Conserved helicase domain of human RecQ4 is required for strand annealing-independent DNA unwinding

DNA Repair

Volumn 9, Issue 7, 2010, Pages 796-804

  Rossi, Marie L ^a   Ghosh, Avik K ^a   Kulikowicz, Tomasz ^a   Croteau, Deborah L ^a   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Aging; DNA repair; Helicases; RecQ helicase; Replication protein A

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BLOOM SYNDROME HELICASE; LYSINE; RECQ HELICASE; RECQ1 HELICASE; RECQ4 HELICASE; RECQ5 HELICASE; REPLICATION FACTOR A; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DENATURATION; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; POINT MUTATION; PRIORITY JOURNAL;

AMINO ACID MOTIFS; CELL NUCLEUS; CONSERVED SEQUENCE; DNA; DNA REPAIR; HUMANS; LYSINE; NUCLEIC ACID CONFORMATION; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; RECQ HELICASES; SUBSTRATE SPECIFICITY;

EID: 77953326659     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.04.003     Document Type: Article

References (67)

1. Bachrati C.Z., and Hickson I.D. RecQ helicases: guardian angels of the DNA replication fork. Chromosoma 117 (2008) 219-233
2. Brosh Jr. R.M., and Bohr V.A. Human premature aging, DNA repair and RecQ helicases. Nucleic Acids Res. 35 (2007) 7527-7544
3. Hanada K., and Hickson I.D. Molecular genetics of RecQ helicase disorders. Cell Mol. Life Sci. 64 (2007) 2306-2322
4. Sharma S., Doherty K.M., and Brosh Jr. R.M. Mechanisms of RecQ helicases in pathways of DNA metabolism and maintenance of genomic stability. Biochem. J. 398 (2006) 319-337
5. Singh D.K., Ahn B., and Bohr V.A. Roles of RECQ helicases in recombination based DNA repair, genomic stability and aging. Biogerontology 10 (2009) 235-252
6. Stinco G., Governatori G., Mattighello P., and Patrone P. Multiple cutaneous neoplasms in a patient with Rothmund-Thomson syndrome: case report and published work review. J. Dermatol. 35 (2008) 154-161
7. Vennos E.M., Collins M., and James W.D. Rothmund-Thomson syndrome: review of the world literature. J. Am. Acad. Dermatol. 27 (1992) 750-762
8. Anbari K.K., Ierardi-Curto L.A., Silber J.S., Asada N., Spinner N., Zackai E.H., Belasco J., Morrissette J.D., and Dormans J.P. Two primary osteosarcomas in a patient with Rothmund-Thomson syndrome. Clin. Orthop. Relat Res. (2000) 213-223
9. Der K., McGill V.J.J., Vekemans M., and Kopelman H.R. Clonal lines of aneuploid cells in Rothmund-Thomson syndrome. Am. J. Med. Genet. 37 (1990) 336-339
10. Durand F., Castorina P., Morant C., Delobel B., Barouk E., and Modiano P. Rothmund-Thomson syndrome, trisomy 8 mosaicism and RECQ4 gene mutation, Ann. Dermatol. Venereol. 129 (2002) 892-895
11. Orstavik K.H., McFadden N., Hagelsteen J., Ormerod E., and Hagen van der C.B. Instability of lymphocyte chromosomes in a girl with Rothmund-Thomson syndrome. J. Med. Genet. 31 (1994) 570-572
12. Jin W., Liu H., Zhang Y., Otta S.K., Plon S.E., and Wang L.L. Sensitivity of RECQL4-deficient fibroblasts from Rothmund-Thomson syndrome patients to genotoxic agents. Hum. Genet. 123 (2008) 643-653
13. Werner S.R., Prahalad A.K., Yang J., and Hock J.M. RECQL4-deficient cells are hypersensitive to oxidative stress/damage: insights for osteosarcoma prevalence and heterogeneity in Rothmund-Thomson syndrome. Biochem. Biophys. Res. Commun. 345 (2006) 403-409
