RECQ1 is required for cellular resistance to replication stress and catalyzes strand exchange on stalled replication fork structures

Cell Cycle

Volumn 11, Issue 22, 2012, Pages 4252-4265

  Popuri, Venkateswarlu ^a   Croteau, Deborah L ^a   Brosh, Robert M ^a   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Chromosomal condensation; DNA replication; RecQ helicases; RECQ1; RPA phosphorylation; Strand exchange

Indexed keywords

CHECKPOINT KINASE 1; DNA; HELICASE; RECQ HELICASE; RECQ1 PROTEIN; RECQ4 HELICASE; RECQ5 BETA HELICASE; REPLICATION FACTOR A; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN;

ARTICLE; CATALYSIS; CELL DIVISION; CELL PROLIFERATION; CELL STRESS; CHROMOSOME; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; ENZYME ACTIVITY; EQUILIBRIUM CONSTANT; HUMAN; HUMAN CELL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

EID: 84869390406     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.22581     Document Type: Article

References (61)

1. Bohr VA. Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem Sci 2008; 33:609-20; PMID:18926708; http://dx.doi.org/10.1016/j.tibs.2008.09.003.
2. Singh DK, Ghosh AK, Croteau DL, Bohr VA. RecQ helicases in DNA double strand break repair and telomere maintenance. Mutat Res 2012; 736:15-24; PMID:21689668; http://dx.doi.org/10.1016/j.mrfmmm.2011.06.002.
3. Cheng WH, Muftic D, Muftuoglu M, Dawut L, Morris C, Helleday T, et al. WRN is required for ATM activation and the S-phase checkpoint in response to interstrand cross-link-induced DNA double-strand breaks. Mol Biol Cell 2008; 19:3923-33; PMID:18596239; http://dx.doi.org/10.1091/mbc.E07-07-0698.
4. Crabbe L, Verdun RE, Haggblom CI, Karlseder J. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 2004; 306:1951-3; PMID:15591207; http://dx.doi.org/10.1126/science.1103619.
5. Raynard S, Bussen W, Sung P. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J Biol Chem 2006; 281:13861-4; PMID:16595695; http://dx.doi.org/10.1074/jbc.C600051200.
6. Hu Y, Lu X, Barnes E, Yan M, Lou H, Luo G. Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol Cell Biol 2005; 25:3431-42; PMID:15831450; http://dx.doi.org/10.1128/MCB.25.9.3431-3442.2005.
7. Hu Y, Raynard S, Sehorn MG, Lu X, Bussen W, Zheng L, et al. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev 2007; 21:3073-84; PMID:18003859; http://dx.doi.org/10.1101/gad.1609107.
8. Puranam KL, Blackshear PJ. Cloning and characterization of RECQL, a potential human homologue of the Escherichia coli DNA helicase RecQ. J Biol Chem 1994; 269:29838-45; PMID:7961977.
9. Kawabe T, Tsuyama N, Kitao S, Nishikawa K, Shimamoto A, Shiratori M, et al. Differential regulation of human RecQ family helicases in cell transformation and cell cycle. Oncogene 2000; 19:4764-72; PMID:11032027; http://dx.doi.org/10.1038/sj.onc.1203841.
10. Thangavel S, Mendoza-Maldonado R, Tissino E, Sidorova JM, Yin J, Wang W, et al. Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol Cell Biol 2010; 30:1382-96; PMID:20065033; http://dx.doi.org/10. 1128/MCB.01290-09.
11. Sangrithi MN, Bernal JA, Madine M, Philpott A, Lee J, Dunphy WG, et al. Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 2005; 121:887-98; PMID:15960976; http://dx.doi.org/10.1016/j.cell.2005.05.015.
12. Xu X, Rochette PJ, Feyissa EA, Su TV, Liu Y. MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J 2009; 28:3005-14; PMID:19696745; http://dx.doi.org/10.1038/emboj.2009.235.
