Genetic interaction of RAD53 protein kinase with histones is important for DNA replication

References

• Takeda DY, Dutta A. DNA replication and progression through S phase. Oncogene 2005; 24:2827 - 2843
   PubMed Web of Science ®Google Scholar
• Sclafani RA, Holzen TM. Cell cycle regulation of DNA replication. Annu Rev Genet 2007; 41:237 - 280
   PubMed Web of Science ®Google Scholar
• Cocker JH, Piatti S, Santocanale C, Nasmyth K, Diffley JF. An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature 1996; 379:180 - 182
   PubMed Web of Science ®Google Scholar
• Tanaka S, Diffley JF. Interdependent nuclear accumulation of budding yeast Cdt1 and Mcm2-7 during G1 phase. Nat Cell Biol 2002; 4:198 - 207
   PubMed Web of Science ®Google Scholar
• Labib K, Tercero JA, Diffley JF. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 2000; 288:1643 - 1647
   PubMed Web of Science ®Google Scholar
• Bochman ML, Schwacha A. The Mcm2-7 complex has in vitro helicase activity. Mol Cell 2008; 31:287 - 293
   PubMed Web of Science ®Google Scholar
• Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, et al. Replication dynamics of the yeast genome. Science 2001; 294:115 - 121
   PubMed Web of Science ®Google Scholar
• Tanaka S, Umemori T, Hirai K, Muramatsu S, Kamimura Y, Araki H. CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 2007; 445:328 - 332
   PubMed Web of Science ®Google Scholar
• Zegerman P, Diffley JF. Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 2007; 445:281 - 285
   PubMed Web of Science ®Google Scholar
• Sclafani RA. Cdc7p-Dbf4p becomes famous in the cell cycle. J Cell Sci 2000; 113:2111 - 2117
   PubMed Web of Science ®Google Scholar
• Murray AW. Recycling the cell cycle: cyclins revisited. Cell 2004; 116:221 - 234
   PubMed Web of Science ®Google Scholar
• Hardy CF, Dryga O, Seematter S, Pahl PM, Sclafani RA. mcm5/cdc46-bob1 bypasses the requirement for the S phase activator Cdc7p. Proc Natl Acad Sci USA 1997; 94:3151 - 3155
   PubMed Web of Science ®Google Scholar
• Sheu YJ, Stillman B. The Dbf4-Cdc7 kinase promotes S phase by alleviating an inhibitory activity in Mcm4. Nature 2010; 463:113 - 117
   PubMed Web of Science ®Google Scholar
• Fletcher RJ, Chen XS. Biochemical activities of the BOB1 mutant in Methanobacterium thermoautotrophicum MCM. Biochemistry 2006; 45:462 - 467
   PubMed Web of Science ®Google Scholar
• Hoang ML, Leon RP, Pessoa-Brandao L, Hunt S, Raghuraman MK, Fangman WL, et al. Structural changes in Mcm5 protein bypass Cdc7-Dbf4 function and reduce replication origin efficiency in Saccharomyces cerevisiae. Mol Cell Biol 2007; 27:7594 - 7602
   PubMed Web of Science ®Google Scholar
• Nyberg KA, Michelson RJ, Putnam CW, Weinert TA. Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 2002; 36:617 - 656
   PubMed Web of Science ®Google Scholar
• Branzei D, Foiani M. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 2008; 9:297 - 308
   PubMed Web of Science ®Google Scholar
• Hartwell LH, Weinert TA. Checkpoints: Controls that ensure the order of cell cycle events. Science 1989; 246:629 - 634
   PubMed Web of Science ®Google Scholar
• Zhou Z, Elledge SJ. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 1993; 75:1119 - 11127
   PubMed Web of Science ®Google Scholar
• Bashkirov VI, Bashkirova EV, Haghnazari E, Heyer WD. Direct kinase-to-kinase signaling mediated by the FHA phosphoprotein recognition domain of the Dun1 DNA damage checkpoint kinase. Mol Cell Biol 2003; 23:1441 - 1452
   PubMed Web of Science ®Google Scholar
• Segurado M, Tercero JA. The S-phase checkpoint: Targeting the replication fork. Biol Cell 2009; 101:617 - 627
   PubMed Web of Science ®Google Scholar
