DNA repair and replication fork helicases are differentially affected by alkyl phosphotriester lesion

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19188-19198

  Suhasini, Avvaru N ^a   Sommers, Joshua A ^a   Yu, Stephen ^a   Wu, Yuliang ^b   Xu, Ting ^c   Kelman, Zvi ^d   Kaplan, Daniel L ^e   Brosh, Robert M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; SUGARS;

CELLULARS; DNA ADDUCTS; DNA HELICASES; DNA REPLICATIONS; DNA UNWINDING; DNA-REPAIR; HELICASES; NUCLEIC ACID METABOLISM; PHOSPHOTRIESTER; REPLICATION FORK;

REPAIR;

BLOOM SYNDROME HELICASE; CHLR1 HELICASE; DNA; DNAB HELICASE; DOUBLE STRANDED DNA; ESTER DERIVATIVE; FANCJ HELICASE; HELICASE; MCM HELICASE; PHOSPHORIC ACID TRIESTER; PROTEIN UVRD1; RECQ HELICASE; RECQ1 HELICASE; SUGAR PHOSPHATE; UNCLASSIFIED DRUG; WRN HELICASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA DAMAGE; DNA DENATURATION; DNA MODIFICATION; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; HUMAN; NONHUMAN; PRIORITY JOURNAL;

EID: 84861722500     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.352757     Document Type: Article

References (53)

