Human SIRT1 regulates DNA binding and stability of the Mcm10 DNA replication factor via deacetylation

Nucleic Acids Research

Volumn 41, Issue 7, 2013, Pages 4065-4079

  Fatoba, Samuel T ^a   Tognetti, Silvia ^a   Berto, Melissa ^a   Leo, Elisabetta ^a,b   Mulvey, Claire M ^c   Godovac Zimmermann, Jasminka ^c   Pommier, Yves ^b   Okorokov, Andrei L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MCM10 PROTEIN; SIRTUIN 1; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; DEACETYLATION; DNA BINDING; DNA REPLICATION; DNA SYNTHESIS; HUMAN; HUMAN CELL; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STABILITY;

ACETYLATION; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; DNA REPLICATION; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; REPLICATION ORIGIN; SIRTUIN 1;

EUKARYOTA; METAZOA;

EID: 84876521963     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt131     Document Type: Article

References (77)

1. Bell, S.P. and Dutta, A. (2002) DNA replication in eukaryotic cells. Annu. Rev. Biochem., 71, 333-374. (Pubitemid 34800224)
2. Costa, S. and Blow, J.J. (2007) The elusive determinants of replication origins. EMBO Rep., 8, 332-334. (Pubitemid 46511032)
3. Mendez, J. and Stillman, B. (2003) Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays, 25, 1158-1167. (Pubitemid 37499316)
4. Remus, D. and Diffley, J.F. (2009) Eukaryotic DNA replication control: lock and load, then fire. Curr. Opin. Cell Biol., 21, 771-777.
5. Gregan, J., Lindner, K., Brimage, L., Franklin, R., Namdar, M., Hart, E.A., Aves, S.J. and Kearsey, S.E. (2003) Fission yeast Cdc23/Mcm10 functions after pre-replicative complex formation to promote Cdc45 chromatin binding. Mol. Biol. Cell, 14, 3876-3887. (Pubitemid 37151633)
6. Homesley, L., Lei, M., Kawasaki, Y., Sawyer, S., Christensen, T. and Tye, B.K. (2000) Mcm10 and the MCM2-7 complex interact to initiate DNA synthesis and to release replication factors from origins. Genes Dev., 14, 913-926. (Pubitemid 30253001)
7. Izumi, M., Yanagi, K., Mizuno, T., Yokoi, M., Kawasaki, Y., Moon, K.Y., Hurwitz, J., Yatagai, F. and Hanaoka, F. (2000) The human homolog of Saccharomyces cerevisiae Mcm10 interacts with replication factors and dissociates from nuclease-resistant nuclear structures in G(2) phase. Nucleic Acids Res., 28, 4769-4777.
8. Izumi, M., Yatagai, F. and Hanaoka, F. (2001) Cell cycle-dependent proteolysis and phosphorylation of human Mcm10. J. Biol. Chem., 276, 48526-48531.
9. Lee, J.K., Seo, Y.S. and Hurwitz, J. (2003) The Cdc23 (Mcm10) protein is required for the phosphorylation of minichromosome maintenance complex by the Dfp1-Hsk1 kinase. Proc. Natl Acad. Sci. USA, 100, 2334-2339. (Pubitemid 36297500)
10. Okorokov, A.L., Waugh, A., Hodgkinson, J., Murthy, A., Hong, H.K., Leo, E., Sherman, M.B., Stoeber, K., Orlova, E.V. and Williams, G.H. (2007) Hexameric ring structure of human MCM10 DNA replication factor. EMBO Rep., 8, 925-930. (Pubitemid 47500475)
11. Sawyer, S.L., Cheng, I.H., Chai, W. and Tye, B.K. (2004) Mcm10 and Cdc45 cooperate in origin activation in Saccharomyces cerevisiae. J. Mol. Biol., 340, 195-202. (Pubitemid 38759904)
12. Wohlschlegel, J.A., Dhar, S.K., Prokhorova, T.A., Dutta, A. and Walter, J.C. (2002) Xenopus Mcm10 binds to origins of DNA replication after Mcm2-7 and stimulates origin binding of Cdc45. Mol. Cell, 9, 233-240. (Pubitemid 34195550)
13. Izumi, M., Yatagai, F. and Hanaoka, F. (2004) Localization of human Mcm10 is spatially and temporally regulated during the S phase. J. Biol. Chem., 279, 32569-32577. (Pubitemid 39014713)
14. Fien, K. and Hurwitz, J. (2006) Fission yeast Mcm10p contains primase activity. J. Biol. Chem., 281, 22248-22260. (Pubitemid 44181928)
