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Molecular Mechanism for Chromatin Regulation During MCM Loading in Mammalian Cells

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Book cover DNA Replication

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1042))

Abstract

DNA replication is a fundamental process required for the accurate and timely duplication of chromosomes. During late mitosis to G1 phase, the MCM2-7 complex is loaded onto chromatin in a manner dependent on ORC, CDC6, and Cdt1, and chromatin becomes licensed for replication. Although every eukaryotic organism shares common features in replication control, there are also some differences among species. For example, in higher eukaryotic cells including human cells, no strict sequence specificity has been observed for replication origins, unlike budding yeast or bacterial replication origins. Therefore, elements other than beyond DNA sequences are important for regulating replication. For example, the stability and precise positioning of nucleosomes affects replication control. However, little is known about how nucleosome structure is regulated when replication licensing occurs. During the last decade, histone acetylation enzyme HBO1, chromatin remodeler SNF2H, and histone chaperone GRWD1 have been identified as chromatin-handling factors involved in the promotion of replication licensing. In this review, we discuss how the rearrangement of nucleosome formation by these factors affects replication licensing.

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References

  • Aalfs JD, Kingston RE (2000) What does ‘chromatin remodeling’ mean? Trends Biochem Sci 25:548–555

    Article  CAS  PubMed  Google Scholar 

  • Abe T, Sugimura K, Hosono Y, Takami Y, Akita M, Yoshimura A, Tada S, Nakayama T, Murofushi H, Okumura K, Takeda S, Horikoshi M, Seki M, Enomoto T (2011) The histone chaperone facilitates chromatin transcription (FACT) protein maintains normal replication fork rates. J Biol Chem 286:30504–30512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aggarwal BD, Calvi BR (2004) Chromatin regulates origin activity in Drosophila follicle cells. Nature 430:372–376

    Article  CAS  PubMed  Google Scholar 

  • Aizawa M, Sugimoto N, Watanabe S, Yoshida K, Fujita M (2016) Nucleosome assembly and disassembly activity of GRWD1, a novel Cdt1-binding protein that promotes pre-replication complex formation. Biochim Biophys Acta 1863:2739–2748

    Google Scholar 

  • Alenghat T, Yu J, Lazar MA (2006) The N-CoR complex enables chromatin remodeler SNF2H to enhance repression by thyroid hormone receptor. EMBO J 25:3966–3974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Annunziato AT, Hansen JC (2000) Role of histone acetylation in the assembly and modulation of chromatin structures. Gene Expr 9:37–61

    Article  CAS  PubMed  Google Scholar 

  • Araki H (2011) Initiation of chromosomal DNA replication in eukaryotic cells; contribution of yeast genetics to the elucidation. Genes Genet Syst 86:141–149

    Article  CAS  PubMed  Google Scholar 

  • Arias EE, Walter JC (2006) PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat Cell Biol 8:84–90

    Article  CAS  PubMed  Google Scholar 

  • Arias EE, Walter JC (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev 21:497–518

    Article  CAS  PubMed  Google Scholar 

  • Au TJ, Rodriguez J, Vincent JA, Tsukiyama T (2011) ATP-dependent chromatin remodeling factors tune S phase checkpoint activity. Mol Cell Biol 31:4454–4463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avvakumov N, Cote J (2007) The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene 26:5395–5407

    Article  CAS  PubMed  Google Scholar 

  • Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, Tsui K, Carlson CD, Gossett AJ, Hasinoff MJ, Warren CL, Gebbia M, Talukder S, Yang A, Mnaimneh S, Terterov D, Coburn D, Li Yeo A, Yeo ZX, Clarke ND, Lieb JD, Ansari AZ, Nislow C, Hughes TR (2008) A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol Cell 32:878–887

    Google Scholar 

  • Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR (2002) Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420:833–837

    Article  CAS  PubMed  Google Scholar 

  • Bell SP, Stillman B (1992) ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357:128–134

    Article  CAS  PubMed  Google Scholar 

  • Besnard E, Babled A, Lapasset L, Milhavet O, Parrinello H, Dantec C, Marin JM, Lemaitre JM (2012) Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol 19:837–844

