Abstract
The coordination of DNA replication with histone synthesis is of utmost importance as any imbalance between the two processes results in genomic instability and may even cause lethality. Hence, to maintain genome stability, histone synthesis is regulated at multiple levels—transcriptionally, posttranscriptionally and by modulating protein stability. This tight regulation facilitates the creation of a very transient histone pool for replication-coupled chromatin assembly and ensures that histone synthesis is downregulated when DNA replication is completed or stalled due to replication inhibition. As illustrated in this chapter, the bulk of histone synthesis during S phase is activated by the same cell cycle signals that initiate DNA replication and downregulated by the same DNA damage response pathways that arrest the DNA replication machinery upon DNA damage. Conversely, the availability of histone proteins and their chaperones that help package the newly replicated DNA into chromatin in turn regulate replication fork progression. Further, in senescent cells, the histone chaperone Histone Regulatory Homolog A (HIRA), a co-repressor of histone gene transcription, plays an important role in the formation of transcriptionally silent heterochromatin that incorporates replication-dependent histone genes as well as many genes needed for DNA replication to concomitantly shut down both histone and DNA synthesis. This chapter discusses the current state of knowledge on the coregulation of histone and DNA synthesis during S phase.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Richmond TJ, Davey CA. The structure of DNA in the nucleosome core. Nature. 2003;423(6936):145–50.
Thoma F, Koller T, Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979;83(2 Pt 1):403–27. Pubmed Central PMCID: 2111545.
Sogo JM, Stahl H, Koller T, Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol. 1986;189(1):189–204.
Lycan DE, Osley MA, Hereford LM. Role of transcriptional and posttranscriptional regulation in expression of histone genes in Saccharomyces cerevisiae. Mol Cell Biol. 1987;7(2):614–21. Pubmed Central PMCID: 365116.
Kaygun H, Marzluff WF. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol. 2005;12(9):794–800.
Dominski Z, Yang XC, Kaygun H, Dadlez M, Marzluff WF. A 3′ exonuclease that specifically interacts with the 3′ end of histone mRNA. Mol Cell. 2003;12(2):295–305.
Sittman DB, Graves RA, Marzluff WF. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A. 1983;80(7):1849–53. Pubmed Central PMCID: 393707.
Gunjan A, Verreault A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell. 2003;115(5):537–49.
Meeks-Wagner D, Hartwell LH. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell. 1986;44(1):43–52.
Prado F, Aguilera A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 2005;24(6):1267–76. Pubmed Central PMCID: 556405.
Prado F, Cortes-Ledesma F, Aguilera A. The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep. 2004;5(5):497–502. Pubmed Central PMCID: 1299049.
Myung K, Pennaneach V, Kats ES, Kolodner RD. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc Natl Acad Sci U S A. 2003;100(11):6640–5. Pubmed Central PMCID: 164500.
Herrick D, Parker R, Jacobson A. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 1990;10(5):2269–84. Pubmed Central PMCID: 360574.
Osley MA. The regulation of histone synthesis in the cell cycle. Annu Rev Biochem. 1991;60:827–61.
Eriksson PR, Ganguli D, Nagarajavel V, Clark DJ. Regulation of histone gene expression in budding yeast. Genetics. 2012;191(1):7–20. Pubmed Central PMCID: 3338271.
Hess D, Liu B, Roan NR, Sternglanz R, Winston F. Spt10-dependent transcriptional activation in Saccharomyces cerevisiae requires both the Spt10 acetyltransferase domain and Spt21. Mol Cell Biol. 2004;24(1):135–43. Pubmed Central PMCID: 303362.
Kurat CF, Lambert JP, Petschnigg J, Friesen H, Pawson T, Rosebrock A, et al. Cell cycle-regulated oscillator coordinates core histone gene transcription through histone acetylation. Proc Natl Acad Sci U S A. 2014;111(39):14124–9. Pubmed Central PMCID: 4191790.
Xu F, Zhang K, Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell. 2005;121(3):375–85.
Iyer VR, Horak CE, Scafe CS, Botstein D, Snyder M, Brown PO. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature. 2001;409(6819):533–8.
Simon I, Barnett J, Hannett N, Harbison CT, Rinaldi NJ, Volkert TL, et al. Serial regulation of transcriptional regulators in the yeast cell cycle. Cell. 2001;106(6):697–708.
Ng HH, Robert F, Young RA, Struhl K. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev. 2002;16(7):806–19. Pubmed Central PMCID: 186327.
