Claspin is Required for Growth Recovery from Serum Starvation through Regulating the PI3K-PDK1-mTOR Pathway in Mammalian Cells

REFERENCES

• Branzei D, Foiani M. The checkpoint response to replication stress. DNA Repair. 2009;8:1038–1046. doi:10.1016/j.dnarep.2009.04.014.
   PubMed Web of Science ®Google Scholar
• Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol. 2001;21:4129–4139. doi:10.1128/MCB.21.13.4129-4139.2001.
   PubMed Web of Science ®Google Scholar
• Lindsey-Boltz LA, Serçin Ö, Choi JH, Sancar A. Reconstitution of human claspin-mediated phosphorylation of Chk1 by the ATR (ataxia telangiectasia-mutated and Rad3-related) checkpoint kinase. J Biol Chem. 2009;284:33107–33114. doi:10.1074/jbc.M109.064485.
   PubMed Web of Science ®Google Scholar
• Kumagai A, Dunphy WG. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol Cell. 2000;6:839–849. doi:10.1016/S1097-2765(05)00092-4.
   PubMed Web of Science ®Google Scholar
• Tanaka K, Russell P. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat Cell Biol. 2001;3:966–972. doi:10.1038/ncb1101-966.
   PubMed Web of Science ®Google Scholar
• Alcasabas AA, Osborn AJ, Bachant J, Hu F, Werler PJH, Bousset K, Furuya K, Diffley JF, Carr AM, Elledge SJ. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol. 2001;3:958–965. doi:10.1038/ncb1101-958.
   PubMed Web of Science ®Google Scholar
• Christiano C, Chini S, Chen J. Human claspin is required for replication checkpoint control. J Biol Chem. 2003;278:30057–30062. doi:10.1074/jbc.M301136200.
   PubMed Web of Science ®Google Scholar
• Osborn AJ, Elledge SJ. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 2003;17:1755–1767. doi:10.1101/gad.1098303.
   PubMed Web of Science ®Google Scholar
• Hae YY, Jeong SY, Dunphy WG. Site-specific phosphorylation of a checkpoint mediator protein controls its responses to different DNA structures. Genes Dev. 2006;20:772–783. doi:10.1101/gad.1398806.
   PubMed Web of Science ®Google Scholar
• Kim JM, Kakusho N, Yamada M, Kanoh Y, Takemoto N, Masai H. Cdc7 kinase mediates Claspin phosphorylation in DNA replication checkpoint. Oncogene. 2008;29;27(24):3475–3482. doi:10.1038/sj.onc.1210994.
   Web of Science ®Google Scholar
• Kumagai A, Dunphy WG. Repeated phosphopeptide motifts in claspin mediate the regulated binding of Chk1. Nat Cell Biol. 2003;5:161–165. doi:10.1038/ncb921.
   PubMed Web of Science ®Google Scholar
• Chini CCS, Chen J. Repeated phosphopeptide motifs in human claspin are phosphorylated by Chk1 and mediate claspin function. J Biol Chem. 2006;281:33276–33282. doi:10.1074/jbc.M604373200.
   PubMed Web of Science ®Google Scholar
• Meng Z, Capalbo L, Glover DM, Dunphy WG. Role for casein kinase 1 in the phosphorylation of claspin on critical residues necessary for the activation of Chk1. Mol Biol Cell. 2011;22:2834–2847. doi:10.1091/mbc.e11-01-0048.
   PubMed Web of Science ®Google Scholar
• Yang CC, Kato H, Shindo M, Masai H. Cdc7 activates replication checkpoint by phosphorylating the chk1 binding domain of claspin in human cells. Elife. 2019;8:e50796. doi:10.7554/eLife.50796.
   PubMed Web of Science ®Google Scholar
• Szyjka SJ, Viggiani CJ, Aparicio OM. Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol Cell. 2005;19:691–697. doi:10.1016/j.molcel.2005.06.037.
   PubMed Web of Science ®Google Scholar
• Tourrière H, Versini G, Cordón-Preciado V, Alabert C, Pasero P. Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell. 2005;19:699–706. doi:10.1016/j.molcel.2005.07.028.