14. Balraj P., Concannon P., Jamal R., Beghini A., Hoe T.S., Khoo A.S., and Volpi L. An unusual mutation in RECQ4 gene leading to Rothmund-Thomson syndrome. Mutat. Res. 508 (2002) 99-105
15. Kitao S., Shimamoto A., Goto M., Miller R.W., Smithson W.A., Lindor N.M., and Furuichi Y. Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22 (1999) 82-84
16. Lindor N.M., Furuichi Y., Kitao S., Shimamoto A., Arndt C., and Jalal S. 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 (2000) 223-228
17. Sangrithi M.N., Bernal J.A., Madine M., Philpott A., Lee J., Dunphy W.G., and Venkitaraman A.R. Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 121 (2005) 887-898
18. Matsuno K., Kumano M., Kubota Y., Hashimoto Y., and Takisawa H. 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 (2006) 4843-4852
19. Kumata Y., Tada S., Yamanada Y., Tsuyama T., Kobayashi T., Dong Y.P., Ikegami K., Murofushi H., Seki M., and Enomoto T. Possible involvement of RecQL4 in the repair of double-strand DNA breaks in Xenopus egg extracts. Biochim. Biophys. Acta 1773 (2007) 556-564
20. Xu Y., Lei Z., Huang H., Dui W., Liang X., Ma J., and Jiao R. dRecQ4 is required for DNA synthesis and essential for cell proliferation in Drosophila. PLoS One 4 (2009) e6107
21. Petkovic M., Dietschy T., Freire R., Jiao R., and Stagljar I. 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 (2005) 4261-4269
22. Fan W., and Luo J. RecQ4 facilitates UV light-induced DNA damage repair through interaction with nucleotide excision repair factor xeroderma pigmentosum group A (XPA). J. Biol. Chem. 283 (2008) 29037-29044
23. Woo L.L., Futami K., Shimamoto A., Furuichi Y., and Frank K.M. The Rothmund-Thomson gene product RECQL4 localizes to the nucleolus in response to oxidative stress. Exp. Cell Res. 312 (2006) 3443-3457
24. Schurman S.H., Hedayati M., Wang Z., Singh D.K., Speina E., Zhang Y., Becker K., Macris M., Sung P., Wilson III D.M., Croteau D.L., and Bohr V.A. Direct and indirect roles of RECQL4 in modulating base excision repair capacity. Hum. Mol. Genet. 18 (2009) 3470-3483
25. Macris M.A., Krejci L., Bussen W., Shimamoto A., and Sung P. Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair (Amst) 5 (2006) 172-180
26. Yin J., Kwon Y.T., Varshavsky A., and Wang W. RECQL4, mutated in the Rothmund-Thomson and RAPADILINO syndromes, interacts with ubiquitin ligases UBR1 and UBR2 of the N-end rule pathway. Hum. Mol. Genet. 13 (2004) 2421-2430
27. Suzuki T., Kohno T., and Ishimi Y. DNA helicase activity in purified human RECQL4 protein. J. Biochem. 146 (2009) 327-335
28. Xu X., and Liu Y. Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J. 28 (2009) 568-577
29. Henricksen L.A., Umbricht C.B., and Wold M.S. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269 (1994) 11121-11132
30. Araki M., Masutani C., Takemura M., Uchida A., Sugasawa K., Kondoh J., Ohkuma Y., and Hanaoka F. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J. Biol. Chem. 276 (2001) 18665-18672
31. Orren D.K., Brosh Jr. R.M., Nehlin J.O., Machwe A., Gray M.D., and Bohr V.A. Enzymatic and DNA binding properties of purified WRN protein: high affinity binding to single-stranded DNA but not to DNA damage induced by 4NQO. Nucleic Acids Res. 27 (1999) 3557-3566
32. Lloyd R.G., and Sharples G.J. Processing of recombination intermediates by the RecG and RuvAB proteins of Escherichia coli. Nucleic Acids Res. 21 (1993) 1719-1725