1. Jones, G. D., Le Pla, R. C., and Farmer, P. B. (2010) Phosphotriester adducts (PTEs). DNA's overlooked lesion. Mutagenesis 25, 3-16
2. Gorbalenya, A. E., Koonin, E. V., Donchenko, A. P., and Blinov, V. M. (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 17, 4713-4730 (Pubitemid 19165040)
3. Matson, S. W. (1991)DNAhelicases of Escherichia coli. Prog. Nucleic Acid Res. Mol. Biol. 40, 289-326
4. Brosh, R. M., Jr., and Bohr, V. A. (2007) Human premature aging, DNA repair, and RecQ helicases. Nucleic Acids Res. 35, 7527-7544
5. Hickson, I. D. (2003) RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3, 169-178
6. Aygün, O., and Svejstrup, J. Q. (2010) RECQL5 helicase. Connections to DNA recombination and RNA polymerase II transcription. DNA Repair 9, 345-353
7. Lu, X., Lou, H., and Luo, G. (2011) A Blm-Recql5 partnership in replication stress response. J. Mol. Cell. Biol. 3, 31-38
8. Wu, Y., and Brosh, R. M., Jr. (2010) Distinct roles of RECQ1 in the maintenance of genomic stability. DNA Repair 9, 315-324
9. White, M. F. (2009) Structure, function, and evolution of the XPD family of iron-sulfur-containing 5′→3′ DNA helicases. Biochem. Soc. Trans. 37, 547-551
10. van der Lelij, P., Chrzanowska, K. H., Godthelp, B. C., Rooimans, M. A., Oostra, A. B., Stumm, M., Zdzienicka, M. Z., Joenje, H., and de Winter, J. P. (2010) Warsaw breakage syndrome, a cohesinopathy associated with mutations in the XPD helicase family member DDX11/ChlR1. Am. J. Hum. Genet. 86, 262-266
11. Lehmann, A. R. (2001) The xeroderma pigmentosum group D (XPD) gene. One gene, two functions, three diseases. Genes Dev. 15, 15-23
12. Singleton, M. R., Dillingham, M. S., and Wigley, D. B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23-50
13. Lee, J. Y., and Yang, W. (2006) UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127, 1349-1360 (Pubitemid 44960421)
14. Killoran, M. P., and Keck, J. L. (2006) Sit down, relax, and unwind. Structural insights into RecQ helicase mechanisms. Nucleic Acids Res. 34, 4098-4105 (Pubitemid 44542189)
15. Fan, L., Fuss, J. O., Cheng, Q. J., Arvai, A. S., Hammel, M., Roberts, V. A., Cooper, P. K., and Tainer, J. A. (2008) XPD helicase structures and activities. Insights into the cancer and aging phenotypes from XPD mutations. Cell 133, 789-800 (Pubitemid 351715395)
16. Kuper, J., Wolski, S. C., Michels, G., and Kisker, C. (2012) Functional and structural studies of the nucleotide excision repair helicase XPD suggest a polarity for DNA translocation. EMBO J. 31, 494-502
17. Liu, H., Rudolf, J., Johnson, K. A., McMahon, S. A., Oke, M., Carter, L., McRobbie, A. M., Brown, S. E., Naismith, J. H., and White, M. F. (2008) Structure of the DNA repair helicase XPD. Cell 133, 801-812 (Pubitemid 351707686)
18. Wolski, S. C., Kuper, J., Hänzelmann, P., Truglio, J. J., Croteau, D. L., Van Houten, B., and Kisker, C. (2008) Crystal structure of the FeS clustercontaining nucleotide excision repair helicase XPD. PLoS Biol. 6, e149
19. Kaplan, D. L. (2000) The 3′-tail of a forked duplex sterically determines whether one or two DNA strands pass through the central channel of a replication fork helicase. J. Mol. Biol. 301, 285-299
20. Bochman, M. L., and Schwacha, A. (2009) TheMcmcomplex. Unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 73, 652-683
21. Sakakibara, N., Kelman, L. M., and Kelman, Z. (2009) Unwinding the structure and function of the archaealMCMhelicase. Mol. Microbiol. 72, 286-296
22. Forsburg, S. L. (2008) The MCM helicase. Linking checkpoints to the replication fork. Biochem. Soc. Trans. 36, 114-119
23. Suhasini, A. N., and Brosh, R. M. Jr. (2010) Mechanistic and biological aspects of helicase action on damaged DNA. Cell Cycle 9, 2317-2329
24. Brosh, R. M. Jr., Waheed, J., and Sommers, J. A. (2002) Biochemical characterization of the DNA substrate specificity of Werner syndrome helicase. J. Biol. Chem. 277, 23236-23245 (Pubitemid 34952151)
25. Cantor, S., Drapkin, R., Zhang, F., Lin, Y., Han, J., Pamidi, S., and Livingston, D. M. (2004) The BRCA1-associated protein BACH1 is a DNA helicase targeted by clinically relevant inactivating mutations. Proc. Natl. Acad. Sci. U.S.A. 101, 2357-2362 (Pubitemid 38269316)
26. Wu, Y., Sommers, J. A., Khan, I., de Winter, J. P., and Brosh, R. M., Jr. (2012) Biochemical characterization of Warsaw breakage syndrome helicase. J. Biol. Chem. 287, 1007-1021
27. Sharma, S., Sommers, J. A., Choudhary, S., Faulkner, J. K., Cui, S., Andreoli, L., Muzzolini, L., Vindigni, A., and Brosh, R. M., Jr. (2005) Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J. Biol. Chem. 280, 28072-28084 (Pubitemid 41076925)
28. Sharma, S., Otterlei, M., Sommers, J. A., Driscoll, H. C., Dianov, G. L., Kao, H. I., Bambara, R. A., and Brosh, R. M., Jr. (2004)WRNhelicase and FEN-1 form a complex upon replication arrest and together process branch migrating DNA structures associated with the replication fork. Mol. Biol. Cell 15, 734-750 (Pubitemid 38146489)
29. Kaplan, D. L., and O'Donnell, M. (2002) DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell 10, 647-657 (Pubitemid 35284180)
30. Shin, J. H., Heo, G. Y., and Kelman, Z. (2009) The Methanothermobacter thermautotrophicus MCM helicase is active as a hexameric ring. J. Biol. Chem. 284, 540-546
