Human RECQL5 participates in the removal of endogenous DNA damage

Molecular Biology of the Cell

Volumn 23, Issue 21, 2012, Pages 4273-4285

  Tadokoro, Takashi ^a   Ramamoorthy, Mahesh ^a   Popuri, Venkateswarlu ^a   May, Alfred ^a   Tian, Jingyan ^a   Sykora, Peter ^a   Rybanska, Ivana ^a,b   Wilson III, David M ^a   Croteau, Deborah L ^a   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; HYDROGEN PEROXIDE; MENADIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; REACTIVE OXYGEN METABOLITE; RECQ HELICASE; RECQL5 PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CANCER CELL; CELL STRAIN HCT116; CELL SURVIVAL; CELL VIABILITY; COLORECTAL CANCER; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; HELA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INTERACTION;

DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HCT116 CELLS; HELA CELLS; HUMANS; LASERS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; POLY ADENOSINE DIPHOSPHATE RIBOSE; RECOMBINANT FUSION PROTEINS; RECQ HELICASES;

EID: 84868224735     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-02-0110     Document Type: Article

References (74)

1. Ahn B, Harrigan JA, Indig FE, Wilson DM III, Bohr VA (2004). Regulation of WRN helicase activity in human base excision repair. J Biol Chem 279, 53465-53474. (Pubitemid 40051852)
2. Anson RM, Hudson E, Bohr VA (2000). Mitochondrial endogenous oxidative damage has been overestimated. FASEB J 14, 355-360. (Pubitemid 30086072)
3. Asagoshi K et al. (2010). DNA polymerase beta-dependent long patch base excision repair in living cells. DNA Repair (Amst) 9, 109-119.
4. Aygun O, Svejstrup J, Liu YL (2008). A RECQ5-RNA polymerase II association identified by targeted proteomic analysis of human chromatin. Proc Natl Acad Sci USA 105, 8580-8584. (Pubitemid 351987723)
5. Bentley D, Selfridge J, Millar JK, Samuel K, Hole N, Ansell JD, Melton DW (1996). DNA ligase I is required for fetal liver erythropoiesis but is not essential for mammalian cell viability. Nat Genet 13, 489-491. (Pubitemid 26256628)
6. Bohr VA (2008). Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem Sci 33, 609-620.
7. Brosh RM Jr, Bohr VA (2007). Human premature aging, DNA repair and RecQ helicases. Nucleic Acids Res 35, 7527-7544.
8. Brosh RM Jr, von Kobbe C, Sommers JA, Karmakar P, Opresko PL, Piotrowski J, Dianova I, Dianov GL, Bohr VA (2001). Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J 20, 5791-5801. (Pubitemid 33010054)
9. Cabelof DC, Guo Z, Raffoul JJ, Sobol RW, Wilson SH, Richardson A, Heydari AR (2003). Base excision repair deficiency caused by polymerase beta haploinsufficiency: accelerated DNA damage and increased mutational response to carcinogens. Cancer Res 63, 5799-5807. (Pubitemid 37187477)
10. Caldecott KW (2008). Single-strand break repair and genetic disease. Nat Rev Genet 9, 619-631.
11. Campalans A, Marsin S, Nakabeppu Y, O'Connor TR, Boiteux S, Radicella JP (2005). XRCC1 interactions with multiple DNA glycosylases: a model for its recruitment to base excision repair. DNA Repair (Amst) 4, 826-835. (Pubitemid 40835854)
12. Chu WK, Hickson ID (2009). RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer 9, 644-654.
13. Das A et al. (2007). The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1. J Biol Chem 282, 26591-26602. (Pubitemid 47443759)
14. Dietschy T, Shevelev I, Stagljar I (2007). The molecular role of the Rothmund-Thomson-, RAPADI. Cell Mol Life Sci 64, 796-802.
15. Fan J, Otterlei M, Wong HK, Tomkinson AE, Wilson DM III (2004). XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res 32, 2193-2201. (Pubitemid 38864686)