Osley MA, Gould J, Kim S, Kane MY, Hereford L. Identification of sequences in a yeast histone promoter involved in periodic transcription. Cell. 1986;45(4):537–44.
Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K. A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science. 1993;261(5128):1551–7.
Spector MS, Raff A, DeSilva H, Lee K, Osley MA. Hir1p and Hir2p function as transcriptional corepressors to regulate histone gene transcription in the Saccharomyces cerevisiae cell cycle. Mol Cell Biol. 1997;17(2):545–52. Pubmed Central PMCID: 231779.
Sutton A, Bucaria J, Osley MA, Sternglanz R. Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics. 2001;158(2):587–96. Pubmed Central PMCID: 1461693.
Xu H, Kim UJ, Schuster T, Grunstein M. Identification of a new set of cell cycle-regulatory genes that regulate S-phase transcription of histone genes in Saccharomyces cerevisiae. Mol Cell Biol. 1992;12(11):5249–59. Pubmed Central PMCID: 360458.
De Koning L, Corpet A, Haber JE, Almouzni G. Histone chaperones: an escort network regulating histone traffic. Nat Struct Mol Biol. 2007;14(11):997–1007.
Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, Yates 3rd JR, et al. Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol. 2005;15(22):2044–9. Pubmed Central PMCID: 2819815.
Fillingham J, Kainth P, Lambert JP, van Bakel H, Tsui K, Pena-Castillo L, et al. Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression. Mol Cell. 2009;35(3):340–51.
Ferreira ME, Flaherty K, Prochasson P. The Saccharomyces cerevisiae histone chaperone Rtt106 mediates the cell cycle recruitment of SWI/SNF and RSC to the HIR-dependent histone genes. PLoS One. 2011;6(6), e21113. Pubmed Central PMCID: 3115976.
Amin AD, Dimova DK, Ferreira ME, Vishnoi N, Hancock LC, Osley MA, et al. The mitotic Clb cyclins are required to alleviate HIR-mediated repression of the yeast histone genes at the G1/S transition. Biochim Biophys Acta. 2012;1819(1):16–27. Pubmed Central PMCID: 3249481.
White JH, Green SR, Barker DG, Dumas LB, Johnston LH. The CDC8 transcript is cell cycle regulated in yeast and is expressed coordinately with CDC9 and CDC21 at a point preceding histone transcription. Exp Cell Res. 1987;171(1):223–31.
Sherwood PW, Tsang SV, Osley MA. Characterization of HIR1 and HIR2, two genes required for regulation of histone gene transcription in Saccharomyces cerevisiae. Mol Cell Biol. 1993;13(1):28–38. Pubmed Central PMCID: 358881.
Goh PY, Surana U. Cdc4, a protein required for the onset of S phase, serves an essential function during G(2)/M transition in Saccharomyces cerevisiae. Mol Cell Biol. 1999;19(8):5512–22. Pubmed Central PMCID: 84393.
Drury LS, Perkins G, Diffley JF. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 1997;16(19):5966–76. Pubmed Central PMCID: 1170227.
Feldman RM, Correll CC, Kaplan KB, Deshaies RJ. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell. 1997;91(2):221–30.
Mathias N, Johnson SL, Winey M, Adams AE, Goetsch L, Pringle JR, et al. Cdc53p acts in concert with Cdc4p and Cdc34p to control the G1-to-S-phase transition and identifies a conserved family of proteins. Mol Cell Biol. 1996;16(12):6634–43. Pubmed Central PMCID: 231665.
Schneider BL, Yang QH, Futcher AB. Linkage of replication to start by the Cdk inhibitor Sic1. Science. 1996;272(5261):560–2.
Schwob E, Bohm T, Mendenhall MD, Nasmyth K. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell. 1994;79(2):233–44.
Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell. 1997;91(2):209–19.
DeSalle LM, Pagano M. Regulation of the G1 to S transition by the ubiquitin pathway. FEBS Lett. 2001;490(3):179–89.
Hall C, Nelson DM, Ye X, Baker K, DeCaprio JA, Seeholzer S, et al. HIRA, the human homologue of yeast Hir1p and Hir2p, is a novel cyclin-cdk2 substrate whose expression blocks S-phase progression. Mol Cell Biol. 2001;21(5):1854–65. Pubmed Central PMCID: 86753.
Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, et al. Targets of the cyclin-dependent kinase Cdk1. Nature. 2003;425(6960):859–64.