• Alvino GM, Collingwood D, Murphy JM, Delrow J, Brewer BJ, Raghuraman MK. Replication in hydroxyurea: it's a matter of time. Mol Cell Biol 2007; 27:6396 - 6406
   PubMed Web of Science ®Google Scholar
• Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, Muzi-Falconi M, et al. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 2001; 412:557 - 561
   PubMed Web of Science ®Google Scholar
• Sogo JM, Lopes M, Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 2002; 297:599 - 602
   PubMed Web of Science ®Google Scholar
• Tercero JA, Diffley JF. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 2001; 412:553 - 557
   PubMed Web of Science ®Google Scholar
• Segurado M, Diffley JF. Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev 2008; 22:1816 - 1827
   PubMed Web of Science ®Google Scholar
• Hofmann K, Bucher P. The FHA domain: A putative nuclear signalling domain found in protein kinases and transcription factors. Trends Biochem Sci 1995; 20:347 - 349
   PubMed Web of Science ®Google Scholar
• Durocher D, Jackson SP. The FHA domain. FEBS Lett 2002; 513:58 - 66
   PubMed Web of Science ®Google Scholar
• Alcasabas AA, Osborn AJ, Bachant J, Hu F, Werler PJ, Bousset K, et al. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol 2001; 3:958 - 965
   PubMed Web of Science ®Google Scholar
• Smolka MB, Chen SH, Maddox PS, Enserink JM, Albuquerque CP, Wei XX, et al. An FHA domainmediated protein interaction network of Rad53 reveals its role in polarized cell growth. J Cell Biol 2006; 175:743 - 753
   PubMed Web of Science ®Google Scholar
• Duncker BP, Shimada K, Tsai-Pflugfelder M, Pasero P, Gasser SM. An N-terminal domain of Dbf4p mediates interaction with both origin recognition complex (ORC) and Rad53p and can deregulate late origin firing. Proc Natl Acad Sci USA 2002; 99:16087 - 16092
   PubMed Web of Science ®Google Scholar
• Schwartz MF, Lee SJ, Duong JK, Eminaga S, Stern DF. FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2003; 2:384 - 396
   PubMed Web of Science ®Google Scholar
• Sun Z, Hsiao J, Fay DS, Stern DF. Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science 1998; 281:272 - 274
   PubMed Web of Science ®Google Scholar
• Chen SH, Zhou H. Reconstitution of Rad53 activation by Mec1 through adaptor protein Mrc1. J Biol Chem 2009; 284:18593 - 18604
   PubMed Web of Science ®Google Scholar
• Jia-Lin Ma N, Stern DF. Regulation of the Rad53 protein kinase in signal amplification by oligomer assembly and disassembly. Cell Cycle 2008; 7:808 - 817
   PubMed Web of Science ®Google Scholar
• Zhao X, Chabes A, Domkin V, Thelander L, Rothstein R. The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage. EMBO J 2001; 20:3544 - 3553
   PubMed Web of Science ®Google Scholar
• Chabes A, Georgieva B, Domkin V, Zhao X, Rothstein R, Thelander L. Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 2003; 112:391 - 401
   PubMed Web of Science ®Google Scholar
• Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev 1994; 8:2401 - 2415
   PubMed Web of Science ®Google Scholar
• Fay DS, Sun Z, Stern DF. Mutations in SPK1/RAD53 that specifically abolish checkpoint but not growthrelated functions. Curr Genet 1997; 31:97 - 105
   PubMed Web of Science ®Google Scholar
• Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J. Diverse but overlapping functions of the two forkheadassociated (FHA) domains in Rad53 checkpoint kinase activation. J Biol Chem 2003; 278:30421 - 30424
   PubMed Web of Science ®Google Scholar
• Desany BA, Alcasabas AA, Bachant JB, Elledge SJ. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev 1998; 12:2956 - 2970
   PubMed Web of Science ®Google Scholar
• Zhao X, Muller EG, Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 1998; 2:329 - 340
   PubMed Web of Science ®Google Scholar