16. Godon C, Cordelieres FP, Biard D, Giocanti N, Megnin-Chanet F, Hall J, Favaudon V (2008). PARP inhibition versus PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res 36, 4454-4464.
17. Golden TR, Hinerfeld DA, Melov S (2002). Oxidative stress and aging: beyond correlation. Aging Cell 1, 117-123.
18. Haince JF, McDonald D, Rodrigue A, Dery U, Masson JY, Hendzel MJ, Poirier GG (2008). PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem 283, 1197-1208.
19. Harrigan JA, Opresko PL, von Kobbe C, Kedar PS, Prasad R, Wilson SH, Bohr VA (2003). The Werner syndrome protein stimulates DNA polymerase beta strand displacement synthesis via its helicase activity. J Biol Chem 278, 22686-22695. (Pubitemid 36833256)
20. Harrigan JA, Wilson DM III, Prasad R, Opresko PL, Beck G, May A, Wilson SH, Bohr VA (2006). The Werner syndrome protein operates in base excision repair and cooperates with DNA polymerase beta. Nucleic Acids Res 34, 745-754. (Pubitemid 43240260)
21. Heeres JT, Hergenrother PJ (2007). Poly (ADP-ribose) makes a date with death. Curr Opin Chem Biol 11, 644-653. (Pubitemid 350180567)
22. Hu J, de Souza-Pinto NC, Haraguchi K, Hogue BA, Jaruga P, Greenberg MM, Dizdaroglu M, Bohr VA (2005a). Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes. J Biol Chem 280, 40544-40551. (Pubitemid 41780543)
23. Hu Y et al. (2007). RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev 21, 3073-3084. (Pubitemid 350223525)
24. Hu Y, Lu X, Barnes E, Yan M, Lou H, Luo G (2005b). Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol Cell Biol 25, 3431-3442. (Pubitemid 40559552)
25. Hu Y, Lu X, Zhou G, Barnes EL, Luo G (2009). Recql5 plays an important role in DNA replication and cell survival after camptothecin treatment. Mol Biol Cell 20, 114-123.
26. Imamura O, Fujita K, Itoh C, Takeda S, Furuichi Y, Matsumoto T (2002). Werner and Bloom helicases are involved in DNA repair in a complementary fashion. Oncogene 21, 954-963. (Pubitemid 34146309)
27. Islam MN, Fox D III, Guo R, Enomoto T, Wang W (2010). RecQL5 promotes genome stabilization through two parallel mechanisms-interacting with RNA polymerase II and acting as a helicase. Mol Cell Biol 30, 2460-2472.
28. Izumikawa K et al. (2008). Association of human DNA helicase RecQ5beta with RNA polymerase II and its possible role in transcription. Biochem J 413, 505-516.
29. Jeong YS, Kang Y, Lim KH, Lee MH, Lee J, Koo HS (2003). Deficiency of Caenorhabditis elegans RecQ5 homologue reduces life span and increases sensitivity to ionizing radiation. DNA Repair (Amst) 2, 1309-1319. (Pubitemid 37464810)
30. Jin R, Sun Y, Qi X, Zhang H, Zhang Y, Li N, Ding W, Chen D (2011). E2F1 is involved in DNA single-strand break repair through cell-cycledependent upregulation of XRCC1 expression. DNA Repair (Amst) 10, 926-933.
31. Kanagaraj R, Huehn D, MacKellar A, Menigatti M, Zheng L, Urban V, Shevelev I, Greenleaf AL, Janscak P (2010). RECQ5 helicase associates with the C-terminal repeat domain of RNA polymerase II during productive elongation phase of transcription. Nucleic Acids Res 38, 8131-8140.
32. Kanagaraj R, Saydam N, Garcia PL, Zheng L, Janscak P (2006). Human RECQ5beta helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res 34, 5217-5231. (Pubitemid 44742486)
33. Karmakar P et al. (2006). BLM is an early responder to DNA double-strand breaks. Biochem Biophys Res Commun 348, 62-69. (Pubitemid 44163482)
34. Kitao S, Ohsugi I, Ichikawa K, Goto M, Furuichi Y, Shimamoto A (1998). Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54, 443-452. (Pubitemid 29036231)
35. Kitao S, Shimamoto A, Goto M, Miller RW, Smithson WA, Lindor NM, Furuichi Y (1999). Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat Genet 22, 82-84. (Pubitemid 29214810)