   PubMed Web of Science ®Google Scholar
• Yeeles JTP, Janska A, Early A, Diffley JFX. How the eukaryotic replisome achieves rapid and efficient DNA replication. Mol Cell. 2017;65:105–116. doi:10.1016/j.molcel.2016.11.017.
   PubMed Web of Science ®Google Scholar
• Petermann E, Helleday T, Caldecott KW. Claspin promotes normal replication fork rates in human cells. Mol Biol Cell. 2008;19:2373–2378. doi:10.1091/mbc.e07-10-1035.
   PubMed Web of Science ®Google Scholar
• Yang CC, Suzuki M, Yamakawa S, Uno S, Ishii A, Yamazaki S, Fukatsu R, Fujisawa R, Sakimura K, Tsurimoto T, et al. Claspin recruits Cdc7 kinase for initiation of DNA replication in human cells. Nat Commun. 2016;7:12135. doi:10.1038/ncomms12135.
   PubMed Web of Science ®Google Scholar
• Masai H, Yang CC, Matsumoto S. Mrc1/Claspin: a new role for regulation of origin firing. Curr Genet. 2017;63(5):813–818. doi:10.1007/s00294-017-0690-y.
   PubMed Web of Science ®Google Scholar
• Hsiao, HW., Yang, CC, Masai, H. Roles of Claspin in regulation of DNA replication, replication stress responses and oncogenesis in human cells. Genome Instab Dis. 2021;2:263–280. doi:10.1007/s42764-021-00049-8.
   Google Scholar
• Uno S, Masai H. Efficient expression and purification of human replication fork-stabilizing factor, Claspin, from mammalian cells: DNA-binding activity and novel protein interactions. Genes Cells. 2011;16(8):842–856. doi:10.1111/j.1365-2443.2011.01535.x.
   PubMed Web of Science ®Google Scholar
• Hayano M, Kanoh Y, Matsumoto S, Masai H. Mrc1 marks early-firing origins and coordinates timing and efficiency of initiation in fission yeast. Mol Cell Biol. 2011;31(12):2380–91. doi:10.1128/MCB.01239-10.
   PubMed Web of Science ®Google Scholar
• Duch A, Felipe-Abrio I, Barroso S, Yaakov G, García-Rubio M, Aguilera A, de Nadal E, Posas F. Coordinated control of replication and transcription by a SAPK protects genomic integrity. Nature. 2013;493:116–121. doi:10.1038/nature11675.
   PubMed Web of Science ®Google Scholar
• Duch A, Canal B, Barroso SI, García-Rubio M, Seisenbacher G, Aguilera A, de Nadal E, Posas F. Multiple signaling kinases target Mrc1 to prevent genomic instability triggered by transcription-replication conflicts. Nat Commun. 2018;9:379. doi:10.1038/s41467-017-02756-x.
   PubMed Web of Science ®Google Scholar
• de Nadal E, Posas F. Osmostress-induced gene expression – a model to understand how stress-activated protein kinases (SAPKs) regulate transcription. FEBS J. 2015;282: 3275–3285. doi:10.1111/febs.13323.
   PubMed Web of Science ®Google Scholar
• Cabrera E, Hernández-Pérez S, Koundrioukoff S, Debatisse M, Kim D, Smolka MB, Freire R, Gillespie DA. PERK inhibits DNA replication during the unfolded protein response via Claspin and Chk1. Oncogene. 2017;36:678–686. doi:10.1038/onc.2016.239.
   PubMed Web of Science ®Google Scholar
• McDonald NQ, Hendrickson WA. A structural superfamily of growth factors containing a cystine knot motif. Cell. 1993;73: 421–424. doi:10.1016/0092-8674(93)90127-C.
   PubMed Web of Science ®Google Scholar
• Plotnikov AN, Hubbard SR, Schlessinger J, Mohammadi M. Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity. Cell. 2000;101:413–424. doi:10.1016/S0092-8674(00)80851-X.
   PubMed Web of Science ®Google Scholar
• Chang F, Lee JT, Navolanic PM, Steelman LS, Shelton JG, Blalock WL, Franklin RA, McCubrey JA. Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: a target for cancer chemotherapy. Leukemia. 2003;17: 590–603. doi:10.1038/sj.leu.2402824.
