Translocation and stability of replicative DNA helicases upon encountering DNA-protein cross-links

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 4649-4658

  Nakano, Toshiaki ^a   Miyamoto Matsubara, Mayumi ^a   Shoulkamy, Mahmoud I ^a   Salem, Amir M H ^b   Pack, Seung Pil ^c   Ishimi, Yukio ^d   Ide, Hiroshi ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b NATIONAL RESEARCH CENTRE   (Egypt)

^c Korea University   (South Korea)

^d IBARAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DAMAGING AGENTS; DNA HELICASES; HELICASES; REPLISOMES; SIZE DEPENDENT;

PROTEINS;

DNA;

CARRIER PROTEIN; DNAB HELICASE; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN 467; T7 GENE 4 PROTEIN; UNCLASSIFIED DRUG; VIRUS LARGE T ANTIGEN;

ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; DNA PROTEIN COMPLEX; ENZYME STABILITY; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; GENE TRANSLOCATION; HUMAN; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DNA BINDING; REPLISOME;

ANIMALS; CROSS-LINKING REAGENTS; DNA; DNA DAMAGE; DNA HELICASES; DNAB HELICASES; ESCHERICHIA COLI; HUMANS; MADS DOMAIN PROTEINS; MODELS, GENETIC; NEURONAL PLASTICITY; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN TRANSPORT; SYNAPSES; TIME FACTORS; XENOPUS;

EID: 84874054977     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.419358     Document Type: Article

References (61)