13. Cordeiro-Stone M, Zaritskaya LS, Price LK, Kaufmann WK. Replication fork bypass of a pyrimidine dimer blocking leading strand DNA synthesis. J Biol Chem 1997; 272:13945-54; PMID:9153257; http://dx.doi.org/10.1074/jbc.272.21.13945.
14. Lopes M, Foiani M, Sogo JM. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 2006; 21:15-27; PMID:16387650; http://dx.doi.org/10.1016/j. molcel.2005.11.015.
15. Barbour L, Xiao W. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat Res 2003; 532:137-55; PMID:14643434; http://dx.doi.org/10.1016/j.mrfmmm. 2003.08.014.
16. Bugreev DV, Rossi MJ, Mazin AV. Cooperation of RAD51 and RAD54 in regression of a model replication fork. Nucleic Acids Res 2011; 39:2153-64; PMID:21097884; http://dx.doi.org/10.1093/nar/gkq1139.
17. Cox MM. Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annu Rev Genet 2001; 35:53-82; PMID:11700277; http://dx.doi.org/10.1146/annurev.genet.35.102401.090016.
18. Sogo JM, Lopes M, Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 2002; 297:599-602; PMID:12142537; http://dx.doi.org/10.1126/science.1074023.
19. Zou H, Rothstein R. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 1997; 90:87-96; PMID:9230305; http://dx.doi.org/10.1016/S0092-8674(00)80316-5.
20. Kanagaraj R, Saydam N, Garcia PL, Zheng L, Janscak P. Human RECQ5beta helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res 2006; 34:5217-31; PMID:17003056; http://dx.doi.org/10.1093/nar/gkl677.
21. Machwe A, Xiao L, Lloyd RG, Bolt E, Orren DK. Replication fork regression in vitro by the Werner syndrome protein (WRN): holliday junction formation, the effect of leading arm structure and a potential role for WRN exonuclease activity. Nucleic Acids Res 2007; 35:5729-47; PMID:17717003; http://dx.doi.org/10.1093/nar/gkm561.
22. Popuri V, Bachrati CZ, Muzzolini L, Mosedale G, Costantini S, Giacomini E, et al. The Human RecQ helicases, BLM and RECQ1, display distinct DNA substrate specificities. J Biol Chem 2008; 283:17766-76; PMID:18448429; http://dx.doi.org/10.1074/jbc.M709749200.
23. Bugreev DV, Brosh RM Jr., Mazin AV. RECQ1 possesses DNA branch migration activity. J Biol Chem 2008; 283:20231-42; PMID:18495662; http://dx.doi.org/10. 1074/jbc.M801582200.
24. Mazina OM, Rossi MJ, Deakyne JS, Huang F, Mazin AV. Polarity and bypass of DNA heterology during branch migration of Holliday junctions by human RAD54, BLM, and RECQ1 proteins. J Biol Chem 2012; 287:11820-32; PMID:22356911; http://dx.doi.org/10.1074/jbc.M112.341347.
25. Sharma S, Sommers JA, Choudhary S, Faulkner JK, Cui S, Andreoli L, et al. Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J Biol Chem 2005; 280:28072-84; PMID:15899892; http://dx.doi.org/10.1074/jbc.M500264200.
26. Pike AC, Shrestha B, Popuri V, Burgess-Brown N, Muzzolini L, Costantini S, et al. Structure of the human RECQ1 helicase reveals a putative strand-separation pin. Proc Natl Acad Sci USA 2009; 106:1039-44; PMID:19151156; http://dx.doi.org/10.1073/pnas.0806908106.
27. Muzzolini L, Beuron F, Patwardhan A, Popuri V, Cui S, Niccolini B, et al. Different quaternary structures of human RECQ1 are associated with its dual enzymatic activity. PLoS Biol 2007; 5:e20; PMID:17227144; http://dx.doi.org/10. 1371/journal.pbio.0050020.
28. Wang H, Guan J, Wang H, Perrault AR, Wang Y, Iliakis G. Replication protein A2 phosphorylation after DNA damage by the coordinated action of ataxia telangiectasia-mutated and DNA-dependent protein kinase. Cancer Res 2001; 61:8554-63; PMID:11731442.
29. Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003; 300:1542-8; PMID:12791985; http://dx.doi.org/10.1126/science.1083430.