    Article  CAS  PubMed  Google Scholar 

  • Bleichert F, Botchan MR, Berger JM (2017) Mechanisms for initiating cellular DNA replication. Science 355:eaah6317

    Article  PubMed  CAS  Google Scholar 

  • Bosco G, Du W, Orr-Weaver TL (2001) DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat Cell Biol 3:289–295

    Article  CAS  PubMed  Google Scholar 

  • Bowers JL, Randell JC, Chen S, Bell SP (2004) ATP hydrolysis by ORC catalyzes reiterative Mcm2-7 assembly at a defined origin of replication. Mol Cell 16:967–978

    Article  CAS  PubMed  Google Scholar 

  • Cadoret JC, Meisch F, Hassan-Zadeh V, Luyten I, Guillet C, Duret L, Quesneville H, Prioleau MN (2008) Genome-wide studies highlight indirect links between human replication origins and gene regulation. Proc Natl Acad Sci U S A 105:15837–15842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cayrou C, Coulombe P, Vigneron A, Stanojcic S, Ganier O, Peiffer I, Rivals E, Puy A, Laurent-Chabalier S, Desprat R, Mechali M (2011) Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. GenomeRes 21:1438–1449

    CAS  Google Scholar 

  • Cayrou C, Coulombe P, Puy A, Rialle S, Kaplan N, Segal E, Mechali M (2012) New insights into replication origin characteristics in metazoans. Cell Cycle 11:658–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Kelly TJ (1989) Transcriptional activator nuclear factor I stimulates the replication of SV40 minichromosomes in vivo and in vitro. Cell 59:541–551

    Article  CAS  PubMed  Google Scholar 

  • Cheng LZ, Workman JL, Kingston RE, Kelly TJ (1992) Regulation of DNA replication in vitro by the transcriptional activation domain of GAL4-VP16. Proc Natl Acad SciUSA 89:589–593

    Article  CAS  Google Scholar 

  • Chuang RY, Kelly TJ (1999) The fission yeast homologue of Orc4p binds to replication origin DNA via multiple AT-hooks. Proc Natl Acad Sci U S A 96:2656–2661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coleman KE, Grant GD, Haggerty RA, Brantley K, Shibata E, Workman BD, Dutta A, Varma D, Purvis JE, Cook JG (2015) Sequential replication-coupled destruction at G1/S ensures genome stability. GenesDev 29:1734–1746

    Article  CAS  Google Scholar 

  • Corona DF, Tamkun JW (2004) Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim Biophys Acta 1677:113–119

    Article  CAS  PubMed  Google Scholar 

  • Cortez D, Glick G, Elledge SJ (2004) Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci USA 101:10078–10083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai J, Chuang RY, Kelly TJ (2005) DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci U S A 102:337–342

    Article  CAS  PubMed  Google Scholar 

  • Danis E, Brodolin K, Menut S, Maiorano D, Girard-Reydet C, Mechali M (2004) Specification of a DNA replication origin by a transcription complex. Nat Cell Biol 6:721–730

    Article  CAS  PubMed  Google Scholar 

  • Das SP, Borrman T, Liu VW, Yang SC, Bechhoefer J, Rhind N (2015) Replication timing is regulated by the number of MCMs loaded at origins. Genome Res 25:1886–1892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Koning L, Corpet A, Haber JE, Almouzni G (2007) Histone chaperones: an escort network regulating histone traffic. Nat Struct Mol Biol 14:997–1007

    Article  PubMed  CAS  Google Scholar 

  • Dellino GI, Cittaro D, Piccioni R, Luzi L, Banfi S, Segalla S, Cesaroni M, Mendoza-Maldonado R, Giacca M, Pelicci PG (2013) Genome-wide mapping of human DNA-replication origins: levels of transcription at ORC1 sites regulate origin selection and replication timing. Genome Res 23:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dirscherl SS, Krebs JE (2004) Functional diversity of ISWI complexes. Biochem Cell Biol 82:482–489