31. Guarné, A., Ramon-Maiques, S., Wolff, E. M., Ghirlando, R., Hu, X., Miller, J. H., and Yang, W. (2004) Structure of the MutL C-terminal domain: a model of intact MutL and its roles in mismatch repair.EMBOJ. 23, 4134-4145 (Pubitemid 39546152)
32. Gupta, R., Sharma, S., Sommers, J. A., Jin, Z., Cantor, S. B., and Brosh, R. M. Jr. (2005) Analysis of the DNA substrate specificity of the human BACH1 helicase associated with breast cancer. J. Biol. Chem. 280, 25450-25460 (Pubitemid 40962249)
33. Suhasini, A. N., Rawtani, N. A., Wu, Y., Sommers, J. A., Sharma, S., Mosedale, G., North, P. S., Cantor, S. B., Hickson, I. D., and Brosh, R. M., Jr. (2011) Interaction between the helicases genetically linked to Fanconi anemia group J and Bloom's syndrome. EMBO J. 30, 692-705
34. Cadman, C. J., Matson, S. W., and McGlynn, P. (2006) Unwinding of forked DNA structures by UvrD. J. Mol. Biol. 362, 18-25
35. Gupta, R., Sharma, S., Doherty, K. M., Sommers, J. A., Cantor, S. B., and Brosh, R. M. Jr. (2006) Inhibition of BACH1 (FANCJ) helicase by backbone discontinuity is overcome by increased motor ATPase or length of loading strand. Nucleic Acids Res. 34, 6673-6683 (Pubitemid 46017959)
36. Suhasini, A. N., Sommers, J. A., Mason, A. C., Voloshin, O. N., Camerini-Otero, R. D., Wold, M. S., and Brosh, R. M. Jr. (2009) FANCJ helicase uniquely senses oxidative base damage in either strand of duplexDNAand is stimulated by replication protein A to unwind the damaged DNA substrate in a strand-specific manner. J. Biol. Chem. 284, 18458-18470
37. Kumari, A., Minko, I. G., Smith, R. L., Lloyd, R. S., and McCullough, A. K. (2010) Modulation of UvrD helicase activity by covalent DNA-protein cross-links. J. Biol. Chem. 285, 21313-21322
38. Choudhary, S., Sommers, J. A., and Brosh, R. M. Jr. (2004) Biochemical and kinetic characterization of the DNA helicase and exonuclease activities of Werner syndrome protein. J. Biol. Chem. 279, 34603-34613 (Pubitemid 39318090)
39. Graham, B. W., Schauer, G. D., Leuba, S. H., and Trakselis, M. A. (2011) Steric exclusion and wrapping of the excluded DNA strand occurs along discrete external binding paths duringMCMhelicase unwinding. Nucleic Acids Res. 39, 6585-6595
40. Garcia, P. L., Bradley, G., Hayes, C. J., Krintel, S., Soultanas, P., and Janscak, P. (2004) RPA alleviates the inhibitory effect of vinylphosphonate internucleotide linkages on DNA unwinding by BLM and WRN helicases. Nucleic Acids Res. 32, 3771-3778 (Pubitemid 39157724)
41. Bertram, R. D., Hayes, C. J., and Soultanas, P. (2002) Vinylphosphonate internucleotide linkages inhibit the activity of PcrA DNA helicase. Biochemistry 41, 7725-7731 (Pubitemid 34627799)
42. Maluf, N. K., Fischer, C. J., and Lohman, T. M. (2003) A dimer of Escherichia coli UvrD is the active form of the helicase in vitro. J. Mol. Biol. 325, 913-935 (Pubitemid 36263404)
43. Fischer, C. J., Maluf, N. K., and Lohman, T. M. (2004) Mechanism of ATP-dependent translocation of E. coli UvrD monomers along singlestranded DNA. J. Mol. Biol. 344, 1287-1309 (Pubitemid 39550478)
44. Soultanas, P., and Wigley, D. B. (2001) Unwinding the "Gordian knot" of helicase action. Trends Biochem. Sci. 26, 47-54 (Pubitemid 32124710)
45. Xu, H. Q., Deprez, E., Zhang, A. H., Tauc, P., Ladjimi, M. M., Brochon, J. C., Auclair, C., and Xi, X. G. (2003) The Escherichia coli RecQ helicase functions as a monomer. J. Biol. Chem. 278, 34925-34933 (Pubitemid 37102252)
46. Zhang, X. D., Dou, S. X., Xie, P., Hu, J. S., Wang, P. Y., and Xi, X. G. (2006) Escherichia coli RecQ is a rapid, efficient, and monomeric helicase. J. Biol. Chem. 281, 12655-12663 (Pubitemid 43855355)
47. Lucic, B., Zhang, Y., King, O., Mendoza-Maldonado, R., Berti, M., Niesen, F. H., Burgess-Brown, N. A., Pike, A. C., Cooper, C. D., Gileadi, O., and Vindigni, A. (2011) A prominent β-hairpin structure in the winged-helix domain of RECQ1 is required for DNA unwinding and oligomer formation. Nucleic Acids Res. 39, 1703-1717
48. Karow, J. K., Newman, R. H., Freemont, P. S., and Hickson, I. D. (1999) Oligomeric ring structure of the Bloom's syndrome helicase. Curr. Biol. 9, 597-600 (Pubitemid 29273108)
49. Janscak, P., Garcia, P. L., Hamburger, F., Makuta, Y., Shiraishi, K., Imai, Y., Ikeda, H., and Bickle, T. A. (2003) Characterization and mutational analysis of the RecQ core of the Bloom syndrome protein. J. Mol. Biol. 330, 29-42 (Pubitemid 36890590)
50. West, S. C. (1997) Processing of recombination intermediates by the Ruv-ABC proteins. Annu. Rev. Genet. 31, 213-244
51. Compton, S. A., Tolun, G., Kamath-Loeb, A. S., Loeb, L. A., and Griffith, J. D. (2008) The Werner syndrome protein binds replication fork and holliday junction DNAs as an oligomer. J. Biol. Chem. 283, 24478-24483
52. Sontz, P. A., Mui, T. P., Fuss, J. O., Tainer, J. A., and Barton, J. K. (2012) DNA charge transport as a first step in coordinating the detection of lesions by repair proteins. Proc. Natl. Acad. Sci. U.S.A. 109, 1856-1861
53. Yashiki, T., Yamana, K., Nunota, K., and Negishi, K. (1992) Sequencespecific block of in vitro DNA synthesis with isopropyl phosphotriesters in template oligodeoxyribonucleotides. Nucleic Acids Symp. Ser. 27, 197-198