The E3 ligase RFWD3 stabilizes ORC in a p53-dependent manner

References

• Bell SP, Dutta A. DNA replication in eukaryotic cells. Annu Rev Biochem. 2002;71:333–374.
   PubMed Web of Science ®Google Scholar
• Arias EE, Walter JC. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 2007;21:497–518.
   PubMed Web of Science ®Google Scholar
• Drury LS, Diffley JF. Factors affecting the diversity of DNA replication licensing control in eukaryotes. Curr Biol. 2009;19:530–535.
   PubMed Web of Science ®Google Scholar
• Truong LN, Wu X. Prevention of DNA re-replication in eukaryotic cells. J Mol Cell Biol. 2011;3:13–22.
   PubMed Web of Science ®Google Scholar
• Shen Z, Sathyan KM, Geng Y, et al. A WD-repeat protein stabilizes ORC binding to chromatin. Mol Cell. 2010;40:99–111. doi:10.1016/j.molcel.2010.09.021
   Google Scholar
• Shen Z, Chakraborty A, Jain A, et al. Dynamic association of ORCA with prereplicative complex components regulates DNA replication initiation. Mol Cell Biol. 2012;32:3107–3120.
   PubMed Web of Science ®Google Scholar
• Gambus A, Jones RC, Sanchez-Diaz A, et al. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat Cell Biol. 2006;8:358–366.
   PubMed Web of Science ®Google Scholar
• Moyer SE, Lewis PW, Botchan MR. Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc Natl Acad Sci U S A. 2006;103:10236–10241.
   PubMed Web of Science ®Google Scholar
• Ge XQ, Jackson DA, Blow JJ. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 2007;21:3331–3341.
   PubMed Web of Science ®Google Scholar
• Ibarra A, Schwob E, Mendez J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A. 2008;105:8956–8961.
   PubMed Web of Science ®Google Scholar
• Lunn CL, Chrivia JC, Baldassare JJ. Activation of Cdk2/Cyclin E complexes is dependent on the origin of replication licensing factor Cdc6 in mammalian cells. Cell Cycle. 2010;9:4533–4541.
   PubMed Web of Science ®Google Scholar
• Machida YJ, Teer JK, Dutta A. Acute reduction of an origin recognition complex (ORC) subunit in human cells reveals a requirement of ORC for Cdk2 activation. J Biol Chem. 2005;280:27624–27630.
   PubMed Web of Science ®Google Scholar
• Nevis KR, Cordeiro-Stone M, Cook JG. Origin licensing and p53 status regulate Cdk2 activity during G1. Cell Cycle. 2009;8:1952–1963.
   PubMed Web of Science ®Google Scholar
• Ekholm-Reed S, Méndez J, Tedesco D, et al. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J Cell Biol. 2004;165:789–800.
   PubMed Web of Science ®Google Scholar
• Macheret M, Halazonetis TD. Intragenic origins due to short G1 phases underlie oncogene-induced DNA replication stress. Nature. 2018;555:112–116.
   PubMed Web of Science ®Google Scholar
• Dominguez-Sola D, Ying CY, Grandori C, et al. Non-transcriptional control of DNA replication by c-Myc. Nature. 2007;448:445–451.
   PubMed Web of Science ®Google Scholar
• Hernandez-Carralero E, Cabrera E, Alonso-de Vega I, et al. Control of DNA replication initiation by ubiquitin. Cells. 2018;7. DOI:10.3390/cells7100146
   PubMed Web of Science ®Google Scholar
• Parker MW, Botchan MR, Berger JM. Mechanisms and regulation of DNA replication initiation in eukaryotes. Crit Rev Biochem Mol Biol. 2017;52:107–144.
   PubMed Web of Science ®Google Scholar
• Diffley FX, Cocker JH, Dowell SJ, et al. Two steps in the assembly of complexes at yeast replication origins in vivo. Cell. 1994;70:303–316.
   Google Scholar
• Liang. C, Stillman B. Genes and development persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev. 1997;11:3375–3386.
   PubMed Web of Science ®Google Scholar
• Nguyen VQ, Co. C, Li JJ. Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature. 2001;411:1068–1073.
   PubMed Web of Science ®Google Scholar
• Araki M, Wharton RP, Tang Z, et al. Degradation of origin recognition complex large subunit by the anaphase-promoting complex in Drosophila. Embo J. 2003;22:6115–6126.
   PubMed Web of Science ®Google Scholar
• Li CJ, DePamphilis ML. Mammalian Orc1 protein is selectively released from chromatin and ubiquitinated during the S-to-M transition in the cell division cycle. Mol Cell Biol. 2002;22:105–116.
   PubMed Web of Science ®Google Scholar
• Li CJ, Vassilev A, DePamphilis ML. Role for Cdk1 (Cdc2)/cyclin A in preventing the mammalian origin recognition complex’s largest subunit (Orc1) from binding to chromatin during mitosis. Mol Cell Biol. 2004;24:5875–5886.
   PubMed Web of Science ®Google Scholar
• Hiraga SI, Ly T, Garzón J, et al. Human RIF 1 and protein phosphatase 1 stimulate DNA replication origin licensing but suppress origin activation. EMBO Rep. 2017;18:403–419.