36. Lan L, Nakajima S, Komatsu K, Nussenzweig A, Shimamoto A, Oshima J, Yasui A (2005). Accumulation of Werner protein at DNA double-strand breaks in human cells. J Cell Sci 118, 4153-4162. (Pubitemid 41488954)
37. Larsen E, Gran C, Saether BE, Seeberg E, Klungland A (2003). Proliferation failure and gamma radiation sensitivity of Fen1 null mutant mice at the blastocyst stage. Mol Cell Biol 23, 5346-5353. (Pubitemid 36950889)
38. Li M, Xu X, Liu Y (2011). The SET2-RPB1 interaction domain of human RECQ5 is important for transcription-associated genome stability. Mol Cell Biol 31, 2090-2099.
39. Lieber MR (1997). The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Bioessays 19, 233-240. (Pubitemid 27140647)
40. Lindor NM, Furuichi Y, Kitao S, Shimamoto A, Arndt C, Jalal S (2000). Rothmund-Thomson syndrome due to RECQ4 helicase mutations: report and clinical and molecular comparisons with Bloom syndrome and Werner syndrome. Am J Med Genet 90, 223-228. (Pubitemid 30051869)
41. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J (2007). RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900. (Pubitemid 350138084)
42. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G (1998). XRCC1 is specifically associated with poly (ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18, 3563-3571. (Pubitemid 28240528)
43. Morris EJ, Dreixler JC, Cheng KY, Wilson PM, Gin RM, Geller HM (1999). Optimization of single-cell gel electrophoresis (SCGE) for quantitative analysis of neuronal DNA damage. Biotechniques 26, 282-289. (Pubitemid 29072475)
44. Mortusewicz O, Rothbauer U, Cardoso MC, Leonhardt H (2006). Differential recruitment of DNA Ligase I and III to DNA repair sites. Nucleic Acids Res 34, 3523-3532.
45. Nakayama M, Yamaguchi S, Sagisu Y, Sakurai H, Ito F, Kawasaki K (2009). Loss of RecQ5 leads to spontaneous mitotic defects and chromosomal aberrations in Drosophila melanogaster. DNA Repair (Amst) 8, 232-241.
46. Opresko PL, von Kobbe C, Laine J P, Harrigan J, Hickson ID, Bohr VA (2002). Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J Biol Chem 277, 41110-41119. (Pubitemid 35215702)
47. Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR (2000). Poly (ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275, 40974-40980. (Pubitemid 32054922)
48. Popuri V, Croteau DL, Bohr VA (2010). Substrate specific stimulation of NEIL1 by WRN but not the other human RecQ helicases. DNA Repair (Amst) 9, 636-642.
49. Popuri V, Ramamoorthy M, Tadokoro T, Singh DK, Karmakar P, Croteau DL, Bohr VA (2012). Recruitment and retention dynamics of RECQL5 at DNA double strand break sites. DNA Repair (Amst) 11, 624-635.
50. Puebla-Osorio N, Lacey DB, Alt FW, Zhu C (2006). Early embryonic lethality due to targeted inactivation of DNA ligase III. Mol Cell Biol 26, 3935-3941. (Pubitemid 43726408)
51. Ramamoorthy M, Tadokoro T, Rybanska I, Ghosh AK, Wersto R, May A, Kulikowicz T, Sykora P, Croteau DL, Bohr VA (2012). RECQL5 cooperates with topoisomerase II alpha in DNA decatenation and cell cycle progression. Nucleic Acids Res 40, 1621-1635.
52. Saharia A, Guittat L, Crocker S, Lim A, Steffen M, Kulkarni S, Stewart SA (2008). Flap endonuclease 1 contributes to telomere stability. Curr Biol 18, 496-500.
53. Schurman SH et al. (2009). Direct and indirect roles of RECQL4 in modulating base excision repair capacity. Hum Mol Genet 18, 3470-3483.
54. Schwendener S, Raynard S, Paliwal S, Cheng A, Kanagaraj R, Shevelev I, Stark JM, Sung P, Janscak P (2010). Physical interaction of RECQ5 helicase with RAD51 facilitates its anti-recombinase activity. J Biol Chem 285, 15739-15745.
