (Pubitemid 350060335)
27. Heller RC, Marians KJ. 2006. Replisome assembly and the direct restart of stalled replication forks. Nat Rev Mol Cell Biol 7: 932-943.
28. Hickson ID. 2003. RecQ helicases: Caretakers of the genome. Nat Rev Cancer 3: 169-178.
29. Hockensmith JW, Wahl AF, Kowalski S, Bambara RA. 1986. Purification of a calf thymus DNA-dependent adenosinetriphosphatase that prefers a primer-template junction effector. Biochemistry 25: 7812-7821. (Pubitemid 17228254)
30. Kastan MB, Bartek J. 2004. Cell-cycle checkpoints and cancer. Nature 432: 316-323.
31. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, Sugimoto K, Shirahige K. 2003. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083. (Pubitemid 37064311)
32. Kolodner RD, Putnam CD, Myung K. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297: 552-557. (Pubitemid 34815331)
33. Kumagai A, Lee J, Yoo HY, Dunphy WG. 2006. TopBP1 activates the ATR-ATRIP complex. Cell 124: 943-955.
34. Lambert S, Carr AM. 2005. Checkpoint responses to replication fork barriers. Biochimie 87: 591-602. (Pubitemid 40884622)
35. Majka J, Burgers PM. 2004. The PCNA-RFC families of DNA clamps and clamp loaders. Prog Nucleic Acid Res Mol Biol 78: 227-260.
36. Majka J, Binz SK, Wold MS, Burgers PM. 2006. Replication protein A directs loading of the DNA damage checkpoint clamp to 5′-DNA junctions. J Biol Chem 281: 27855-27861. (Pubitemid 44414497)
37. Masumoto H, Hawke D, Kobayashi R, Verreault A. 2005. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294-298. (Pubitemid 41021284)
38. McGlynn P, Lloyd RG. 2002. Replicating past lesions in DNA. Mol Cell 10: 700-701.
39. Mer G, Bochkarev A, Gupta R, Bochkareva E, Frappier L, Ingles CJ, Edwards AM, Chazin WJ. 2000. Structural basis for the recognition of DNA repair proteins UNG2, XPA, and RAD52 by replication factor RPA. Cell 103: 449-456.
40. Mordes DA, Glick GG, Zhao R, Cortez D. 2008. TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes & Dev 22: 1478-1489. (Pubitemid 351793082)
41. Muthuswami R, Truman PA, Mesner LD, Hockensmith JW. 2000. A eukaryotic SWI2/SNF2 domain, an exquisite detector of double-stranded to single-stranded DNA transition elements. J Biol Chem 275: 7648-7655. (Pubitemid 30159666)
42. O'Driscoll M, Jeggo PA. 2008. The role of the DNA damage response pathways in brain development and microcephaly: Insight from human disorders. DNA Repair (Amst) 7: 1039-1050.
43. 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. (Pubitemid 46041912)
44. Papamichos-Chronakis M, Peterson CL. 2008. The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat Struct Mol Biol 15: 338-345.
45. Paques F, Haber JE. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404. (Pubitemid 29264976)
46. Pacek M, Walter JC. 2004. A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J 23: 3667-3676. (Pubitemid 39336288)
47. Paulsen RD, Cimprich KA. 2007. The ATR pathway: Fine-tuning the fork. DNA Repair (Amst) 6: 953-966.
48. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. 2007. Human CtIP promotes DNA end resection. Nature 450: 509-514. (Pubitemid 350190253)
49. Shimada K, Oma Y, Schleker T, Kugou K, Ohta K, Harata M, Gasser SM. 2008. Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr Biol 18: 566-575.
50. Smirnova M, Klein HL. 2003. Role of the error-free damage bypass postreplication repair pathway in the maintenance of genomic stability. Mutat Res 532: 117-135.
51. Smith KD, Fu MA, Brown E. 2009. Tim/Tipin dysfunction creates an indispensible reliance on the ATR-Chk1 pathway for continued DNA synthesis. J Cell Biol (in press).
52. Sogo JM, Lopes M, Foiani M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602. (Pubitemid 34815343)
53. Spranger J, Hinkel GK, Stoss H, Thoenes W, Wargowski D, Zepp F. 1991. Schimke immuno-osseous dysplasia: A newly recognized multisystem disease. J Pediatr 119: 64-72.
54. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123: 1213-1226. (Pubitemid 41821780)
55. Tittel-Elmer M, Alabert C, Pasero P, Cobb JA. 2009. The MRX complex stabilizes the replisome independently of the S phase checkpoint during replication stress. EMBO J 28: 1142-1156.
56. Tourriere H, Pasero P. 2007. Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst) 6: 900-913. (Pubitemid 46880471)
57. Unsal-Kacmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK. 2007. The human Tim/Tipin complex coordinates an intra-S checkpoint response to UV that slows replication fork displacement. Mol Cell Biol 27: 3131-3142. (Pubitemid 46581324)
58. Yuan J, Ghosal G, Chen J. 2009. The annealing helicase HARP protects stalled replication forks. Genes & Dev (this issue). doi: 10.1101/gad.1836409.
59. Yusufzai T, Kadonaga JT. 2008. HARP is an ATP-driven annealing helicase. Science 322: 748-750.
60. Yusufzai T, Kong X, Yokomori K, Kadonaga JT. 2009. The annealing helicase HARP is recruited to DNA repair sites via an interaction with RPA. Genes & Dev (this issue). doi: 10.1101/gad.1831509.
61. Zou L. 2007. Single- and double-stranded DNA: Building a trigger of ATR-mediated DNA damage response. Genes & Dev 21: 879-885.
62. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548. (Pubitemid 36682880)
63. Zou Y, Liu Y, Wu X, Shell SM. 2006. Functions of human replication protein A (RPA): From DNA replication to DNA damage and stress responses. J Cell Physiol 208: 267-273. (Pubitemid 43993416)