15. Fien, K., Cho, Y.S., Lee, J.K., Raychaudhuri, S., Tappin, I. and Hurwitz, J. (2004) Primer utilization by DNA polymerase alpha-primase is influenced by its interaction with Mcm10p. J. Biol. Chem., 279, 16144-16153. (Pubitemid 38509306)
16. Ricke, R.M. and Bielinsky, A.K. (2004) Mcm10 regulates the stability and chromatin association of DNA polymerase-alpha. Mol. Cell, 16, 173-185. (Pubitemid 39388833)
17. Zhu, W., Ukomadu, C., Jha, S., Senga, T., Dhar, S.K., Wohlschlegel, J.A., Nutt, L.K., Kornbluth, S. and Dutta, A. (2007) Mcm10 and And-1/CTF4 recruit DNA polymerase alpha to chromatin for initiation of DNA replication. Genes Dev., 21, 2288-2299. (Pubitemid 47443335)
18. Warren, E.M., Huang, H., Fanning, E., Chazin, W.J. and Eichman, B.F. (2009) Physical interactions between Mcm10, DNA, and DNA polymerase alpha. J. Biol. Chem., 284, 24662-24672.
19. Robertson, P.D., Chagot, B., Chazin, W.J. and Eichman, B.F. (2010) Solution NMR structure of the C-terminal DNA binding domain of Mcm10 reveals a conserved MCM motif. J. Biol. Chem., 285, 22942-22949.
20. Robertson, P.D., Warren, E.M., Zhang, H., Friedman, D.B., Lary, J.W., Cole, J.L., Tutter, A.V., Walter, J.C., Fanning, E. and Eichman, B.F. (2008) Domain architecture and biochemical characterization of vertebrate Mcm10. J. Biol. Chem., 283, 3338-3348.
21. Warren, E.M., Vaithiyalingam, S., Haworth, J., Greer, B., Bielinsky, A.K., Chazin, W.J. and Eichman, B.F. (2008) Structural basis for DNA binding by replication initiator Mcm10. Structure, 16, 1892-1901.
22. Pacek, M., Tutter, A.V., Kubota, Y., Takisawa, H. and Walter, J.C. (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell, 21, 581-587. (Pubitemid 43228013)
23. Park, J.H., Bang, S.W., Jeon, Y., Kang, S. and Hwang, D.S. (2008) Knockdown of human MCM10 exhibits delayed and incomplete chromosome replication. Biochem. Biophys. Res. Commun., 365, 575-582. (Pubitemid 350181682)
24. Park, J.H., Bang, S.W., Kim, S.H. and Hwang, D.S. (2008) Knockdown of human MCM10 activates G2 checkpoint pathway. Biochem. Biophys. Res. Commun., 365, 490-495. (Pubitemid 350181683)
25. Das-Bradoo, S., Ricke, R.M. and Bielinsky, A.K. (2006) Interaction between PCNA and diubiquitinated Mcm10 is essential for cell growth in budding yeast. Mol. Cell. Biol., 26, 4806-4817. (Pubitemid 43955799)
26. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M.L., Rehman, M., Walther, T.C., Olsen, J.V. and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science, 325, 834-840.
27. Hu, L.I., Lima, B.P. and Wolfe, A.J. (2010) Bacterial protein acetylation: the dawning of a new age. Mol. Microbiol., 77, 15-21.
28. Unnikrishnan, A., Gafken, P.R. and Tsukiyama, T. (2010) Dynamic changes in histone acetylation regulate origins of DNA replication. Nat. Struct. Mol. Biol., 17, 430-437.
29. Yang, X.J. and Seto, E. (2008) Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell, 31, 449-461.
30. Blander, G. and Guarente, L. (2004) The Sir2 family of protein deacetylases. Annu. Rev. Biochem., 73, 417-435. (Pubitemid 39050375)
31. Michan, S. and Sinclair, D. (2007) Sirtuins in mammals: insights into their biological function. Biochem. J., 404, 1-13. (Pubitemid 46788079)
32. Michishita, E., Park, J.Y., Burneskis, J.M., Barrett, J.C. and Horikawa, I. (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell., 16, 4623-4635. (Pubitemid 41416446)
33. Vaquero, A., Scher, M.B., Lee, D.H., Sutton, A., Cheng, H.L., Alt, F.W., Serrano, L., Sternglanz, R. and Reinberg, D. (2006) SirT2 is a histone deacetylase with preference for histone H4 Lys 16 during mitosis. Genes Dev., 20, 1256-1261. (Pubitemid 43727586)
34. Brooks, C.L, and Gu, W. (2009) Anti-aging protein SIRT1: a role in cervical cancer Aging (Albany NY), 1, 278-280.
35. Finkel, T., Deng, C.X. and Mostoslavsky, R. (2009) Recent progress in the biology and physiology of sirtuins. Nature, 460, 587-591.