30. Rossi ML, Ghosh AK, Kulikowicz T, Croteau DL, Bohr VA. Conserved helicase domain of human RecQ4 is required for strand annealing-independent DNA unwinding. DNA Repair (Amst) 2010; 9:796-804; PMID:20451470; http://dx.doi.org/10.1016/j.dnarep.2010.04.003.
31. Brosh RM Jr., Waheed J, Sommers JA. Biochemical characterization of the DNA substrate specificity of Werner syndrome helicase. J Biol Chem 2002; 277:23236-45; PMID:11956187; http://dx.doi.org/10.1074/jbc.M111446200.
32. Capp C, Wu J, Hsieh TS. Drosophila RecQ4 has a 3'-5' DNA helicase activity that is essential for viability. J Biol Chem 2009; 284:30845-52; PMID:19759018; http://dx.doi.org/10.1074/jbc.M109.008052.
33. Ozsoy AZ, Ragonese HM, Matson SW. Analysis of helicase activity and substrate specificity of Drosophila RECQ5. Nucleic Acids Res 2003; 31:1554-64; PMID:12595564; http://dx.doi.org/10.1093/nar/gkg243.
34. Futami K, Ogasawara S, Goto H, Yano H, Furuichi Y. RecQL1 DNA repair helicase: A potential tumor marker and therapeutic target against hepatocellular carcinoma. Int J Mol Med 2010; 25:537-45; PMID:20198302.
35. Mendoza-Maldonado R, Faoro V, Bajpai S, Berti M, Odreman F, Vindigni M, et al. The human RECQ1 helicase is highly expressed in glioblastoma and plays an important role in tumor cell proliferation. Mol Cancer 2011; 10:83; PMID:21752281; http://dx.doi.org/10.1186/1476-4598-10-83.
36. Sharma S, Brosh RM Jr. Human RECQ1 is a DNA damage responsive protein required for genotoxic stress resistance and suppression of sister chromatid exchanges. PLoS One 2007; 2:e1297; PMID:18074021; http://dx.doi.org/10.1371/ journal.pone.0001297.
37. Wu Y, Brosh RM Jr. Distinct roles of RECQ1 in the maintenance of genomic stability. DNA Repair (Amst) 2010; 9:315-24; PMID:20061189; http://dx.doi.org/ 10.1016/j.dnarep.2009.12.010.
38. Noll DM, Mason TM, Miller PS. Formation and repair of interstrand cross-links in DNA. Chem Rev 2006; 106:277-301; PMID:16464006; http://dx.doi.org/10.1021/cr040478b.
39. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001; 15:2177-96; PMID:11544175; http://dx.doi.org/10.1101/ gad.914401.
40. Choi JH, Lindsey-Boltz LA, Kemp M, Mason AC, Wold MS, Sancar A. Reconstitution of RPA-covered single-stranded DNA-activated ATR-Chk1 signaling. Proc Natl Acad Sci USA 2010; 107:13660-5; PMID:20616048; http://dx.doi.org/10. 1073/pnas.1007856107.
41. Petermann E, Woodcock M, Helleday T. Chk1 promotes replication fork progression by controlling replication initiation. Proc Natl Acad Sci USA 2010; 107:16090-5; PMID:20805465; http://dx.doi.org/10.1073/pnas.1005031107.
42. Elvers I, Hagenkort A, Johansson F, Djureinovic T, Lagerqvist A, Schultz N, et al. CHK1 activity is required for continuous replication fork elongation but not stabilization of post-replicative gaps after UV irradiation. [Epub ahead of print]. Nucleic Acids Res 2012; 40:8440-8; PMID:22753029; http://dx.doi.org/10.1093/nar/gks646.
43. Futami K, Kumagai E, Makino H, Goto H, Takagi M, Shimamoto A, et al. Induction of mitotic cell death in cancer cells by small interference RNA suppressing the expression of RecQL1 helicase. Cancer Sci 2008; 99:71-80; PMID:17953710.
44. Pflumm MF, Botchan MR. Orc mutants arrest in metaphase with abnormally condensed chromosomes. Development 2001; 128:1697-707; PMID:11290306.
45. Petermann E, Helleday T. DNA replication-associated lesions: importance in early tumorigenesis and cancer therapy. Biochem Soc Trans 2007; 35:1352-4; PMID:17956349; http://dx.doi.org/10.1042/BST0351352.