    Article  CAS  PubMed  Google Scholar 

  • Dominguez-Sola D, Ying CY, Grandori C, Ruggiero L, Chen B, Li M, Galloway DA, Gu W, Gautier J, Dalla-Favera R (2007) Non-transcriptional control of DNA replication by c-Myc. Nature 448:445–451

    Article  CAS  PubMed  Google Scholar 

  • Du YC, Stillman B (2002) Yph1p, an ORC-interacting protein: potential links between cell proliferation control, DNA replication, and ribosome biogenesis. Cell 109:835–848

    Article  CAS  PubMed  Google Scholar 

  • Eberharter A, Becker PB (2004) ATP-dependent nucleosome remodelling: factors and functions. J Cell Sci 117:3707–3711

    Article  CAS  PubMed  Google Scholar 

  • Edwards MC, Tutter AV, Cvetic C, Gilbert CH, Prokhorova TA, Walter JC (2002) MCM2-7 complexes bind chromatin in a distributed pattern surrounding the origin recognition complex in Xenopus egg extracts. J Biol Chem 277:33049–33057

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Vlassis A, Roques C, Lalonde ME, Gonzalez-Aguilera C, Lambert JP, Lee SB, Zhao X, Alabert C, Johansen JV, Paquet E, Yang XJ, Gingras AC, Cote J, Groth A (2016) BRPF3-HBO1 regulates replication origin activation and histone H3K14 acetylation. EMBO J 35:176–192

    Article  CAS  PubMed  Google Scholar 

  • Flanagan JF, Peterson CL (1999) A role for the yeast SWI/SNF complex in DNA replication. Nucleic Acids Res 27:2022–2028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita M (2006) Cdt1 revisited: complex and tight regulation during the cell cycle and consequences of deregulation in mammalian cells. Cell Div 1:22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gambus A, Jones RC, Sanchez-Diaz A, Kanemaki M, van Deursen F, Edmondson RD, Labib K (2006) GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol 8:358–366

    Article  CAS  PubMed  Google Scholar 

  • Ge XQ, Jackson DA, Blow JJ (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. GenesDev 21:3331–3341

    Article  CAS  Google Scholar 

  • Georgiakaki M, Chabbert-Buffet N, Dasen B, Meduri G, Wenk S, Rajhi L, Amazit L, Chauchereau A, Burger CW, Blok LJ, Milgrom E, Lombes M, Guiochon-Mantel A, Loosfelt H (2006) Ligand-controlled interaction of histone acetyltransferase binding to ORC-1 (HBO1) with the N-terminal transactivating domain of progesterone receptor induces steroid receptor coactivator 1-dependent coactivation of transcription. Mol Endocrinol 20:2122–2140

    Article  CAS  PubMed  Google Scholar 

  • Gratenstein K, Heggestad AD, Fortun J, Notterpek L, Pestov DG, Fletcher BS (2005) The WD-repeat protein GRWD1: potential roles in myeloid differentiation and ribosome biogenesis. Genomics 85:762–773

    Article  CAS  PubMed  Google Scholar 

  • Grienenberger A, Miotto B, Sagnier T, Cavalli G, Schramke V, Geli V, Mariol MC, Berenger H, Graba Y, Pradel J (2002) The MYST domain acetyltransferase Chameau functions in epigenetic mechanisms of transcriptional repression. Curr Biol 12:762–766

    Article  CAS  PubMed  Google Scholar 

  • Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, Almouzni G (2007) Regulation of replication fork progression through histone supply and demand. Science 318:1928–1931

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez JL, Chandy M, Carrozza MJ, Workman JL (2007) Activation domains drive nucleosome eviction by SWI/SNF. EMBO J 26:730–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hakimi MA, Bochar DA, Schmiesing JA, Dong Y, Barak OG, Speicher DW, Yokomori K, Shiekhattar R (2002) A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418:994–998