55. Sharma S, Otterlei M, Sommers JA, Driscoll HC, Dianov GL, Kao HI, Bambara RA, Brosh RM Jr (2004a). WRN helicase and FEN-1 form a complex upon replication arrest and together process branchmigrating DNA structures associated with the replication fork. Mol Biol Cell 15, 734-750. (Pubitemid 38146489)
56. Sharma S, Phatak P, Stortchevoi A, Jasin M, Larocque JR (2012). RECQ1 plays a distinct role in cellular response to oxidative DNA damage. DNA Repair (Amst) 11, 537-549.
57. Sharma S, Sommers JA, Wu L, Bohr VA, Hickson ID, Brosh RM Jr (2004b). Stimulation of flap endonuclease-1 by the Bloom's syndrome protein. J Biol Chem 279, 9847-9856. (Pubitemid 38372583)
58. Shen B, Singh P, Liu R, Qiu J, Zheng L, Finger LD, Alas S (2005). Multiple but dissectible functions of FEN-1 nucleases in nucleic acid processing, genome stability and diseases. Bioessays 27, 717-729. (Pubitemid 41153356)
59. Shigenaga MK, Park JW, Cundy KC, Gimeno CJ, Ames BN (1990). In vivo oxidative DNA damage: measurement of 8-hydroxy-2'-deoxyguanosine in DNA and urine by high-performance liquid chromatography with electrochemical detection. Methods Enzymol 186, 521-530. (Pubitemid 20279994)
60. Shimamoto A, Nishikawa K, Kitao S, Furuichi Y (2000). Human RecQ5beta, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3alpha and 3beta. Nucleic Acids Res 28, 1647-1655. (Pubitemid 30160578)
61. Singh DK, Ghosh AK, Croteau DL, Bohr VA (2012). RecQ helicases in DNA double strand break repair and telomere maintenance. Mutat Res 736, 15-24.
62. Singh DK, Karmakar P, Aamann M, Schurman SH, May A, Croteau DL, Burks L, Plon SE, Bohr VA (2010). The involvement of human RECQL4 in DNA double-strand break repair. Aging Cell 9, 358-371.
63. Speina E, Dawut L, Hedayati M, Wang Z, May A, Schwendener S, Janscak P, Croteau DL, Bohr VA (2010). Human RECQL5beta stimulates flap endonuclease 1. Nucleic Acids Res 38, 2904-2916.
64. Szekely AM, Bleichert F, Numann A, Van KS, Manasanch E, Ben NA, Canaan A, Weissman SM (2005). Werner protein protects nonproliferating cells from oxidative DNA damage. Mol Cell Biol 25, 10492-10506. (Pubitemid 41681970)
65. Tebbs RS, Flannery ML, Meneses JJ, Hartmann A, Tucker JD, Thompson LH, Cleaver JE, Pedersen RA (1999). Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev Biol 208, 513-529. (Pubitemid 29184008)
66. Thompson LH, West MG (2000). XRCC1 keeps DNA from getting stranded. Mutat Res 459, 1-18. (Pubitemid 30085463)
67. von Kobbe C, Bohr VA (2002). A nucleolar targeting sequence in the Werner syndrome protein resides within residues 949-1092. J Cell Sci 115, 3901-3907. (Pubitemid 35256491)
68. von Kobbe C, Harrigan JA, May A, Opresko PL, Dawut L, Cheng WH, Bohr VA (2003). Central role for the Werner syndrome protein/poly (ADP-ribose) polymerase 1 complex in the poly (ADP-ribosyl) ation pathway after DNA damage. Mol Cell Biol 23, 8601-8613. (Pubitemid 37433365)
69. 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. (Pubitemid 36539185)
70. Wang X, Lu X, Zhou G, Lou H, Luo G (2011). RECQL5 is an important determinant for camptothecin tolerance in human colorectal cancer cells. Biosci Rep 31, 363-369.
71. Wilson DM III, Bohr VA (2007). The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair (Amst) 6, 544-559. (Pubitemid 46357056)
72. Xanthoudakis S, Smeyne RJ, Wallace JD, Curran T (1996). The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc Natl Acad Sci USA 93, 8919-8923. (Pubitemid 26281992)
73. Yano K, Morotomi-Yano K, Wang SY, Uematsu N, Lee KJ, Asaithamby A, Weterings E, Chen DJ (2008). Ku recruits XLF to DNA double-strand breaks. EMBO Rep 9, 91-96.
74. Yu CE et al. (1996). Positional cloning of the Warner's syndrome gene. Science 272, 258-262.