46. Arai A, Chano T, Futami K, Furuichi Y, Ikebuchi K, Inui T, et al. RECQL1 and WRN proteins are potential therapeutic targets in head and neck squamous cell carcinoma. Cancer Res 2011; 71:4598-607; PMID:21571861; http://dx.doi.org/10.1158/0008-5472.CAN-11-0320.
47. Machwe A, Xiao L, Groden J, Orren DK. The Werner and Bloom syndrome proteins catalyze regression of a model replication fork. Biochemistry 2006; 45:13939-46; PMID:17115688; http://dx.doi.org/10.1021/bi0615487.
48. Ralf C, Hickson ID, Wu L. The Bloom's syndrome helicase can promote the regression of a model replication fork. J Biol Chem 2006; 281:22839-46; PMID:16766518; http://dx.doi.org/10.1074/jbc.M604268200.
49. Sidorova JM, Li N, Folch A, Monnat RJ Jr. The RecQ helicase WRN is required for normal replication fork progression after DNA damage or replication fork arrest. Cell Cycle 2008; 7:796-807; PMID:18250621; http://dx.doi.org/10. 4161/cc.7.6.5566.
50. Popuri V, Jing H, Ramamoorthy V, Tadokoro T, Croteau DL, Bohr VA. RECQL5 plays both co-operative and complementary roles with WRN syndrome helicase. Nucleic Acids Res 2012; In press.
51. Bessho T. Induction of DNA replication-mediated double strand breaks by psoralen DNA interstrand cross-links. J Biol Chem 2003; 278:5250-4; PMID:12473662; http://dx.doi.org/10.1074/jbc.M212323200.
52. Sharma S, Stumpo DJ, Balajee AS, Bock CB, Lansdorp PM, Brosh RM Jr., et al. RECQL, a member of the RecQ family of DNA helicases, suppresses chromosomal instability. Mol Cell Biol 2007; 27:1784-94; PMID:17158923; http://dx.doi.org/ 10.1128/MCB.01620-06.
53. Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39-85; PMID:15189136; http://dx.doi.org/10.1146/annurev. biochem.73.011303.073723.
54. Jinushi M. Chronic activation of DNA damage signals causes tumor immune evasion in the chemoresistant niche. Oncoimmunology 2012; 1:400-2; PMID:22737630; http://dx.doi.org/10.4161/onci.19123.
55. Futami K, Kumagai E, Makino H, Sato A, Takagi M, Shimamoto A, et al. Anticancer activity of RecQL1 helicase siRNA in mouse xenograft models. Cancer Sci 2008; 99:1227-36; PMID:18422747; http://dx.doi.org/10.1111/j.1349-7006.2008. 00794.x.
56. Breger KS, Smith L, Thayer MJ. Engineering translocations with delayed replication: evidence for cis control of chromosome replication timing. Hum Mol Genet 2005; 14:2813-27; PMID:16115817; http://dx.doi.org/10.1093/hmg/ddi314.
57. Matsuyama M, Goto H, Kasahara K, Kawakami Y, Nakanishi M, Kiyono T, et al. Nuclear Chk1 prevents premature mitotic entry. J Cell Sci 2011; 124:2113-9; PMID:21628425; http://dx.doi.org/10.1242/jcs.086488.
58. Garcia PL, Liu Y, Jiricny J, West SC, Janscak P. Human RECQ5beta, a protein with DNA helicase and strandannealing activities in a single polypeptide. EMBO J 2004; 23:2882-91; PMID:15241474; http://dx.doi.org/10.1038/ sj.emboj.7600301.
59. Tadokoro T, Kulikowicz T, Dawut L, Croteau DL, Bohr VA. DNA binding residues in the RQC domain of Werner protein are critical for its catalytic activities. Aging (Albany NY) 2012; 4:417-29; PMID:22713343.
60. Ramamoorthy M, Tadokoro T, Rybanska I, Ghosh AK, Wersto R, May A, et al. RECQL5 cooperates with Topoisomerase II alpha in DNA decatenation and cell cycle progression. Nucleic Acids Res 2012; 40:1621-35; PMID:22013166; http://dx.doi.org/10.1093/nar/gkr844.
61. Muniandy PA, Thapa D, Thazhathveetil AK, Liu ST, Seidman MM. Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J Biol Chem 2009; 284:27908-17; PMID:19684342; http://dx.doi.org/10.1074/jbc.M109. 029025.