    Article  CAS  PubMed  Google Scholar 

  • Hammond CM, Strømme CB, Huang H, Patel DJ, Groth A (2017) Histone chaperone networks shaping chromatin function. Nat Rev Mol Cell Biol 18:141–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han J, Li Q, McCullough L, Kettelkamp C, Formosa T, Zhang Z (2010) Ubiquitylation of FACT by the cullin-E3 ligase Rtt101 connects FACT to DNA replication. Genes Dev 24:1485–1490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl T, Boswell C, Orr-Weaver TL, Bosco G (2007) Developmentally regulated histone modifications in Drosophila follicle cells: initiation of gene amplification is associated with histone H3 and H4 hyperacetylation and H1 phosphorylation. Chromosoma 116:197–214

    Article  CAS  PubMed  Google Scholar 

  • Hartley PD, Madhani HD (2009) Mechanisms that specify promoter nucleosome location and identity. Cell 137:445–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi M, Katou Y, Itoh T, Tazumi A, Yamada Y, Takahashi T, Nakagawa T, Shirahige K, Masukata H (2007) Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO J 26:1327–1339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heller RC, Kang S, Lam WM, Chen S, Chan CS, Bell SP (2011) Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases. Cell 146:80–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horn PJ, Peterson CL (2002) Molecular biology. Chromatin higher order folding – wrapping up transcription. Science 297:1824–1827

    Article  CAS  PubMed  Google Scholar 

  • Hoshina S, Yura K, Teranishi H, Kiyasu N, Tominaga A, Kadoma H, Nakatsuka A, Kunichika T, Obuse C, Waga S (2013) Human origin recognition complex binds preferentially to G-quadruplex-preferable RNA and single-stranded DNA. J Biol Chem 288:30161–30171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu YF, Hao ZL, Li R (1999) Chromatin remodeling and activation of chromosomal DNA replication by an acidic transcriptional activation domain from BRCA1. GenesDev 13:637–642

    Article  CAS  Google Scholar 

  • Huang H, Stromme CB, Saredi G, Hodl M, Strandsby A, Gonzalez-Aguilera C, Chen S, Groth A, Patel DJ (2015) A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks. Nat Struct Mol Biol 22:618–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibarra A, Schwob E, Mendez J (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad SciA 105:8956–8961

    Article  CAS  Google Scholar 

  • Iizuka M, Stillman B (1999) Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J Biol Chem 274:23027–23034

    Article  CAS  PubMed  Google Scholar 

  • Iizuka M, Takahashi Y, Mizzen CA, Cook RG, Fujita M, Allis CD, Frierson HF Jr, Fukusato T, Smith MM (2009) Histone acetyltransferase Hbo1: catalytic activity, cellular abundance, and links to primary cancers. Gene 436:108–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iouk TL, Aitchison JD, Maguire S, Wozniak RW (2001) Rrb1p, a yeast nuclear WD-repeat protein involved in the regulation of ribosome biosynthesis. Mol Cell Biol 21:1260–1271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishii T, Shiomi Y, Takami T, Murakami Y, Ohnishi N, Nishitani H (2010) Proliferating cell nuclear antigen-dependent rapid recruitment of Cdt1 and CRL4Cdt2 at DNA-damaged sites after UV irradiation in HeLa cells. J Biol Chem 285:41993–42000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishimi Y, Komamura-Kohno Y, Arai K, Masai H (2001) Biochemical activities associated with mouse Mcm2 protein. J Biol Chem 276:42744–42752

    Article  CAS  PubMed  Google Scholar 

  • Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A, Almouzni G, Groth A (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37:736–743

    Article  CAS  PubMed  Google Scholar 

  • Jin J, Arias EE, Chen J, Harper JW, Walter JC (2006) A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol Cell 23:709–721

    Article  CAS  PubMed  Google Scholar 

  • Jin Q, Mao X, Li B, Guan S, Yao F, Jin F (2015) Overexpression of SMARCA5 correlates with cell proliferation and migration in breast cancer. Tumour Biol 36:1895–1902

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki Y, Kim HD, Kojima A, Seki T, Sugino A (2006) Reconstitution of Saccharomyces cerevisiae prereplicative complex assembly in vitro. Genes Cells 11:745–756