   PubMed Web of Science ®Google Scholar
• Toker A, Cantley LC. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature. 1997;387: 673–676. doi:10.1038/42648.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck B, Leevers SJ, Panayotou G, Waterfield MD, Waterfield MD. Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem Sci. 1997;22: 267–272. doi:10.1016/S0968-0004(97)01061-X.
   PubMed Web of Science ®Google Scholar
• Leevers SJ, Vanhaesebroeck B, Waterfield MD. Signalling through phosphoinositide 3-kinases: the lipids take centre stage. Curr Opin Cell Biol. 1999;11(2), 219–225. doi:10.1016/s0955-0674(99)80029-5.
   PubMed Web of Science ®Google Scholar
• Williams MR, Arthur JSC, Balendran A, Van der Kaay J, Poli V, Cohen P, Alessi DR. The role of 3-phosphoinositide-dependent protein kinase 1 in activating AGC kinases defined in embryonic stem cells. Curr Biol. 2000;10:439–448. doi:10.1016/S0960-9822(00)00441-3.
   PubMed Web of Science ®Google Scholar
• Toker A, Newton AC. Cellular signaling: pivoting around PDK-1. Cell. 2000;103: 185–188. doi:10.1016/S0092-8674(00)00110-0.
   PubMed Web of Science ®Google Scholar
• Belham C, Shilan W, Avruch J. Intracellular signalling: PDK1 – a kinase at the hub of things. Curr Biol. 1999;9:R93–R96. doi:10.1016/S0960-9822(99)80058-X.
   PubMed Web of Science ®Google Scholar
• Ma Y, Vassetzky Y, Dokudovskaya S. mTORC1 pathway in DNA damage response. Biochim Biophys Acta - Mol Cell Res. 2018;1865:1293–1311. doi:10.1016/j.bbamcr.2018.06.011.
   PubMed Web of Science ®Google Scholar
• Navé BT, Ouwens DM, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J. 1999;344:427–431. doi:10.1042/bj3440427.
   PubMed Web of Science ®Google Scholar
• Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J. Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science. 2001;294:1942–1945. doi:10.1126/science.1066015.
   PubMed Web of Science ®Google Scholar
• Pullen N, Thomas G. The modular phosphorylation and activation of p70(s6k). FEBS Lett. 1997;410:78–82. doi:10.1016/S0014-5793(97)00323-2.
   PubMed Web of Science ®Google Scholar
• Dufner A, Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res. 1999;253:100–109. doi:10.1006/excr.1999.4683.
   PubMed Web of Science ®Google Scholar
• Jewell JL, Guan KL. Nutrient signaling to mTOR and cell growth. Trends Biochem Sci. 2013;38:233–242. doi:10.1016/j.tibs.2013.01.004.
   PubMed Web of Science ®Google Scholar
• Budanov AV., Karin M. p53 target genes Sestrin1 and Sestrin2 connect genotoxic stress and mTOR signaling. Cell. 2008;134:451–460. doi:10.1016/j.cell.2008.06.028.
   PubMed Web of Science ®Google Scholar
• Feng Z, Hu W, de Stanchina E, Teresky AK, Jin S, Lowe S, Levine AJ. The regulation of AMPK β1, TSC2, and PTEN expression by p53: stress, cell and tissue specificity, and the role of these gene products in modulating the IGF-1-AKT-mTOR pathways. Cancer Res. 2007;67:3043–3053. doi:10.1158/0008-5472.CAN-06-4149.
   PubMed Web of Science ®Google Scholar
• Budanov AV., Sablina AA, Feinstein E, Koonin EV., Chumakov PM. Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science. 2004;304:596–600. doi:10.1126/science.1095569.
   PubMed Web of Science ®Google Scholar
• Zhang X, Shu L, Hosoi H, Gopal Murti K, Houghton PJ. Predominant nuclear localization of mammalian target of rapamycin in normal and malignant cells in culture. J Biol Chem. 2002;277:28127–28134. doi:10.1074/jbc.M202625200.
   PubMed Web of Science ®Google Scholar
• Devarenne TP, Ekengren SK, Pedley KF, Martin GB. Adi3 is a Pdk1-interacting AGC kinase that negatively regulates plant cell death. EMBO J. 2006;25:255–265. doi:10.1038/sj.emboj.7600910.