• Gunjan A, Verreault A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 2003; 115:537 - 549
   PubMed Web of Science ®Google Scholar
• Singh RK, Kabbaj MH, Paik J, Gunjan A. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat Cell Biol 2009; 11:925 - 933
   PubMed Web of Science ®Google Scholar
• Dohrmann PR, Oshiro G, Tecklenburg M, Sclafani RA. RAD53 regulates DBF4 independently of checkpoint function in Saccharomyces cerevisiae. Genetics 1999; 151:965 - 977
   PubMed Web of Science ®Google Scholar
• Dohrmann PR, Sclafani RA. Novel role for checkpoint Rad53 protein kinase in the initiation of chromosomal DNA replication in Saccharomyces cerevisiae. Genetics 2006; 174:87 - 99
   PubMed Web of Science ®Google Scholar
• Zheng P, Fay DS, Burton J, Xiao H, Pinkham JL, Stern DF. SPK1 is an essential S-phase-specific gene of Saccharomyces cerevisiae that encodes a nuclear serine/threonine/tyrosine kinase. Mol Cell Biol 1993; 13:5829 - 5842
   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
   PubMed Web of Science ®Google Scholar
• Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, Plevani P, et al. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J 1999; 18:6561 - 6572
   PubMed Web of Science ®Google Scholar
• Lee SJ, Schwartz MF, Duong JK, Stern DF. Rad53 phosphorylation site clusters are important for Rad53 regulation and signaling. Mol Cell Biol 2003; 23:6300 - 6314
   PubMed Web of Science ®Google Scholar
• Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, et al. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 2003; 424:1078 - 1083
   PubMed Web of Science ®Google Scholar
• Li JJ, Herskowitz I. Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system. Science 1993; 262:1870 - 1874
   PubMed Web of Science ®Google Scholar
• Dowell SJ, Romanowski P, Diffley JF. Interaction of Dbf4, the Cdc7 protein kinase regulatory subunit, with yeast replication origins in vivo. Science 1994; 265:1243 - 1246
   PubMed Web of Science ®Google Scholar
• Maine GT, Sinha P, Tye BK. Mutants of S. cerevisiae defective in the maintenance of minichromosomes. Genetics 1984; 106:365 - 385
   PubMed Web of Science ®Google Scholar
• Hogan E, Koshland D. Addition of extra origins of replication to a minichromosome suppresses its mitotic loss in cdc6 and cdc14 mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1992; 89:3098 - 3102
   PubMed Web of Science ®Google Scholar
• Leon RP, Tecklenburg M, Sclafani RA. Functional conservation of beta-hairpin DNA binding domains in the Mcm protein of Methanobacterium thermoautotrophicum and the Mcm5 protein of Saccharomyces cerevisiae. Genetics 2008; 179:1757 - 1768
   PubMed Web of Science ®Google Scholar
• Loo S, Fox CA, Rine J, Kobayashi R, Stillman B, Bell S. The origin recognition complex in silencing, cell cycle progression and DNA replication. Mol Biol Cell 1995; 6:741 - 756
   PubMed Web of Science ®Google Scholar
• English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK. Structural basis for the histone chaperone activity of Asf1. Cell 2006; 127:495 - 508
   PubMed Web of Science ®Google Scholar
• Groth A, Ray-Gallet D, Quivy JP, Lukas J, Bartek J, Almouzni G. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol Cell 2005; 17:301 - 311
   PubMed Web of Science ®Google Scholar
• Morillo-Huesca M, Maya D, Munoz-Centeno MC, Singh RK, Oreal V, Reddy GU, et al. FACT prevents the accumulation of free histones evicted from transcribed chromatin and a subsequent cell cycle delay in G1. PLoS Genet 2010; 6:1000964
   PubMed Web of Science ®Google Scholar
• Tamburini BA, Carson JJ, Adkins MW, Tyler JK. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot Cell 2005; 4:1583 - 1590
   PubMed Web of Science ®Google Scholar