Amon A, Surana U, Muroff I, Nasmyth K. Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature. 1992;355(6358):368–71.
Kellogg DR, Murray AW. NAP1 acts with Clb1 to perform mitotic functions and to suppress polar bud growth in budding yeast. J Cell Biol. 1995;130(3):675–85. Pubmed Central PMCID: 2120541.
Hereford L, Bromley S, Osley MA. Periodic transcription of yeast histone genes. Cell. 1982;30(1):305–10.
Campbell SG, Li Del Olmo M, Beglan P, Bond U. A sequence element downstream of the yeast HTB1 gene contributes to mRNA 3′ processing and cell cycle regulation. Mol Cell Biol. 2002;22(24):8415–25. Pubmed Central PMCID: 139887.
Canavan R, Bond U. Deletion of the nuclear exosome component RRP6 leads to continued accumulation of the histone mRNA HTB1 in S-phase of the cell cycle in Saccharomyces cerevisiae. Nucleic Acids Res. 2007;35(18):6268–79. Pubmed Central PMCID: 2094057.
Reis CC, Campbell JL. Contribution of Trf4/5 and the nuclear exosome to genome stability through regulation of histone mRNA levels in Saccharomyces cerevisiae. Genetics. 2007;175(3):993–1010. Pubmed Central PMCID: 1840065.
LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell. 2005;121(5):713–24.
Vanacova S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 2005;3(6), e189. Pubmed Central PMCID: 1079787.
Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell. 2005;121(5):725–37.
Arigo JT, Eyler DE, Carroll KL, Corden JL. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol Cell. 2006;23(6):841–51.
Vasiljeva L, Buratowski S. Nrd1 interacts with the nuclear exosome for 3′ processing of RNA polymerase II transcripts. Mol Cell. 2006;21(2):239–48.
Harris ME, Bohni R, Schneiderman MH, Ramamurthy L, Schumperli D, Marzluff WF. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol. 1991;11(5):2416–24. Pubmed Central PMCID: 359999.
Schumperli D. Cell-cycle regulation of histone gene expression. Cell. 1986;45(4):471–2.
Heintz N. The regulation of histone gene expression during the cell cycle. Biochim Biophys Acta. 1991;1088(3):327–39.
Albig W, Doenecke D. The human histone gene cluster at the D6S105 locus. Hum Genet. 1997;101(3):284–94.
Pauli U, Chrysogelos S, Stein G, Stein J, Nick H. Protein-DNA interactions in vivo upstream of a cell cycle-regulated human H4 histone gene. Science. 1987;236(4806):1308–11.
Birnbaum MJ, Wright KL, van Wijnen AJ, Ramsey-Ewing AL, Bourke MT, Last TJ, et al. Functional role for Sp1 in the transcriptional amplification of a cell cycle regulated histone H4 gene. Biochemistry. 1995;34(23):7648–58.
Guo B, Stein JL, van Wijnen AJ, Stein GS. ATF1 and CREB trans-activate a cell cycle regulated histone H4 gene at a distal nuclear matrix associated promoter element. Biochemistry. 1997;36(47):14447–55.
Last TJ, van Wijnen AJ, Birnbaum MJ, Stein GS, Stein JL. Multiple interactions of the transcription factor YY1 with human histone H4 gene regulatory elements. J Cell Biochem. 1999;72(4):507–16.
van Wijnen AJ, van Gurp MF, de Ridder MC, Tufarelli C, Last TJ, Birnbaum M, et al. CDP/cut is the DNA-binding subunit of histone gene transcription factor HiNF-D: a mechanism for gene regulation at the G1/S phase cell cycle transition point independent of transcription factor E2F. Proc Natl Acad Sci U S A. 1996;93(21):11516–21. Pubmed Central PMCID: 38089.
Vaughan PS, van der Meijden CM, Aziz F, Harada H, Taniguchi T, van Wijnen AJ, et al. Cell cycle regulation of histone H4 gene transcription requires the oncogenic factor IRF-2. J Biol Chem. 1998;273(1):194–9.
Aziz F, van Wijnen AJ, Stein JL, Stein GS. HiNF-D (CDP-cut/CDC2/cyclin A/pRB-complex) influences the timing of IRF-2-dependent cell cycle activation of human histone H4 gene transcription at the G1/S phase transition. J Cell Physiol. 1998;177(3):453–64.
Kelly TJ, Brown GW. Regulation of chromosome replication. Annu Rev Biochem. 2000;69:829–80.