   PubMed Web of Science ®Google Scholar
• Romero-Pozuelo J, Figlia G, Kaya O, Martin-Villalba A, Teleman AA. Cdk4 and Cdk6 couple the cell-cycle machinery to cell growth via mTORC1. Cell Rep. 2020;31: 107504. doi:10.1016/j.celrep.2020.03.068.
   PubMed Web of Science ®Google Scholar
• Kumar A, Redondo-Munoz J, Perez-Garcia V, Cortes I, Chagoyen M, Carrera AC. Nuclear but not cytosolic phosphoinositide 3-kinase beta has an essential function in cell survival. Mol Cell Biol. 2011;31:2122–2133. doi:10.1128/MCB.01313-10.
   PubMed Web of Science ®Google Scholar
• Marqués M, Kumar A, Poveda AM, Zuluaga S, Hernández C, Jackson S, Pasero P, Carrera AC. Specific function of phosphoinositide 3-kinase beta in the control of DNA replication. Proc Natl Acad Sci U S A. 2009;106:7525–7530. doi:10.1073/pnas.0812000106.
   PubMed Web of Science ®Google Scholar
• Budanov AV. The role of tumor suppressor p53 in the antioxidant defense and metabolism. Subcell Biochem. 2014;85:337–358. doi:10.1007/978-94-017-9211-0_18.
   PubMedGoogle Scholar
• Czarny P, Pawlowska E, Bialkowska-Warzecha J, Kaarniranta K, Blasiak J. Autophagy in DNA damage response. Int J Mol Sci. 2015;16: 2641–2662. doi:10.3390/ijms16022641.
   PubMed Web of Science ®Google Scholar
• Hasty P, Sharp ZD, Curiel TJ, Campisi J. mTORC1 and p53: clash of the gods? Cell Cycle. 2013;12: 20–25. doi:10.4161/cc.22912.
   PubMed Web of Science ®Google Scholar
• Liebl MC, Hofmann TG. Cell fate regulation upon DNA damage: p53 serine 46 kinases pave the cell death road. BioEssays. 2019;41:e1900127. doi:10.1002/bies.201900127.
   PubMed Web of Science ®Google Scholar
• Lai KP, Leong WF, Chau JFL, Jia D, Zeng L, Liu H, He L, Hao A, Zhang H, Meek D, et al. S6K1 is a multifaceted regulator of Mdm2 that connects nutrient status and DNA damage response. EMBO J. 2010;29:2994–3006. doi:10.1038/emboj.2010.166.
   PubMed Web of Science ®Google Scholar
• He Z, Simon HU. A novel link between p53 and ROS. Cell Cycle. 2013;12:201–202. doi:10.4161/cc.23418.
   PubMed Web of Science ®Google Scholar
• Achanta G, Huang P. Role of p53 in sensing oxidative DNA damage in response to reactive oxygen species-generating agents. Cancer Res. 2004;64:6233–6239. doi:10.1158/0008-5472.CAN-04-0494.
   PubMed Web of Science ®Google Scholar
• Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;169:361–371. doi:10.1016/j.cell.2017.03.035.
   PubMed Web of Science ®Google Scholar
• Wang X, Proud CG. The mTOR pathway in the control of protein synthesis. Physiology. 2006;21:362–369. doi:10.1152/physiol.00024.2006.
   PubMed Web of Science ®Google Scholar
• Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004;18:1926–1945. doi:10.1101/gad.1212704.
   PubMed Web of Science ®Google Scholar
• Ma XM, Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol. 2009;10:307–318. doi:10.1038/nrm2672.
   PubMed Web of Science ®Google Scholar
• Muñoz IM, Hain K, Déclais AC, Gardiner M, Toh GW, Sanchez-Pulido L, Heuckmann JM, Toth R, Macartney T, Eppink B, et al. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell. 2009;35:116–127. doi:10.1016/j.molcel.2009.06.020.
   PubMed Web of Science ®Google Scholar
• Tesmer JJG. Chapter 4. Structure and function of regulator of G protein signaling homology domains. Prog Mol Biol Transl Sci. 2009;86:75–113.
   PubMed Web of Science ®Google Scholar
• Uno S, You Z, Masai H. Purification of replication factors using insect and mammalian cell expression systems. Methods. 2012;57:214–21. doi:10.1016/j.ymeth.2012.06.016.
   PubMed Web of Science ®Google Scholar