The RecQ4 orthologue Hrq1 is critical for DNA interstrand cross-link repair and genome stability in fission yeast

Molecular and Cellular Biology

Volumn 32, Issue 2, 2012, Pages 276-287

  Groocock, Lynda M ^a   Prudden, John ^a   Perry, J Jefferson P ^a,b   Boddy, Michael N ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b AMRITA UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

HRQ1 PROTEIN; MMS2 PROTEIN; NUCLEIC ACID BINDING PROTEIN; PCNA PROTEIN; RECQ HELICASE; RECQ4 PROTEIN; UBIQUITIN CONJUGATING ENZYME 13; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXCISION REPAIR; GENETIC EPISTASIS; GENOMIC INSTABILITY; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RECOMBINATION REPAIR; ULTRAVIOLET RADIATION; YEAST;

AMINO ACID MOTIFS; CISPLATIN; CROSS-LINKING REAGENTS; DNA HELICASES; DNA REPAIR; DNA, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENOMIC INSTABILITY; MUTATION; RECQ HELICASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84856794104     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06184-11     Document Type: Article

References (65)

1. Ahn JS, Osman F, Whitby MC. 2005. Replication fork blockage by RTS1 at an ectopic site promotes recombination in fission yeast. EMBO J. 24: 2011-2023.
2. Ashton TM, Hickson ID. 2010. Yeast as a model system to study RecQ helicase function. DNA Repair (Amst.) 9:303-314.
3. Ashton TM, Mankouri HW, Heidenblut A, McHugh PJ, Hickson ID. 2011. Pathways for Holliday junction processing during homologous recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 31:1921-1933.
4. Barea F, Tessaro S, Bonatto D. 2008. In silico analyses of a new group of fungal and plant RecQ4-homologous proteins. Comput. Biol. Chem. 32: 349-358.
5. Berg E, Chuang TY, Cripps D. 1987. Rothmund-Thomson syndrome. A case report, phototesting, and literature review. J. Am. Acad. Dermatol. 17:332-338.
6. Bernstein KA, Gangloff S, Rothstein R. 2010. The RecQ DNA helicases in DNA repair. Annu. Rev. Genet. 44:393- 417.
7. Boddy MN, et al. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537-548.
8. Boddy MN, et al. 2000. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20: 8758-8766.
9. Boddy MN, et al. 2003. Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60. Mol. Cell. Biol. 23:5939 -5946.
10. Branzei D, Foiani M. 2010. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11:208 -219.
11. Chu WK, Hickson ID. 2009. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer 9:644-654.
12. Coulon S, et al. 2010. Rad8Rad5/Mms2-Ubc13 ubiquitin ligase complex controls translesion synthesis in fission yeast. EMBO J. 29:2048 -2058.
13. Doe CL, Ahn JS, Dixon J, Whitby MC. 2002. Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 277:32753-32759.
14. Durand F, et al. 2002. Rothmund-Thomson syndrome, trisomy 8 mosaicism and RECQ4 gene mutation. Ann. Dermatol. Venereol. 129: 892-895.
15. Fan W, Luo J. 2008. RecQ4 facilitates UV light-induced DNA damage repair through interaction with nucleotide excision repair factor xeroderma pigmentosum group A (XPA). J. Biol. Chem. 283:29037-29044.
16. Frampton J, et al. 2006. Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol. Biol. Cell 17:2976 -2985.
17. Gray MD, et al. 1997. The Werner syndrome protein is a DNA helicase. Nat. Genet. 17:100 -103.
18. Heyer WD, Ehmsen KT, Liu J. 2010. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44:113-139.
19. Hinz JM. 2010. Role of homologous recombination in DNA interstrand crosslink repair. Environ. Mol. Mutagen. 51:582- 603.
20. Jin W, et al. 2008. Sensitivity of RECQL4-deficient fibroblasts from Rothmund-Thomson syndrome patients to genotoxic agents. Hum. Genet. 123:643- 653.
21. Kai M, Wang TS. 2003. Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 17:64 -76.
22. Karow JK, Chakraverty RK, Hickson ID. 1997. The Bloom's syndrome gene product is a 3=-5= DNA helicase. J. Biol. Chem. 272:30611-30614.
23. Kartalou M, Essigmann JM. 2001. Recognition of cisplatin adducts by cellular proteins. Mutat. Res. 478:1-21.
24. Kitao S, et al. 1998. Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54:443- 452.
25. Kitao S, et al. 1999. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22:82- 84.
26. Knipscheer P, et al. 2009. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326: 1698-1701.
27. Lambert S, et al. 2003. Schizosaccharomyces pombe checkpoint response to DNA interstrand cross-links. Mol. Cell. Biol. 23:4728-4737.
28. Larizza L, Magnani I, Roversi G. 2006. Rothmund-Thomson syndrome and RECQL4 defect: splitting and lumping. Cancer Lett. 232:107-120.
29. Lee C, et al. 2004. Structural basis for inhibition of the replication licensing factor Cdt1 by geminin. Nature 430:913-917.
30. Lee KY, Myung K. 2008. PCNA modifications for regulation of postreplication repair pathways. Mol. Cells 26:5-11.
31. Lehoczky P, McHugh PJ, Chovanec M. 2007. DNA interstrand cross-link repair in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 31:109 -133.
