The helicase domain and C-terminus of human RecQL4 facilitate replication elongation on DNA templates damaged by ionizing radiation

Carcinogenesis

Volumn 33, Issue 6, 2012, Pages 1203-1210

  Kohzaki, Masaoki ^a   Chiourea, Maria ^b   Versini, Gwennaelle ^a   Adachi, Noritaka ^c   Takeda, Shunichi ^d   Gagos, Sarantis ^b   Halazonetis, Thanos D ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; GENOMIC DNA; HELICASE; HYDROXYUREA; RECQ HELICASE; RECQL4 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE S PHASE; CELL MATURATION; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA TEMPLATE; GENE DELETION; GENE EXPRESSION; GENE TARGETING; HOMOZYGOSITY; HUMAN; HUMAN CELL; IONIZING RADIATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; RADIATION EXPOSURE; WILD TYPE;

CELL LINE; DNA; DNA DAMAGE; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS; HYDROXYUREA; PRECURSOR CELLS, B-LYMPHOID; PROTEIN STRUCTURE, TERTIARY; RADIATION, IONIZING; RECQ HELICASES;

EID: 84864322966     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgs149     Document Type: Article

References (56)

1. Bohr, V.A. (2008) Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci., 33, 609-620.
2. Chu,W.K. et al. (2009) RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer, 9, 644-654.
3. Petermann,E. et al. (2010) Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol., 11, 683-687.
4. Branzei,D. et al. (2010) Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol., 11, 208-219.
5. Wu,L. et al. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature, 426, 870-874.
6. Raynard,S. et al. (2006) A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J. Biol. Chem., 281, 13861-13864.
7. Seki,M. et al. (2006) Bloom helicase and DNA topoisomerase IIIalpha are involved in the dissolution of sister chromatids. Mol. Cell. Biol., 26, 6299-6307.
8. Liberi,G. et al. (2005) Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev., 19, 339-350.
9. Crabbe,L. et al. (2004) Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science, 306, 1951-1953.
10. Laud,P.R. et al. (2005) Elevated telomere-telomere recombination in WRN-deficient, telomere dysfunctional cells promotes escape from senescence and engagement of the ALT pathway. Genes Dev., 19, 2560-2570.
11. Masai,H. (2011) RecQL4: a helicase linking formation and maintenance of a replication fork. J. Biochem., 149, 629-631.
12. Kamimura,Y. et al. (1998) Sld2, which interacts with Dpb11 in Saccharomyces cerevisiae, is required for chromosomal DNA replication. Mol. Cell. Biol., 18, 6102-6109.
13. Masumoto,H. et al. (2002) S-Cdk-dependent phosphorylation of Sld2 essential for chromosomal DNA replication in budding yeast. Nature, 415, 651-655.
14. Zegerman,P. et al. (2007) Phosphorylation of Sld2 and Sld3 by cyclindependent kinases promotes DNA replication in budding yeast. Nature, 445, 281-285.
15. Tanaka,S. et al. (2007) CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature, 445, 328-332.
16. Noguchi,E. et al. (2002) CDK phosphorylation of Drc1 regulates DNA replication in fission yeast. Curr. Biol., 12, 599-605.
17. Xu,X. et al. (2009) MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J., 28, 3005-3014.
18. Im,J.S. et al. (2009) Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc. Natl Acad. Sci. USA, 106, 15628-15632.
19. Thangavel,S. et al. (2010) Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol. Cell. Biol., 30, 1382-1396.
20. Sangrithi,M.N. et al. (2005) Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell, 121, 887-898.
21. Matsuno,K. et al. (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.
22. Wu,J. et al. (2008) Drosophila homologue of the Rothmund-Thomson syndrome gene: essential function in DNA replication during development. Dev. Biol., 323, 130-142.
23. Xu,Y. et al. (2009) dRecQ4 is required for DNA synthesis and is essential for cell proliferation in Drosophila. PLoS One, 4, e6107.
24. Hoki,Y. et al. (2003) Growth retardation and skin abnormalities of the Recql4-deficient mouse. Hum. Mol. Genet., 12, 2293-2299.
25. Kitao,S. et al. (1999) Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet., 22, 82-84.