    Article  CAS  PubMed  Google Scholar 

  • Killian A, Le Meur N, Sesboue R, Bourguignon J, Bougeard G, Gautherot J, Bastard C, Frebourg T, Flaman JM (2004) Inactivation of the RRB1-Pescadillo pathway involved in ribosome biogenesis induces chromosomal instability. Oncogene 23:8597–8602

    Article  CAS  PubMed  Google Scholar 

  • Kueh AJ, Dixon MP, Voss AK, Thomas T (2011) HBO1 is required for H3K14 acetylation and normal transcriptional activity during embryonic development. Mol Cell Biol 31:845–860

    Article  CAS  PubMed  Google Scholar 

  • Kurat CF, Yeeles JT, Patel H, Early A, Diffley JF (2017) Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol Cell 65:117–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lafon A, Chang CS, Scott EM, Jacobson SJ, Pillus L (2007) MYST opportunities for growth control: yeast genes illuminate human cancer gene functions. Oncogene 26:5373–5384

    Article  CAS  PubMed  Google Scholar 

  • Li R, Botchan MR (1994) Acidic transcription factors alleviate nucleosome-mediated repression of DNA replication of bovine papillomavirus type 1. Proc Natl Acad Sci U S A 91:7051–7055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zhao Q, Liao R, Sun P, Wu X (2003) The SCF(Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J Biol Chem 278:30854–30858

    Article  CAS  PubMed  Google Scholar 

  • Lipford JR, Bell SP (2001) Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol Cell 7:21–30

    Article  CAS  PubMed  Google Scholar 

  • Liu E, Li X, Yan F, Zhao Q, Wu X (2004) Cyclin-dependent kinases phosphorylate human Cdt1 and induce its degradation. J Biol Chem 279:17283–17288

    Article  CAS  PubMed  Google Scholar 

  • Liu G, Chen X, Gao Y, Lewis T, Barthelemy J, Leffak M (2012) Altered replication in human cells promotes DMPK (CTG) (n) · (CAG)(n) repeat instability. Mol Cell Biol 32:1618–1632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacAlpine DM, Almouzni G (2013) Chromatin and DNA replication. Cold Spring Harb Perspect Biol 5:a010207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • MacCallum DE, Losada A, Kobayashi R, Hirano T (2002) ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol Biol Cell 13:25–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin MM, Ryan M, Kim R, Zakas AL, Fu H, Lin CM, Reinhold WC, Davis SR, Bilke S, Liu H, Doroshow JH, Reimers MA, Valenzuela MS, Pommier Y, Meltzer PS, Aladjem MI (2011) Genome-wide depletion of replication initiation events in highly transcribed regions. Genome Res 21:1822–1832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGarry TJ, Kirschner MW (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93:1043–1053

    Article  CAS  PubMed  Google Scholar 

  • Miotto B, Struhl K (2006) Differential gene regulation by selective association of transcriptional coactivators and bZIP DNA-binding domains. Mol Cell Biol 26:5969–5982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miotto B, Struhl K (2008) HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. GenesDev 22:2633–2638

    Article  CAS  Google Scholar 

  • Miotto B, Struhl K (2010) HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol Cell 37:57–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miotto B, Sagnier T, Berenger H, Bohmann D, Pradel J, Graba Y (2006) Chameau HAT and DRpd3 HDAC function as antagonistic cofactors of JNK/AP-1-dependent transcription during Drosophila metamorphosis. Genes Dev 20:101–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miotto B, Ji Z, Struhl K (2016) Selectivity of ORC binding sites and the relation to replication timing, fragile sites, and deletions in cancers. Proc Natl Acad Sci U S A 113:E4810–E4819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris SA, Baek S, Sung MH, John S, Wiench M, Johnson TA, Schiltz RL, Hager GL (2014) Overlapping chromatin-remodeling systems collaborate genome wide at dynamic chromatin transitions. Nat Struct Mol Biol 21:73–81