32. Locovei AM, Yin L, D'Urso G. 2010. A genetic screen for replication initiation defective (rid) mutants in Schizosaccharomyces pombe. Cell Div. 5:20.
33. Long DT, Raschle M, Joukov V, Walter JC. 2011. Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333:84-87.
34. Mandell JG, Goodrich KJ, Bahler J, Cech TR. 2005. Expression of a RecQ helicase homolog affects progression through crisis in fission yeast lacking telomerase. J. Biol. Chem. 280:5249 -5257.
35. Mann MB, et al. 2005. Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome. Hum. Mol. Genet. 14:813- 825.
36. Matsuno K, Kumano M, Kubota Y, Hashimoto Y, Takisawa H. 2006. The N-terminal noncatalytic region of Xenopus RecQ4 is required for chromatin binding of DNA polymerase alpha in the initiation of DNA replication. Mol. Cell. Biol. 26:4843- 4852.
37. Mimitou EP, Symington LS. 2011. DNA end resection- unraveling the tail. DNA Repair (Amst.) 10:344 -348.
38. Miozzo M, et al. 1998. Chromosomal instability in fibroblasts and mesenchymal tumors from 2 sibs with Rothmund-Thomson syndrome. Int. J. Cancer 77:504 -510.
39. Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795- 823.
40. Nishitani H, Lygerou Z, Nishimoto T, Nurse P. 2000. The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 404: 625-628.
41. Noguchi C, Garabedian MV, Malik M, Noguchi E. 2008. A vector system for genomic FLAG epitope-tagging in Schizosaccharomyces pombe. Biotechnol. J. 3:1280 -1285.
42. Osman F, Adriance M, McCready S. 2000. The genetic control of spon-taneous and UV-induced mitotic intrachromosomal recombination in the fission yeast Schizosaccharomyces pombe. Curr. Genet. 38:113-125.
43. Pebernard S, Wohlschlegel J, McDonald WH, Yates JR, III, Boddy MN. 2006. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol. Cell. Biol. 26:1617-1630.
44. Petkovic M, Dietschy T, Freire R, Jiao R, Stagljar I. 2005. The human Rothmund-Thomson syndrome gene product, RECQL4, localizes to distinct nuclear foci that coincide with proteins involved in the maintenance of genome stability. J. Cell Sci. 118:4261- 4269.
45. Prudden J, et al. 2007. SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 26:4089-4101.
46. Prudden J, Perry JJ, Arvai AS, Tainer JA, Boddy MN. 2009. Molecular mimicry of SUMO promotes DNA repair. Nat. Struct. Mol. Biol. 16: 509-516.
47. Raffa GD, Wohlschlegel J, Yates JR, III, Boddy MN. 2006. SUMObinding motifs mediate the Rad60-dependent response to replicative stress and self-association. J. Biol. Chem. 281:27973-27981.
48. Rhind N, Russell P. 2000. Chk1 and Cds1: linchpins of the DNA damage and replication checkpoint pathways. J. Cell Sci. 113(Pt 22):3889 -3896.
49. Rhind N, Russell P. 1998. Mitotic DNA damage and replication checkpoints in yeast. Curr. Opin. Cell Biol. 10:749 -758.
50. Roguev A, et al. 2008. Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science 322:405- 410.
51. Roseaulin L, et al. 2008. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J. 27:1378 -1387.
52. Rossi ML, Ghosh AK, Kulikowicz T, Croteau DL, Bohr VA. 2010. Conserved helicase domain of human RecQ4 is required for strand annealingindependent DNA unwinding. DNA Repair (Amst.) 9:796-804.
53. Sangrithi MN, et al. 2005. Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 121: 887-898.
54. Schleker T, Nagai S, Gasser SM. 2009. Posttranslational modifications of repair factors and histones in the cellular response to stalled replication forks. DNA Repair (Amst.) 8:1089 -1100.
55. Schurman SH, et al. 2009. Direct and indirect roles of RECQL4 in modulating base excision repair capacity. Hum. Mol. Genet. 18:3470 -3483.
56. Siitonen HA, et al. 2009. The mutation spectrum in RECQL4 diseases. Eur. J. Hum. Genet. 17:151-158.
57. Smith PJ, Paterson MC. 1982. Enhanced radiosensitivity and defective DNA repair in cultured fibroblasts derived from Rothmund Thomson syndrome patients. Mutat. Res. 94:213-228.
58. Stewart E, Chapman C, Al-Khodairy F, Carr A, Enoch T. 1997. rqh1+, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J. 16:2682-2692.
59. Ulrich HD. 2011. Timing and spacing of ubiquitin-dependent DNA damage bypass. FEBS Lett. 585:2861-2867.
60. Vennos EM, Collins M, James WD. 1992. Rothmund-Thomson syndrome: review of the world literature. J. Am. Acad. Dermatol. 27: 750-762.
61. Vennos EM, James WD. 1995. Rothmund-Thomson syndrome. Dermatol. Clin. 13:143-150.
62. Wechsler T, Newman S, West SC. 2011. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 471:642- 646.
63. Wood RD. 2010. Mammalian nucleotide excision repair proteins and interstrand crosslink repair. Environ. Mol. Mutagen. 51:520 -526.
64. Xu X, Liu Y. 2009. Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J. 28:568 -577.
65. Yin L, Locovei AM, D'Urso G. 2008. Activation of the DNA damage checkpoint in mutants defective in DNA replication initiation. Mol. Biol. Cell 19:4374-4382.