1. Johnson, A., and O'Donnell, M. (2005) Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem. 74, 283-315
2. Hamdan, S. M., and Richardson, C. C. (2009) Motors, switches, and contacts in the replisome. Annu. Rev. Biochem. 78, 205-243
3. Alabert, C., and Groth, A. (2012) Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13, 153-167
4. Masai, H., Matsumoto, S., You, Z., Yoshizawa-Sugata, N., and Oda, M. (2010) Eukaryotic chromosome DNA replication: where, when, and how? Annu. Rev. Biochem. 79, 89-130
5. Yancey-Wrona, J. E., and Matson, S. W. (1992) Bound Lac repressor protein differentially inhibits the unwinding reactions catalyzed by DNA helicases. Nucleic Acids Res. 20, 6713-6721
6. Shin, J. H., and Santangelo., T. J., Xie, Y., Reeve, J. N., and Kelman, Z. (2007) Archaeal minichromosome maintenance (MCM) helicase can unwind DNA bound by archaeal histones and transcription factors. J. Biol. Chem. 282, 4908-4915
7. 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
8. Barker, S., Weinfeld, M., and Murray, D. (2005) DNA-protein crosslinks: their induction, repair, and biological consequences. Mutat. Res. 589, 111-135
9. Pommier, Y. (2009) DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem. Rev. 109, 2894-2902
10. Ide, H., and Shoulkamy., M. I., Nakano, T., Miyamoto-Matsubara, M., and Salem, A. M. (2011) Repair and biochemical effects of DNA-protein crosslinks. Mutat. Res. 711, 113-122
11. Shoulkamy, M. I., Nakano, T., Ohshima, M., Hirayama, R., Uzawa, A., Furusawa, Y., and Ide, H. (2012) Detection of DNA-protein crosslinks (DPCs) by novel direct fluorescence labeling methods: distinct stabilities of aldehyde and radiation-induced DPCs. Nucleic Acids Res. 40, e143
12. Kuo, H. K., and Griffith., J. D., and Kreuzer, K. N. (2007) 5-Azacytidine induced methyltransferase-DNA adducts block DNA replication in vivo. Cancer Res. 67, 8248-8254
13. Nakano, T., Morishita, S., Katafuchi, A., Matsubara, M., Horikawa, Y., Terato, H., Salem, A. M., Izumi, S., and Pack., S. P., Makino, K., and Ide, H. (2007) Nucleotide excision repair and homologous recombination systems commit differentially to the repair of DNA-protein cross-links. Mol. Cell 28, 147-158
14. Kumari, A., and 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
15. 2]: a concept for activation of the trans geometry in platinum antitumor complexes. Nucleic Acids Res. 31, 6450-6460
16. Chválová, K., Brabec, V., and Kaspárková, J. (2007) Mechanism of the formation of DNA-protein cross-links by antitumor cisplatin. Nucleic Acids Res. 35, 1812-1821
17. Nakano, T., Ouchi, R., Kawazoe, J., Pack, S. P., Makino, K., and Ide, H. (2012) T7 RNA polymerases backed up by covalently trapped proteins catalyze highly error-prone transcription. J. Biol. Chem. 287, 6562-6572
18. Patel, S. S., and Picha, K. M. (2000) Structure and function of hexameric helicases. Annu. Rev. Biochem. 69, 651-697
19. Bochman, M. L., and Schwacha, A. (2009) The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 73, 652-683
20. Costa, A., and Onesti, S. (2009) Structural biology of MCM helicases. Crit. Rev. Biochem. Mol. Biol. 44, 326-342
21. Ishimi, Y. (1997) A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. J. Biol. Chem. 272, 24508-24513
22. Sato, M., Gotow, T., You, Z., Komamura-Kohno, Y., Uchiyama, Y., Yabuta, N., Nojima, H., and Ishimi, Y. (2000) Electron microscopic observation and single-stranded DNA binding activity of the Mcm4, 6, 7 complex. J. Mol. Biol. 300, 421-431
23. Lee, J. K., and Hurwitz, J. (2000) Isolation and characterization of various complexes of the minichromosome maintenance proteins of Schizosac-charomyces pombe. J. Biol. Chem. 275, 18871-18878
24. Kaplan, D. L., and Davey., M. J., and O'Donnell, M. (2003) Mcm4, 6, 7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J. Biol. Chem. 278, 49171-49182
25. Li, D., Zhao, R., Lilyestrom, W., Gai, D., Zhang, R., DeCaprio, J. A., Fanning, E., Jochimiak, A., Szakonyi, G., and Chen, X. S. (2003) Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 423, 512-518
26. Bailey, S., and Eliason., W. K., and Steitz, T. A. (2007) Structure of hexameric DnaB helicase and its complex with a domain of DnaG primase. Science 318, 459-463
27. Fletcher, R. J., and Bishop., B. E., Leon, R. P., Sclafani, R. A., and Ogata., C. M., and Chen, X. S. (2003) The structure and function of MCM from archaeal M. thermoautotrophicum. Nat. Struct. Biol. 10, 160-167
28. 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
29. Veaute, X., Mari-Giglia, G., Lawrence, C. W., and Sarasin, A. (2000) UV lesions located on the leading strand inhibit DNA replication but do not inhibit SV40 T-antigen helicase activity. Mutat. Res. 459, 19-28
30. Suhasini, A. N., and 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 duplex DNA and is stimulated by replication protein A to unwind the damaged DNA substrate in a strand-specific manner. J. Biol. Chem. 284, 18458-18470
31. Yong, Y., and Romano, L. J. (1996) Benzo[α]pyrene-DNA adducts inhibit the DNA helicase activity of the bacteriophage T7 gene 4 protein. Chem. Res. Toxicol. 9, 179-187
32. Hacker, K. J., and Johnson, K. A. (1997) A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding. Biochemistry 36, 14080-14087
33. Graham, B. W., and 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 during MCM helicase unwinding. Nucleic Acids Res. 39, 6585-6595