    Article  CAS  PubMed  Google Scholar 

  • Nishitani H, Taraviras S, Lygerou Z, Nishimoto T (2001) The human licensing factor for DNA replication Cdt1 accumulates in G1 and is destabilized after initiation of S-phase. J Biol Chem 276:44905–44911

    Article  CAS  PubMed  Google Scholar 

  • Nishitani H, Sugimoto N, Roukos V, Nakanishi Y, Saijo M, Obuse C, Tsurimoto T, Nakayama KI, Nakayama K, Fujita M, Lygerou Z, Nishimoto T (2006) Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J 25:1126–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orr SJ, Gaymes T, Ladon D, Chronis C, Czepulkowski B, Wang R, Mufti GJ, Marcotte EM, Thomas NS (2010) Reducing MCM levels in human primary T cells during the G(0)-->G(1) transition causes genomic instability during the first cell cycle. Oncogene 29:3803–3814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petryk N, Kahli M, d’Aubenton-Carafa Y, Jaszczyszyn Y, Shen Y, Silvain M, Thermes C, Chen CL, Hyrien O (2016) Replication landscape of the human genome. NatCommun 7:10208

    CAS  Google Scholar 

  • Pruitt SC, Bailey KJ, Freeland A (2007) Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells 25:3121–3132

    Article  CAS  PubMed  Google Scholar 

  • Randell JC, Bowers JL, Rodriguez HK, Bell SP (2006) Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol Cell 21:29–39

    Article  CAS  PubMed  Google Scholar 

  • Rao H, Marahrens Y, Stillman B (1994) Functional conservation of multiple elements in yeast chromosomal replicators. Mol Cell Biol 14:7643–7651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid JL, Iyer VR, Brown PO, Struhl K (2000) Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase. Mol Cell 6:1297–1307

    Article  CAS  PubMed  Google Scholar 

  • Richet N, Liu D, Legrand P, Velours C, Corpet A, Gaubert A, Bakail M, Moal-Raisin G, Guerois R, Compper C, Besle A, Guichard B, Almouzni G, Ochsenbein F (2015) Structural insight into how the human helicase subunit MCM2 may act as a histone chaperone together with ASF1 at the replication fork. Nucleic Acids Res 43:1905–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson PJ, An W, Routh A, Martino F, Chapman L, Roeder RG, Rhodes D (2008) 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J Mol Biol 381:816–825

    Article  CAS  PubMed  Google Scholar 

  • Schaarschmidt D, Baltin J, Stehle IM, Lipps HJ, Knippers R (2004) An episomal mammalian replicon: sequence-independent binding of the origin recognition complex. EMBO J 23:191–201

    Article  CAS  PubMed  Google Scholar 

  • Schaper S, Fromont-Racine M, Linder P, de la Cruz J, Namane A, Yaniv M (2001) A yeast homolog of chromatin assembly factor 1 is involved in early ribosome assembly. Curr Biol 11:1885–1890

    Article  CAS  PubMed  Google Scholar 

  • Segurado M, de Luis A, Antequera F (2003) Genome-wide distribution of DNA replication origins at A+T-rich islands in Schizosaccharomyces pombe. EMBO Rep 4:1048–1053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seki T, Diffley JF (2000) Stepwise assembly of initiation proteins at budding yeast replication origins in vitro. Proc Natl Acad Sci U S A 97:14115–14120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sequeira-Mendes J, Diaz-Uriarte R, Apedaile A, Huntley D, Brockdorff N, Gomez M (2009) Transcription initiation activity sets replication origin efficiency in mammalian cells. PLoS Genet 5:e1000446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen Z, Sathyan KM, Geng Y, Zheng R, Chakraborty A, Freeman B, Wang F, Prasanth KV, Prasanth SG (2010) A WD-repeat protein stabilizes ORC binding to chromatin. Mol Cell 40:99–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shima N, Alcaraz A, Liachko I, Buske TR, Andrews CA, Munroe RJ, Hartford SA, Tye BK, Schimenti JC (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat Genet 39:93–98