26. Wang,L.L. et al. (2003) Association between osteosarcoma and deleterious mutations in the RECQL4 gene in Rothmund-Thomson syndrome. J. Natl. Cancer Inst., 95, 669-674.
27. Siitonen,H.A. et al. (2003) Molecular defect of RAPADILINO syndrome expands the phenotype spectrum of RECQL diseases. Hum. Mol. Genet., 12, 2837-2844.
28. Siitonen,H.A. et al. (2009) The mutation spectrum in RECQL4 diseases. Eur. J. Hum. Genet., 17, 151-158.
29. Cabral,R.E. et al. (2008) Identification of new RECQL4 mutations in Caucasian Rothmund-Thomson patients and analysis of sensitivity to a wide range of genotoxic agents. Mutat. Res., 643, 41-47.
30. Van Maldergem, L. et al. (2006) Revisiting the craniosynostosis-radial ray hypoplasia association: Baller-Gerold syndrome caused by mutations in the RECQL4 gene. J. Med. Genet., 43, 148-152.
31. Abe,T. et al. (2011) The N-terminal region of RECQL4 lacking the helicase domain is both essential and sufficient for the viability of vertebrate cells. Role of the N-terminal region of RECQL4 in cells. Biochim. Biophys. Acta, 1813, 473-479.
32. Capp,C. et al. (2009) Drosophila RecQ4 has a 3'-5' DNA helicase activity that is essential for viability. J. Biol. Chem., 284, 30845-30852.
33. Jin,W. et al. (2008) Sensitivity of RECQL4-deficient fibroblasts from Rothmund-Thomson syndrome patients to genotoxic agents. Hum. Genet., 123, 643-653.
34. Werner,S.R. et al. (2006) RECQL4-deficient cells are hypersensitive to oxidative stress/damage: insights for osteosarcoma prevalence and heterogeneity in Rothmund-Thomson syndrome. Biochem. Biophys. Res. Commun., 345, 403-409.
35. Fan,W. et al. (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.
36. Singh,D.K. et al. (2010) The involvement of human RECQL4 in DNA double-strand break repair. Aging Cell, 9, 358-371.
37. Cescutti,R. et al. (2010) TopBP1 functions with 53BP1 in the G1 DNA damage checkpoint. EMBO J., 29, 3723-3732.
38. Mochan,T.A. et al. (2003) 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res., 63, 8586-8591.
39. Bailey,S.M. et al. (2004) Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res., 32, 3743-3751.
40. Michalet,X. et al. (1997) Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science, 277, 1518-1523.
41. Burks,L.M. et al. (2007) Nuclear import and retention domains in the amino terminus of RECQL4. Gene, 391, 26-38.
42. Suzuki,T. et al. (2009) DNA helicase activity in purified human RECQL4 protein. J. Biochem., 146, 327-335.
43. Xu,X. et al. (2009) Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J., 28, 568-577.
44. Rossi,M.L. et al. (2010) Conserved helicase domain of human RecQ4 is required for strand annealing-independent DNA unwinding. DNA Repair (Amst), 9, 796-804.
45. Adachi,N. et al. (2006) The human pre-B cell line Nalm-6 is highly proficient in gene targeting by homologous recombination. DNA Cell Biol., 25, 19-24.
46. So,S. et al. (2004) Genetic interactions between BLM and DNA ligase IV in human cells. J. Biol. Chem., 279, 55433-55442.
47. Mann,M.B. 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.
48. Jackson,S.P. et al. (2009) The DNA-damage response in human biology and disease. Nature, 461, 1071-1078.
49. Seiler,J.A. et al. (2007) The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol. Cell. Biol., 27, 5806-5818.
50. Petkovic,M. et al. (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.
51. Kumata,Y. et al. (2007) Possible involvement of RecQL4 in the repair of double-strand DNA breaks in Xenopus egg extracts. Biochim. Biophys. Acta, 1773, 556-564.
52. Park,S.J. et al. (2006) A positive involvement of RecQL4 in UV-induced S-phase arrest. DNA Cell Biol., 25, 696-703.
53. Kondo,S. et al. (2011) A genome-wide RNAi screen identifies core components of the G2-M DNA damage checkpoint. Sci. Signal., 4, rs1.
54. Zou,L. et al. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548.
55. Imamura,O. et al. (2002)Werner and Bloom helicases are involved in DNA repair in a complementary fashion. Oncogene, 21, 954-963.
56. Wang,W. et al. (2003) Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chromatid exchange formation. Mol. Cell. Biol., 23, 3527-3535.