36. Crampton, A., Chang, F., Pappas, D.L. Jr, Frisch, R.L. and Weinreich, M. (2008) An ARS element inhibits DNA replication through a SIR2-dependent mechanism. Mol. Cell, 30, 156-166. (Pubitemid 351626680)
37. Fox, C.A. and Weinreich, M. (2008) Beyond heterochromatin: SIR2 inhibits the initiation of DNA replication. Cell Cycle, 7, 3330-3334.
38. Pappas, D.L. Jr, Frisch, R. and Weinreich, M. (2004) The NAD(+)-dependent Sir2p histone deacetylase is a negative regulator of chromosomal DNA replication. Genes Dev., 18, 769-781. (Pubitemid 38480889)
39. Zappulla, D.C., Sternglanz, R. and Leatherwood, J. (2002) Control of replication timing by a transcriptional silencer. Curr. Biol., 12, 869-875. (Pubitemid 34689220)
40. Douglas, N.L., Dozier, S.K. and Donato, J.J. (2005) Dual roles for Mcm10 in DNA replication initiation and silencing at the mating-type loci. Mol. Biol. Rep., 32, 197-204. (Pubitemid 41674318)
41. Liachko, I. and Tye, B.K. (2005) Mcm10 is required for the maintenance of transcriptional silencing in Saccharomyces cerevisiae. Genetics, 171, 503-515. (Pubitemid 43156442)
42. Liachko, I. and Tye, B.K. (2009) Mcm10 mediates the interaction between DNA replication and silencing machineries. Genetics, 181, 379-391.
43. Jeong, J., Juhn, K., Lee, H., Kim, S.H., Min, B.H., Lee, K.M., Cho, M.H., Park, G.H. and Lee, K.H. (2007) SIRT1 promotes DNA repair activity and deacetylation of Ku70. Exp. Mol. Med., 39, 8-13. (Pubitemid 46356001)
44. Li, K., Casta, A., Wang, R., Lozada, E., Fan, W., Kane, S., Ge, Q., Gu, W., Orren, D. and Luo, J. (2008) Regulation of WRN protein cellular localization and enzymatic activities by SIRT1-mediated deacetylation. J. Biol. Chem., 283, 7590-7598.
45. Matsuzaki, H., Daitoku, H., Hatta, M., Aoyama, H., Yoshimochi, K. and Fukamizu, A. (2005) Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc. Natl Acad. Sci. USA, 102, 11278-11283. (Pubitemid 41153811)
46. Vaziri, H., Dessain, S.K., Ng Eaton, E., Imai, S.I., Frye, R.A., Pandita, T.K., Guarente, L. and Weinberg, R.A. (2001) hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell, 107, 149-159. (Pubitemid 33035942)
47. Yuan, Z., Zhang, X., Sengupta, N., Lane, W.S. and Seto, E. (2007) SIRT1 regulates the function of the Nijmegen breakage syndrome protein. Mol. Cell, 27, 149-162. (Pubitemid 46991383)
48. Fan, W. and Luo, J. (2010) SIRT1 regulates UV-induced DNA repair through deacetylating XPA. Mol. Cell, 39, 247-258.
49. Chen, L.F., Mu, Y. and Greene, W.C. (2002) Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J., 21, 6539-6548. (Pubitemid 35448431)
50. North, B.J., Marshall, B.L., Borra, M.T., Denu, J.M. and Verdin, E. (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell, 11, 437-444. (Pubitemid 36293837)
51. Conti, C., Seiler, J.A. and Pommier, Y. (2007) The mammalian DNA replication elongation checkpoint: implication of Chk1 and relationship with origin firing as determined by single DNA molecule and single cell analyses. Cell Cycle, 6, 2760-2767. (Pubitemid 350277167)
52. Conti, C., Leo, E., Eichler, G.S., Sordet, O., Martin, M.M., Fan, A., Aladjem, M.I. and Pommier, Y. (2010) Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res., 70, 4470-4480.
53. Wong, S. and Weber, J.D. (2007) Deacetylation of the retinoblastoma tumour suppressor protein by SIRT1. Biochem. J., 407, 451-460. (Pubitemid 350058478)
54. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J.V. and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc., 1, 2856-2860.
55. Liszt, G., Ford, E., Kurtev, M. and Guarente, L. (2005) Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J. Biol. Chem., 280, 21313-21320. (Pubitemid 40805693)