    Article  CAS  PubMed  Google Scholar 

  • Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847

    Article  CAS  PubMed  Google Scholar 

  • Springer C, Krappmann S, Kunzler M, Zmasek C, Braus GH (1997) Regulation of the yeast HIS7 gene by the global transcription factor Abf1p. Mol Gen Genet 256:136–146

    Article  CAS  PubMed  Google Scholar 

  • Stedman W, Deng Z, Lu F, Lieberman PM (2004) ORC, MCM, and histone hyperacetylation at the Kaposi’s sarcoma-associated herpesvirus latent replication origin. J Virol 78:12566–12575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stinchcomb DT, Struhl K, Davis RW (1979) Isolation and characterisation of a yeast chromosomal replicator. Nature 282:39–43

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto N, Tatsumi Y, Tsurumi T, Matsukage A, Kiyono T, Nishitani H, Fujita M (2004) Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J Biol Chem 279:19691–19697

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto N, Kitabayashi I, Osano S, Tatsumi Y, Yugawa T, Narisawa-Saito M, Matsukage A, Kiyono T, Fujita M (2008) Identification of novel human Cdt1-binding proteins by a proteomics approach: proteolytic regulation by APC/CCdh1. Mol Biol Cell 19:1007–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugimoto N, Yoshida K, Tatsumi Y, Yugawa T, Narisawa-Saito M, Waga S, Kiyono T, Fujita M (2009) Redundant and differential regulation of multiple licensing factors ensures prevention of re-replication in normal human cells. J Cell Sci 122:1184–1191

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto N, Yugawa T, Iizuka M, Kiyono T, Fujita M (2011) Chromatin remodeler sucrose nonfermenting 2 homolog (SNF2H) is recruited onto DNA replication origins through interaction with Cdc10 protein-dependent transcript 1 (Cdt1) and promotes pre-replication complex formation. J Biol Chem 286:39200–39210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugimoto N, Maehara K, Yoshida K, Yasukouchi S, Osano S, Watanabe S, Aizawa M, Yugawa T, Kiyono T, Kurumizaka H, Ohkawa Y, Fujita M (2015) Cdt1-binding protein GRWD1 is a novel histone-binding protein that facilitates MCM loading through its influence on chromatin architecture. Nucleic Acids Res 43:5898–5911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tada S, Li A, Maiorano D, Mechali M, Blow JJ (2001) Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat Cell Biol 3:107–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeda DY, Parvin JD, Dutta A (2005) Degradation of Cdt1 during S phase is Skp2-independent and is required for efficient progression of mammalian cells through S phase. J Biol Chem 280:23416–23423

    Article  CAS  PubMed  Google Scholar 

  • Tan BC, Chien CT, Hirose S, Lee SC (2006) Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication. EMBO J 25:3975–3985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka S, Diffley JF (2002) Interdependent nuclear accumulation of budding yeast Cdt1 and Mcm2-7 during G1 phase. Nat Cell Biol 4:198–207

    Article  CAS  PubMed  Google Scholar 

  • Tsao CC, Geisen C, Abraham RT (2004) Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. EMBO J 23:4660–4669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tse C, Fletcher TM, Hansen JC (1998) Enhanced transcription factor access to arrays of histone H3/H4 tetramer. DNA complexes in vitro: implications for replication and transcription. Proc Natl Acad Sci U S A 95:12169–12173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsukiyama T (2002) The in vivo functions of ATP-dependent chromatin-remodelling factors. Nat Rev Mol CellBiol 3:422–429

    Article  CAS  Google Scholar 

  • Valenzuela MS, Chen Y, Davis S, Yang F, Walker RL, Bilke S, Lueders J, Martin MM, Aladjem MI, Massion PP, Meltzer PS (2011) Preferential localization of human origins of DNA replication at the 5′-ends of expressed genes and at evolutionarily conserved DNA sequences. PLoS One 6:e17308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valton AL, Hassan-Zadeh V, Lema I, Boggetto N, Alberti P, Saintome C, Riou JF, Prioleau MN (2014) G4 motifs affect origin positioning and efficiency in two vertebrate replicators. EMBOJ 33:732–746