33. Karow J.K., Constantinou A., Li J.L., West S.C., and Hickson I.D. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc. Natl. Acad. Sci. U.S.A 97 (2000) 6504-6508
34. Huber M.D., Lee D.C., and Maizels N. G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucleic Acids Res. 30 (2002) 3954-3961
35. Sun H., Karow J.K., Hickson I.D., and Maizels N. The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem. 273 (1998) 27587-27592
36. Brosh Jr. R.M., Orren D.K., Nehlin J.O., Ravn P.H., Kenny M.K., Machwe A., and Bohr V.A. Functional and physical interaction between WRN helicase and human replication protein A. J. Biol. Chem. 274 (1999) 18341-18350
37. Brosh Jr. R.M., Li J.L., Kenny M.K., Karow J.K., Cooper M.P., Kureekattil R.P., Hickson I.D., and Bohr V.A. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275 (2000) 23500-23508
38. Cui S., Arosio D., Doherty K.M., Brosh Jr. R.M., Falaschi A., and Vindigni A. Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence of human replication protein A. Nucleic Acids Res. 32 (2004) 2158-2170
39. Doherty K.M., Sommers J.A., Gray M.D., Lee J.W., von K.C., Thoma N.H., Kureekattil R.P., Kenny M.K., and Brosh Jr. R.M. Physical and functional mapping of the replication protein a interaction domain of the werner and bloom syndrome helicases. J. Biol. Chem. 280 (2005) 29494-29505
40. Garcia P.L., Liu Y., Jiricny J., West S.C., and Janscak P. Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J. 23 (2004) 2882-2891
41. Shen J.C., Gray M.D., Oshima J., and Loeb L.A. Characterization of Werner syndrome protein DNA helicase activity: directionality, substrate dependence and stimulation by replication protein A. Nucleic Acids Res. 26 (1998) 2879-2885
42. Neff N.F., Ellis N.A., Ye T.Z., Noonan J., Huang K., Sanz M., and Proytcheva M. The DNA helicase activity of BLM is necessary for the correction of the genomic instability of bloom syndrome cells. Mol. Biol. Cell 10 (1999) 665-676
43. Sharma S., Sommers J.A., Choudhary S., Faulkner J.K., Cui S., Andreoli L., Muzzolini L., Vindigni A., and Brosh Jr. R.M. Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J. Biol. Chem. 280 (2005) 28072-28084
44. Capp C., Wu J., and Hsieh T.S. Drosophila RecQ4 has a 3′-5′ DNA helicase activity that is essential for viability. J. Biol. Chem. 284 (2009) 30845-30852
45. Georgaki A., Strack B., Podust V., and Hubscher U. DNA unwinding activity of replication protein A. FEBS Lett. 308 (1992) 240-244
46. Georgaki A., and Hubscher U. DNA unwinding by replication protein A is a property of the 70 kDa subunit and is facilitated by phosphorylation of the 32 kDa subunit. Nucleic Acids Res. 21 (1993) 3659-3665
47. Lao Y., Lee C.G., and Wold M.S. Replication protein A interactions with DNA. 2. Characterization of double-stranded DNA-binding/helix-destabilization activities and the role of the zinc-finger domain in DNA interactions. Biochemistry 38 (1999) 3974-3984
48. Treuner K., Ramsperger U., and Knippers R. Replication protein A induces the unwinding of long double-stranded DNA regions. J. Mol. Biol. 259 (1996) 104-112
49. Henricksen L.A., Tom S., Liu Y., and Bambara R.A. Inhibition of flap endonuclease 1 by flap secondary structure and relevance to repeat sequence expansion. J. Biol. Chem. 275 (2000) 16420-16427
50. Kao H.I., Veeraraghavan J., Polaczek P., Campbell J.L., and Bambara R.A. On the roles of Saccharomyces cerevisiae Dna2p and Flap endonuclease 1 in Okazaki fragment processing. J. Biol. Chem. 279 (2004) 15014-15024