Marzluff WF, Pandey NB. Multiple regulatory steps control histone mRNA concentrations. Trends Biochem Sci. 1988;13(2):49–52.
Mailand N, Diffley JF. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell. 2005;122(6):915–26.
Duursma A, Agami R. p53-Dependent regulation of Cdc6 protein stability controls cellular proliferation. Mol Cell Biol. 2005;25(16):6937–47. Pubmed Central PMCID: 1190229.
Zhao J, Dynlacht B, Imai T, Hori T, Harlow E. Expression of NPAT, a novel substrate of cyclin E-CDK2, promotes S-phase entry. Genes Dev. 1998;12(4):456–61. Pubmed Central PMCID: 316526.
Ma T, Van Tine BA, Wei Y, Garrett MD, Nelson D, Adams PD, et al. Cell cycle-regulated phosphorylation of p220(NPAT) by cyclin E/Cdk2 in Cajal bodies promotes histone gene transcription. Genes Dev. 2000;14(18):2298–313. Pubmed Central PMCID: 316935.
Zhao J, Kennedy BK, Lawrence BD, Barbie DA, Matera AG, Fletcher JA, et al. NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription. Genes Dev. 2000;14(18):2283–97. Pubmed Central PMCID: 316937.
Ghule PN, Dominski Z, Yang XC, Marzluff WF, Becker KA, Harper JW, et al. Staged assembly of histone gene expression machinery at subnuclear foci in the abbreviated cell cycle of human embryonic stem cells. Proc Natl Acad Sci U S A. 2008;105(44):16964–9. Pubmed Central PMCID: 2579361.
Liu JL, Buszczak M, Gall JG. Nuclear bodies in the Drosophila germinal vesicle. Chromosome Res. 2006;14(4):465–75.
Miele A, Braastad CD, Holmes WF, Mitra P, Medina R, Xie R, et al. HiNF-P directly links the cyclin E/CDK2/p220NPAT pathway to histone H4 gene regulation at the G1/S phase cell cycle transition. Mol Cell Biol. 2005;25(14):6140–53. Pubmed Central PMCID: 1168814.
Zheng L, Roeder RG, Luo Y. S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell. 2003;114(2):255–66.
Roberts SB, Segil N, Heintz N. Differential phosphorylation of the transcription factor Oct1 during the cell cycle. Science. 1991;253(5023):1022–6.
DeRan M, Pulvino M, Greene E, Su C, Zhao J. Transcriptional activation of histone genes requires NPAT-dependent recruitment of TRRAP-Tip60 complex to histone promoters during the G1/S phase transition. Mol Cell Biol. 2008;28(1):435–47. Pubmed Central PMCID: 2223310.
Yang XC, Sabath I, Kunduru L, van Wijnen AJ, Marzluff WF, Dominski Z. A conserved interaction that is essential for the biogenesis of histone locus bodies. J Biol Chem. 2014;289(49):33767–82. Pubmed Central PMCID: 4256312.
Barcaroli D, Bongiorno-Borbone L, Terrinoni A, Hofmann TG, Rossi M, Knight RA, et al. FLASH is required for histone transcription and S-phase progression. Proc Natl Acad Sci U S A. 2006;103(40):14808–12. Pubmed Central PMCID: 1578501.
Burch BD, Godfrey AC, Gasdaska PY, Salzler HR, Duronio RJ, Marzluff WF, et al. Interaction between FLASH and Lsm11 is essential for histone pre-mRNA processing in vivo in Drosophila. RNA. 2011;17(6):1132–47. Pubmed Central PMCID: 3096045.
Yang XC, Xu B, Sabath I, Kunduru L, Burch BD, Marzluff WF, et al. FLASH is required for the endonucleolytic cleavage of histone pre-mRNAs but is dispensable for the 5' exonucleolytic degradation of the downstream cleavage product. Mol Cell Biol. 2011;31(7):1492–502. Pubmed Central PMCID: 3135297.
Sabath I, Skrajna A, Yang XC, Dadlez M, Marzluff WF, Dominski Z. 3′-End processing of histone pre-mRNAs in Drosophila: U7 snRNP is associated with FLASH and polyadenylation factors. RNA. 2013;19(12):1726–44. Pubmed Central PMCID: 3884669.
Eliassen KA, Baldwin A, Sikorski EM, Hurt MM. Role for a YY1-binding element in replication-dependent mouse histone gene expression. Mol Cell Biol. 1998;18(12):7106–18. Pubmed Central PMCID: 109292.