    Article  CAS  Google Scholar 

  • VanDemark AP, Blanksma M, Ferris E, Heroux A, Hill CP, Formosa T (2006) The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol Cell 22:363–374

    Article  CAS  PubMed  Google Scholar 

  • Varga-Weisz P (2001) ATP-dependent chromatin remodeling factors: nucleosome shufflers with many missions. Oncogene 20:3076–3085

    Article  CAS  PubMed  Google Scholar 

  • Vashee S, Cvetic C, Lu W, Simancek P, Kelly TJ, Walter JC (2003) Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev 17:1894–1908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaziri C, Saxena S, Jeon Y, Lee C, Murata K, Machida Y, Wagle N, Hwang DS, Dutta A (2003) A p53-dependent checkpoint pathway prevents rereplication. Mol Cell 11:997–1008

    Article  CAS  PubMed  Google Scholar 

  • Venditti P, Costanzo G, Negri R, Camilloni G (1994) ABFI contributes to the chromatin organization of Saccharomyces cerevisiae ARS1 B-domain. Biochim Biophys Acta 1219:677–689

    Article  PubMed  Google Scholar 

  • Vincent JA, Kwong TJ, Tsukiyama T (2008) ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat Struct Mol Biol 15:477–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vodermaier HC (2004) APC/C and SCF: controlling each other and the cell cycle. Curr Biol 14:R787–R796

    Article  CAS  PubMed  Google Scholar 

  • Wittmeyer J, Formosa T (1997) The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol Cell Biol 17:4178–4190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, Dutta A (2000) Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290:2309–2312

    Article  CAS  PubMed  Google Scholar 

  • Wong PG, Glozak MA, Cao TV, Vaziri C, Seto E, Alexandrow M (2010) Chromatin unfolding by Cdt1 regulates MCM loading via opposing functions of HBO1 and HDAC11-geminin. Cell Cycle 9:4351–4363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodward AM, Gohler T, Luciani MG, Oehlmann M, Ge X, Gartner A, Jackson DA, Blow JJ (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 173:673–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyrick JJ, Aparicio JG, Chen T, Barnett JD, Jennings EG, Young RA, Bell SP, Aparicio OM (2001) Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 294:2357–2360

    Article  CAS  PubMed  Google Scholar 

  • Yeeles JT, Deegan TD, Janska A, Early A, Diffley JF (2015) Regulated eukaryotic DNA replication origin firing with purified proteins. Nature 519:431–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yompakdee C, Huberman JA (2004) Enforcement of late replication origin firing by clusters of short G-rich DNA sequences. J Biol Chem 279:42337–42344

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Bacal J, Desmarais D, Padioleau I, Tsaponina O, Chabes A, Pantesco V, Dubois E, Parrinello H, Skrzypczak M, Ginalski K, Lengronne A, Pasero P (2014) The histone deacetylases sir2 and rpd3 act on ribosomal DNA to control the replication program in budding yeast. MolCell 54:691–697

    CAS  Google Scholar 

  • You Z, Masai H (2008) Cdt1 forms a complex with the minichromosome maintenance protein (MCM) and activates its helicase activity. J Biol Chem 283:24469–24477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Chau CM, Deng Z, Shiekhattar R, Spindler MP, Schepers A, Lieberman PM (2005) Cell cycle regulation of chromatin at an origin of DNA replication. EMBO J 24:1406–1417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgment

We thank all members of our research group for the helpful discussion and critical reading of the manuscript. This work was supported in part by Grants to Sugimoto and Fujita from the Ministry of Education, Culture, Sports, Science and Technology of Japan (17080013, 21370084, 25291027, 26114713, 09J07233).

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The authors declare no conflicts of interest in relation to this article.

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Sugimoto, N., Fujita, M. (2017). Molecular Mechanism for Chromatin Regulation During MCM Loading in Mammalian Cells. In: Masai, H., Foiani, M. (eds) DNA Replication. Advances in Experimental Medicine and Biology, vol 1042. Springer, Singapore. https://doi.org/10.1007/978-981-10-6955-0_3

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