56. Bonner, W.M., Redon, C.E., Dickey, J.S., Nakamura, A.J., Sedelnikova, O.A., Solier, S. and Pommier, Y. (2008) GammaH2AX and cancer. Nat. Rev. Cancer, 8, 957-967.
57. Anglana, M., Apiou, F., Bensimon, A. and Debatisse, M. (2003) Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell, 114, 385-394. (Pubitemid 36962936)
58. Courbet, S., Gay, S., Arnoult, N., Wronka, G., Anglana, M., Brison, O. and Debatisse, M. (2008) Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature, 455, 557-560.
59. Yang, X.J. (2004) Lysine acetylation and the bromodomain: a new partnership for signaling. Bioessays, 26, 1076-1087.
60. Li, A., Xue, Y., Jin, C., Wang, M. and Yao, X. (2006) Prediction of Ne-acetylation on internal lysines implemented in Bayesian Discriminant Method. Biochem. Biophys. Res. Commun., 350, 818-824. (Pubitemid 44584171)
61. Sharma, A., Kaur, M., Kar, A., Ranade, S.M. and Saxena, S. (2010) Ultraviolet radiation stress triggers the down-regulation of essential replication factor Mcm10. J. Biol. Chem., 285, 8352-8362.
62. Kaur, M., Sharma, A., Khan, M., Kar, A. and Saxena, S. (2010) Mcm10 proteolysis initiates before the onset of M-phase. BMC Cell Biol., 11, 84.
63. Gay, S., Lachages, A.M., Millot, G.A., Courbet, S., Letessier, A., Debatisse, M. and Brison, O. (2010) Nucleotide supply, not local histone acetylation, sets replication origin usage in transcribed regions. EMBO Rep., 11, 698-704.
64. Iizuka, M. and Smith, M.M. (2003) Functional consequences of histone modifications. Curr. Opin. Genet. Dev., 13, 154-160. (Pubitemid 36369739)
65. Iizuka, M. and Stillman, B. (1999) Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J. Biol. Chem., 274, 23027-23034.
66. Miotto, B. and Struhl, K. (2010) HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol. Cell, 37, 57-66.
67. Terret, M.E., Sherwood, R., Rahman, S., Qin, J. and Jallepalli, P.V. (2009) Cohesin acetylation speeds the replication fork. Nature, 462, 231-234.
68. Glozak, M.A. and Seto, E. (2009) Acetylation/deacetylation modulates the stability of DNA replication licensing factor Cdt1. J. Biol. Chem., 284, 11446-11453.
69. Paolinelli, R., Mendoza-Maldonado, R., Cereseto, A. and Giacca, M. (2009) Acetylation by GCN5 regulates CDC6 phosphorylation in the S phase of the cell cycle. Nat. Struct. Mol. Biol., 16, 412-420.
70. Balakrishnan, L., Stewart, J., Polaczek, P., Campbell, J.L. and Bambara, R.A. (2010) Acetylation of Dna2 endonuclease/helicase and flap endonuclease 1 by p300 promotes DNA stability by creating long flap intermediates. J. Biol. Chem., 285, 4398-4404.
71. Woodward, A.M., Göhler, T., Luciani, M.G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D.A. and Blow, J.J. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol., 173, 673-683. (Pubitemid 46165576)
72. Ge, X.Q., Jackson, D.A. and Blow, J.J. (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev., 21, 3331-3341. (Pubitemid 350277759)
73. Gilbert, D.M. (2007) Replication origin plasticity, Taylor-made: inhibition vs recruitment of origins under conditions of replication stress. Chromosoma, 116, 341-347. (Pubitemid 46995574)
74. Ibarra, A., Schwob, E. and Méndez, J. (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl. Acad. Sci. USA, 105, 8956-8961.
75. van Deursen, F., Sengupta, S., De Piccoli, G., Sanchez-Diaz, A. and Labib, K. (2012) Mcm10 associates with the loaded DNA helicase at replication origins and defines a novel step in its activation. EMBO J., 31, 2195-2206.
76. Kanke, M., Kodama, Y., Takahashi, T.S., Nakagawa, T. and Masukata, H. (2012) Mcm10 plays an essential role in origin DNA unwinding after loading of the CMG components. EMBO J., 31, 2182-2194.
77. Watase, G., Takisawa, H. and Kanemaki, M.T. (2012) Mcm10 plays a role in functioning of the eukaryotic replicative DNA helicase, Cdc45-Mcm-GINS. Curr. Biol., 22, 343-349.