Gokhman D, Livyatan I, Sailaja BS, Melcer S, Meshorer E. Multilayered chromatin analysis reveals E2f, Smad and Zfx as transcriptional regulators of histones. Nat Struct Mol Biol. 2013;20(1):119–26.
Oswald F, Dobner T, Lipp M. The E2F transcription factor activates a replication-dependent human H2A gene in early S phase of the cell cycle. Mol Cell Biol. 1996;16(5):1889–95. Pubmed Central PMCID: 231176.
Gould KL, Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature. 1989;342(6245):39–45.
Watanabe N, Broome M, Hunter T. Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J. 1995;14(9):1878–91. Pubmed Central PMCID: 398287.
Mahajan K, Fang B, Koomen JM, Mahajan NP. H2B Tyr37 phosphorylation suppresses expression of replication-dependent core histone genes. Nat Struct Mol Biol. 2012;19(9):930–7.
Gao G, Bracken AP, Burkard K, Pasini D, Classon M, Attwooll C, et al. NPAT expression is regulated by E2F and is essential for cell cycle progression. Mol Cell Biol. 2003;23(8):2821–33. Pubmed Central PMCID: 152552.
Ye X, Wei Y, Nalepa G, Harper JW. The cyclin E/Cdk2 substrate p220(NPAT) is required for S-phase entry, histone gene expression, and Cajal body maintenance in human somatic cells. Mol Cell Biol. 2003;23(23):8586–600. Pubmed Central PMCID: 262656.
Watanabe N, Arai H, Iwasaki J, Shiina M, Ogata K, Hunter T, et al. Cyclin-dependent kinase (CDK) phosphorylation destabilizes somatic Wee1 via multiple pathways. Proc Natl Acad Sci U S A. 2005;102(33):11663–8. Pubmed Central PMCID: 1187955.
Lai ZC, Maxson R, Childs G. Both basal and ontogenic promoter elements affect the timing and level of expression of a sea urchin H1 gene during early embryogenesis. Genes Dev. 1988;2(2):173–83.
Khochbin S, Wolffe AP. Developmentally regulated expression of linker-histone variants in vertebrates. Eur J Biochem. 1994;225(2):501–10.
Duncliffe KN, Rondahl ME, Wells JR. A H1 histone gene-specific AC-box-related element influences transcription from a major chicken H1 promoter. Gene. 1995;163(2):227–32.
van Wijnen AJ, Aziz F, Grana X, De Luca A, Desai RK, Jaarsveld K, et al. Transcription of histone H4, H3, and H1 cell cycle genes: promoter factor HiNF-D contains CDC2, cyclin A, and an RB-related protein. Proc Natl Acad Sci U S A. 1994;91(26):12882–6. Pubmed Central PMCID: 45544.
Guglielmi B, La Rochelle N, Tjian R. Gene-specific transcriptional mechanisms at the histone gene cluster revealed by single-cell imaging. Mol Cell. 2013;51(4):480–92.
Gurley LR, Walters RA, Tobey RA. Sequential phsophorylation of histone subfractions in the Chinese hamster cell cycle. J Biol Chem. 1975;250(10):3936–44.
Yasuda H, Matsumoto Y, Mita S, Marunouchi T, Yamada M. A mouse temperature-sensitive mutant defective in H1 histone phosphorylation is defective in deoxyribonucleic acid synthesis and chromosome condensation. Biochemistry. 1981;20(15):4414–9.
Halmer L, Gruss C. Effects of cell cycle dependent histone H1 phosphorylation on chromatin structure and chromatin replication. Nucleic Acids Res. 1996;24(8):1420–7. Pubmed Central PMCID: 145815.
Alexandrow MG, Hamlin JL. Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J Cell Biol. 2005;168(6):875–86. Pubmed Central PMCID: 2171796.
Lu ZH, Sittman DB, Brown DT, Munshi R, Leno GH. Histone H1 modulates DNA replication through multiple pathways in Xenopus egg extract. J Cell Sci. 1997;110(Pt 21):2745–58.
Lu ZH, Sittman DB, Romanowski P, Leno GH. Histone H1 reduces the frequency of initiation in Xenopus egg extract by limiting the assembly of prereplication complexes on sperm chromatin. Mol Biol Cell. 1998;9(5):1163–76. Pubmed Central PMCID: 25338.