• Simpson RT. Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature 1990; 343:387 - 389
   PubMed Web of Science ®Google Scholar
• Eaton ML, Galani K, Kang S, Bell SP, MacAlpine DM. Conserved nucleosome positioning defines replication origins. Genes Dev 2010; 24:748 - 753
   PubMed Web of Science ®Google Scholar
• Lipford JR, Bell SP. Nucleosomes positioned by ORC facilitate the initiation of DNA replication. Mol Cell 2001; 7:21 - 30
   PubMed Web of Science ®Google Scholar
• Sun Z, Fay DS, Marini F, Foiani M, Stern DF. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev 1996; 10:395 - 406
   PubMed Web of Science ®Google Scholar
• Oliver AW, Paul A, Boxall KJ, Barrie SE, Aherne GW, Garrett MD, et al. Trans-activation of the DNAdamage signalling protein kinase Chk2 by T-loop exchange. EMBO J 2006; 25:3179 - 3190
   PubMed Web of Science ®Google Scholar
• Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298:1912 - 1934
   PubMed Web of Science ®Google Scholar
• Hanks SK, Hunter T. Protein kinase 6. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. Faseb J 1995; 9:576 - 596
   PubMed Web of Science ®Google Scholar
• Felberg J, Lefebvre DC, Lam M, Wang Y, Ng DH, Birkenhead D, et al. Subdomain X of the kinase domain of Lck binds CD45 and facilitates dephosphorylation. J Biol Chem 2004; 279:3455 - 3462
   PubMed Web of Science ®Google Scholar
• Graves PR, Winkfield KM, Haystead TA. Regulation of zipper-interacting protein kinase activity in vitro and in vivo by multisite phosphorylation. J Biol Chem 2005; 280:9363 - 9374
   PubMed Web of Science ®Google Scholar
• Haas AL, Bright PM, Jackson VE. Functional diversity among putative E2 isozymes in the mechanism of ubiquitin-histone ligation. J Biol Chem 1988; 263:13268 - 13275
   PubMed Web of Science ®Google Scholar
• Haas A, Reback PM, Pratt G, Rechsteiner M. Ubiquitin-mediated degradation of histone H3 does not require the substrate-binding ubiquitin protein ligase, E3 or attachment of polyubiquitin chains. J Biol Chem 1990; 265:21664 - 21669
   PubMed Web of Science ®Google Scholar
• Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 2006; 124:1069 - 1081
   PubMed Web of Science ®Google Scholar
• Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, et al. Global mapping of the yeast genetic interaction network. Science 2004; 303:808 - 813
   PubMed Web of Science ®Google Scholar
• Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, et al. The genetic landscape of a cell. Science 2010; 327:425 - 431
   PubMed Web of Science ®Google Scholar
• Hartwell LH. Macromolecule synthesis in temperaturesensitive mutants of yeast. J Bacteriol 1967; 93:1662 - 1670
   PubMed Web of Science ®Google Scholar
• Ito H, Fukuda Y, Murata K, Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol 1983; 153:163 - 168
   PubMed Web of Science ®Google Scholar
• Pessoa-Brandao L, Sclafani RA. CDC7/DBF4 functions in the translesion synthesis branch of the RAD6 epistasis group in Saccharomyces cerevisiae. Genetics 2004; 167:1597 - 1610
   PubMed Web of Science ®Google Scholar
• Foiani M, Liberi G, Piatti S, Plavani P. Cotterill S. Saccharomyces cerevisiae as a model system to study DNA replication. Eukaryotic DNA Replication A Practical Approach 1999; Oxford Oxford University Press 185 - 200
   Google Scholar
• Shellman YG, Schauer IE, Oshiro G, Dohrmann P, Sclafani RA. Oligomers of the Cdc7/Dbf4 protein kinase exist in the yeast cell. Mol Gen Genet 1998; 259:429 - 436
   PubMedGoogle Scholar
• Lengronne A, Schwob E. The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol Cell 2002; 9:1067 - 1078
   PubMed Web of Science ®Google Scholar
• Mann RK, Grunstein M. Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. EMBO J 1992; 11:3297 - 3306
   PubMed Web of Science ®Google Scholar