34. Morris, P. D., and Raney, K. D. (1999) DNA helicases displace streptavidin from biotin-labeled oligonucleotides. Biochemistry 38, 5164-5171
35. Shin, J. H., Jiang, Y., Grabowski, B., Hurwitz, J., and Kelman, Z. (2003) Substrate requirements for duplex DNA translocation by the eukaryal and archaeal minichromosome maintenance helicases. J. Biol. Chem. 278, 49053-49062
36. Byrd, A. K., and Raney, K. D. (2004) Protein displacement by an assembly of helicase molecules aligned along single-stranded DNA. Nat. Struct. Mol. Biol. 11, 531-538
37. Azam, T. A., and Ishihama, A. (1999) Twelve species of the nucleoid-associated protein from Escherichia coli: sequence recognition specificity and DNA binding affinity. J. Biol. Chem. 274, 33105-33113
38. Pack, S. P., Nonogawa, M., Kodaki, T., and Makino, K. (2005) Chemical synthesis and thermodynamic characterization of oxanine-containing oli-godeoxynucleotides. Nucleic Acids Res. 33, 5771-5780
39. Katafuchi, A., Nakano, T., Masaoka, A., Terato, H., Iwai, S., Hanaoka, F., and Ide, H. (2004) Differential specificity of human and Escherichia coli endonuclease III and VIII homologues for oxidative base lesions. J. Biol. Chem. 279, 14464-14471
40. Numata, Y., Ishihara, S., Hasegawa, N., Nozaki, N., and Ishimi, Y. (2010) Interaction of human MCM2-7 proteins with TIM, TIPIN, and Rb. J. Biochem. 147, 917-927
41. Ishimi, Y., Komamura-Kohno, Y., Kwon, H. J., Yamada, K., and Nakanishi, M. (2003) Identification of MCM4as atarget of the DNA replication block checkpoint system. J. Biol. Chem. 278, 24644-24650
42. Ishimi, Y., and Matsumoto, K. (1993) Model system for DNA replication of a plasmid DNA containing the autonomously replicating sequence from Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 90, 5399-5403
43. Nakano, T., Katafuchi, A., Matsubara, M., Terato, H., Tsuboi, T., Masuda, T., Tatsumoto, T., and Pack., S. P., Makino, K., Croteau, D. L., Van Houten, B., Iijima, K., Tauchi, H., and Ide, H. (2009) Homologous recombination but not nucleotide excision repair plays a pivotal role in tolerance of DNAprotein cross-links in mammalian cells. J. Biol. Chem. 284, 27065-27076
44. Nakano, T., Katafuchi, A., Shimizu, R., Terato, H., Suzuki, T., Tauchi, H., Makino, K., Skorvaga, M., Van Houten, B., and Ide, H. (2005) Repair activity of base and nucleotide excision repair enzymes for guanine lesions induced by nitrosative stress. Nucleic Acids Res. 33, 2181-2191
45. Nakano, T., Terato, H., Asagoshi, K., Masaoka, A., Mukuta, M., Ohyama, Y., Suzuki, T., Makino, K., and Ide, H. (2003) DNA-protein cross-link formation mediated by oxanine: a novel genotoxic mechanism of nitric oxide-induced DNA damage. J. Biol. Chem. 278, 25264-25272
46. Bochman, M. L., and Schwacha, A. (2008) The Mcm2-7 complex has in vitro helicase activity. Mol. Cell 31, 287-293
47. Chen, H. J., and Chiu., W. L., Lin, W. P., and Yang, S. S. (2008) Investigation of DNA-protein cross-link formation between lysozyme and oxanine by mass spectrometry. ChemBioChem 9, 1074-1081
48. Jiao, J., and Simmons, D. T. (2003) Nonspecific double-stranded DNA binding activity of simian virus 40 large T antigen is involved in melting and unwinding of the origin. J. Virol. 77, 12720-12728
49. Cimprich, K. A., and Cortez, D. (2008) ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627
50. Takahashi, T. S., and Wigley., D. B., and Walter, J. C. (2005) Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase. Trends Biochem. Sci. 30, 437-444
51. Ilves, I., Petojevic, T., Pesavento, J. J., and Botchan, M. R. (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell 37, 247-258
52. Fu, Y. V., Yardimci, H., Long, D. T., and Ho., T. V., Guainazzi, A., Bermudez, V. P., Hurwitz, J., van Oijen, A., Schärer, O. D., and Walter, J. C. (2011) Selective bypass of alagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 146, 931-941
53. Gai, D., Zhao, R., Li, D., Finkielstein, C. V., and Chen, X. S. (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119, 47-60
54. Enemark, E. J., and Joshua-Tor, L. (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270-275
55. McGlynn, P., and Guy, C. P. (2008) Replication forks blocked by protein DNA complexes have limited stability in vitro. J. Mol. Biol. 381, 249-255
56. Possoz, C., and Filipe., S. R., Grainge, I., and Sherratt, D. J. (2006) Tracking of controlled Escherichia coli replication fork stalling and restart at repres-sor-bound DNA in vivo. EMBO J. 25, 2596-2604
57. Gabbai, C. B., and Marians, K. J. (2010) Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair 9, 202-209
58. Salem, A. M., Nakano, T., Takuwa, M., Matoba, N., Tsuboi, T., Terato, H., Yamamoto, K., Yamada, M., Nohmi, T., and Ide, H. (2009) Genetic analysis of repair and damage tolerance mechanisms for DNA-protein crosslinks in Escherichia coli. J. Bacteriol. 191, 5657-5668
59. Calzada, A., Hodgson, B., Kanemaki, M., Bueno, A., and Labib, K. (2005) Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 19, 1905-1919
60. Labib, K., and Hodgson, B. (2007) Replication fork barriers: pausing for a break or stalling for time? EMBO Rep. 8, 346-353
61. Ivessa, A. S., and Lenzmeier., B. A., Bessler, J. B., Goudsouzian, L.K., Schnakenberg, S. L., and Zakian, V. A. (2003) The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell 12, 1525-1536