51. Wang W., and Bambara R.A. Human Bloom protein stimulates flap endonuclease 1 activity by resolving DNA secondary structure. J. Biol. Chem. 280 (2005) 5391-5399
52. Ouyang K.J., Woo L.L., and Ellis N.A. Homologous recombination and maintenance of genome integrity: cancer and aging through the prism of human RecQ helicases. Mech. Ageing Dev. 129 (2008) 425-440
53. Bartos J.D., Wang W., Pike J.E., and Bambara R.A. Mechanisms by which Bloom protein can disrupt recombination intermediates of Okazaki fragment maturation. J. Biol. Chem. 281 (2006) 32227-32239
54. Kanagaraj R., Saydam N., Garcia P.L., Zheng L., and Janscak P. Human RECQ5beta helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res. 34 (2006) 5217-5231
55. Machwe A., Xiao L., Groden J., Matson S.W., and Orren D.K. RecQ family members combine strand pairing and unwinding activities to catalyze strand exchange. J. Biol. Chem. 280 (2005) 23397-23407
56. Wold M.S. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism, Annu. Rev. Biochem. 66 (1997) 61-92
57. Fry M., and Loeb L.A. Human werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n. J. Biol. Chem. 274 (1999) 12797-12802
58. Mohaghegh P., Karow J.K., Brosh Jr. J.R., Bohr V.A., and Hickson I.D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 29 (2001) 2843-2849
59. Popuri V., Bachrati C.Z., Muzzolini L., Mosedale G., Costantini S., Giacomini E., Hickson I.D., and Vindigni A. The Human RecQ helicases, BLM and RECQ1, display distinct DNA substrate specificities. J. Biol. Chem. 283 (2008) 17766-17776
60. Brosh Jr. R.M., von K.C., Sommers J.A., Karmakar P., Opresko P.L., Piotrowski J., Dianova I., Dianov G.L., and Bohr V.A. Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J. 20 (2001) 5791-5801
61. Sharma S., Sommers J.A., Wu L., Bohr V.A., Hickson I.D., and Brosh Jr. R.M. Stimulation of flap endonuclease-1 by the Bloom's syndrome protein. J. Biol. Chem. 279 (2004) 9847-9856
62. Cheng W.H., von K.C., Opresko P.L., Fields K.M., Ren J., Kufe D., and Bohr V.A. Werner syndrome protein phosphorylation by abl tyrosine kinase regulates its activity and distribution. Mol. Cell Biol. 23 (2003) 6385-6395
63. Karmakar P., Piotrowski J., Brosh Jr. R.M., Sommers J.A., Miller S.P., Cheng W.H., Snowden C.M., Ramsden D.A., and Bohr V.A. Werner protein is a target of DNA-dependent protein kinase in vivo and in vitro, and its catalytic activities are regulated by phosphorylation. J. Biol. Chem. 277 (2002) 18291-18302
64. Yannone S.M., Roy S., Chan D.W., Murphy M.B., Huang S., Campisi J., and Chen D.J. Werner syndrome protein is regulated and phosphorylated by DNA-dependent protein kinase. J. Biol. Chem. 276 (2001) 38242-38248
65. Muftuoglu M., Kusumoto R., Speina E., Beck G., Cheng W.H., and Bohr V.A. Acetylation regulates WRN catalytic activities and affects base excision DNA repair. PLoS One 3 (2008) e1918
66. Dietschy T., Shevelev I., Pena-Diaz J., Huhn D., Kuenzle S., Mak R., Miah M.F., Hess D., Fey M., Hottiger M.O., and Janscak P. I.Stagljar. p300-mediated acetylation of the Rothmund-Thomson-syndrome gene product RECQL4 regulates its subcellular localization. J. Cell Sci. 122 (2009) 1258-1267
67. Dietschy T., Shevelev I., and Stagljar I. The molecular role of the Rothmund-Thomson-, RAPADILINO- and Baller-Gerold-gene product, RECQL4: recent progress. Cell Mol. Life Sci. 64 (2007) 796-802