   PubMed Web of Science ®Google Scholar
• Tatsumi Y, Ohta S, Kimura H, et al. The ORC1 cycle in human cells: I. cell cycle-regulated oscillation of human ORC1. J Biol Chem. 2003;278:41528–41534.
   PubMed Web of Science ®Google Scholar
• Méndez J, Zou-Yang XH, Kim S-Y, et al. Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol Cell. 2002;9:481–491.
   PubMed Web of Science ®Google Scholar
• Shen Z, Prasanth SG. Orc2 protects ORCA from ubiquitin-mediated degradation. Cell Cycle. 2012;11:3578–3589.
   PubMed Web of Science ®Google Scholar
• Coulombe P, Nassar J, Peiffer I, et al. The ORC ubiquitin ligase OBI1 promotes DNA replication origin firing. Nat Commun. 2019;10:2426.
   PubMed Web of Science ®Google Scholar
• Matsuoka S, Ballif BA, Smogorzewska A, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science. 2007;316:1160–1166.
   PubMed Web of Science ®Google Scholar
• Mu JJ, Wang Y, Luo H, et al. A proteomic analysis of ataxia telangiectasia-mutated (ATM)/ATM-Rad3-related (ATR) substrates identifies the ubiquitin-proteasome system as a regulator for DNA damage checkpoints. J Biol Chem. 2007;282:17330–17334.
   PubMed Web of Science ®Google Scholar
• Fu X, Yucer N, Liu S, et al. RFWD3-Mdm2 ubiquitin ligase complex positively regulates p53 stability in response to DNA damage. Proc Natl Acad Sci U S A. 2010;107:4579–4584.
   PubMed Web of Science ®Google Scholar
• Gong Z, Chen J. E3 ligase RFWD3 participates in replication checkpoint control. J Biol Chem. 2011;286:22308–22313.
   PubMed Web of Science ®Google Scholar
• Inano S, Sato K, Katsuki Y, et al. RFWD3-mediated ubiquitination promotes timely removal of both RPA and RAD51 from DNA damage sites to facilitate homologous recombination. Mol Cell. 2017;66:622–634 e628.
   PubMed Web of Science ®Google Scholar
• Elia AE, Wang D, Willis N, et al. RFWD3-dependent ubiquitination of RPA regulates repair at stalled replication forks. Mol Cell. 2015;60:280–293.
   PubMed Web of Science ®Google Scholar
• Feeney L, Muñoz IM, Lachaud C, et al. RPA-mediated recruitment of the E3 ligase RFWD3 is vital for interstrand crosslink repair and human health. Mol Cell. 2017;66:610–62Re614.
   PubMed Web of Science ®Google Scholar
• Knies K, Inano S, Ramírez MJ, et al. Biallelic mutations in the ubiquitin ligase RFWD3 cause Fanconi anemia. J Clin Invest. 2017;127:3013–3027.
   PubMed Web of Science ®Google Scholar
• Lin Y-C, Wang Y, Hsu R, et al. PCNA-mediated stabilization of E3 ligase RFWD3 at the replication fork is essential for DNA replication. Proc Natl Acad Sci U S A. 2018;115:13282–13287. doi:10.1073/pnas.1814521115
   Google Scholar
• Giri S, Chakraborty A, Sathyan KM, et al. Orc5 induces large-scale chromatin decondensation in a GCN5-dependent manner. J Cell Sci. 2016;129:417–429.
   PubMed Web of Science ®Google Scholar
• Hsu RYC, Lin Y-C, Redon C, et al. ORCA/LRWD1 regulates homologous recombination at ALT-telomeres by modulating heterochromatin organization. iScience. 2020;23:101038.
   PubMed Web of Science ®Google Scholar
• Prasanth SG, Prasanth KV, Siddiqui K, et al. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. Embo J. 2004;23:2651–2663.
   PubMed Web of Science ®Google Scholar
• Janicki SM, Tsukamoto T, Salghetti SE, et al. From silencing to gene expression: real-time analysis in single cells. Cell. 2004;116:683–698.
   PubMed Web of Science ®Google Scholar
• El-Deiry WS, Tokino T, Velculescu VE, et al. WAF1, a potential mediator of p53 tumor suppression. Cell. 1993;75: 817–825.
   Google Scholar
• Harper JW, Adami GR, Wei N, et al. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 1993;75:805–816.
   PubMed Web of Science ®Google Scholar
• Liu S, Chu J, Yucer N, et al. RING finger and WD repeat domain 3 (RFWD3) associates with replication protein A (RPA) and facilitates RPA-mediated DNA damage response. J Biol Chem. 2011;286:22314–22322.
   PubMed Web of Science ®Google Scholar
• Akimov V, Barrio-Hernandez I, Hansen SVF, et al. UbiSite approach for comprehensive mapping of lysine and N-terminal ubiquitination sites. Nat Struct Mol Biol. 2018;25:631–640.
   PubMed Web of Science ®Google Scholar
• Petropoulos M, Champeris Tsaniras S, Taraviras S, et al. Replication licensing aberrations, replication stress, and genomic instability. Trends Biochem Sci. 2019;44:752–764.
   PubMed Web of Science ®Google Scholar
• Lee KY, Bang SW, Yoon SW, et al. Phosphorylation of ORC2 protein dissociates origin recognition complex from chromatin and replication origins. J Biol Chem. 2012;287:11891–11898.
   PubMed Web of Science ®Google Scholar