Marzluff WF, Wagner EJ, Duronio RJ. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet. 2008;9(11):843–54. Pubmed Central PMCID: 2715827.
Koseoglu MM, Graves LM, Marzluff WF. Phosphorylation of threonine 61 by cyclin a/Cdk1 triggers degradation of stem-loop binding protein at the end of S phase. Mol Cell Biol. 2008;28(14):4469–79. Pubmed Central PMCID: 2447125.
Koseoglu MM, Dong J, Marzluff WF. Coordinate regulation of histone mRNA metabolism and DNA replication: cyclin A/cdk1 is involved in inactivation of histone mRNA metabolism and DNA replication at the end of S phase. Cell Cycle. 2010;9(19):3857–63. Pubmed Central PMCID: 3047749.
Bracken AP, Ciro M, Cocito A, Helin K. E2F target genes: unraveling the biology. Trends Biochem Sci. 2004;29(8):409–17.
Harbour JW, Luo RX, Dei Santi A, Postigo AA, Dean DC. Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell. 1999;98(6):859–69.
Truscott M, Raynal L, Premdas P, Goulet B, Leduy L, Berube G, et al. CDP/Cux stimulates transcription from the DNA polymerase alpha gene promoter. Mol Cell Biol. 2003;23(8):3013–28. Pubmed Central PMCID: 152546.
Henneke G, Koundrioukoff S, Hubscher U. Phosphorylation of human Fen1 by cyclin-dependent kinase modulates its role in replication fork regulation. Oncogene. 2003;22(28):4301–13.
Singh RK, Kabbaj MH, Paik J, Gunjan A. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat Cell Biol. 2009;11(8):925–33. Pubmed Central PMCID: 2720428.
Singh RK, Liang D, Gajjalaiahvari UR, Kabbaj MH, Paik J, Gunjan A. Excess histone levels mediate cytotoxicity via multiple mechanisms. Cell Cycle. 2010;9(20):4236–44. Pubmed Central PMCID: 3055206.
Su C, Gao G, Schneider S, Helt C, Weiss C, O'Reilly MA, et al. DNA damage induces downregulation of histone gene expression through the G1 checkpoint pathway. EMBO J. 2004;23(5):1133–43. Pubmed Central PMCID: 380976.
Weinert TA, Kiser GL, Hartwell LH. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 1994;8(6):652–65.
Bongiorno-Borbone L, De Cola A, Barcaroli D, Knight RA, Di Ilio C, Melino G, et al. FLASH degradation in response to UV-C results in histone locus bodies disruption and cell-cycle arrest. Oncogene. 2010;29(6):802–10.
Mullen TE, Marzluff WF. Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev. 2008;22(1):50–65. Pubmed Central PMCID: 2151014.
Lyons SM, Ricciardi AS, Guo AY, Kambach C, Marzluff WF. The C-terminal extension of Lsm4 interacts directly with the 3′ end of the histone mRNP and is required for efficient histone mRNA degradation. RNA. 2014;20(1):88–102. Pubmed Central PMCID: 3866647.
Azzalin CM, Lingner J. The human RNA surveillance factor UPF1 is required for S phase progression and genome stability. Curr Biol. 2006;16(4):433–9.
Herrero AB, Moreno S. Lsm1 promotes genomic stability by controlling histone mRNA decay. EMBO J. 2011;30(10):2008–18. Pubmed Central PMCID: 3098488.
Beggs S, James TC, Bond U. The PolyA tail length of yeast histone mRNAs varies during the cell cycle and is influenced by Sen1p and Rrp6p. Nucleic Acids Res. 2012;40(6):2700–11. Pubmed Central PMCID: 3315300.
Alabert C, Groth A. Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol. 2012;13(3):153–67.
Zhao X, McKillop-Smith S, Muller B. The human histone gene expression regulator HBP/SLBP is required for histone and DNA synthesis, cell cycle progression and cell proliferation in mitotic cells. J Cell Sci. 2004;117(Pt 25):6043–51.
Mejlvang J, Feng Y, Alabert C, Neelsen KJ, Jasencakova Z, Zhao X, et al. New histone supply regulates replication fork speed and PCNA unloading. J Cell Biol. 2014;204(1):29–43. Pubmed Central PMCID: 3882791.
Holland L, Gauthier L, Bell-Rogers P, Yankulov K. Distinct parts of minichromosome maintenance protein 2 associate with histone H3/H4 and RNA polymerase II holoenzyme. Eur J Biochem. 2002;269(21):5192–202.
Latreille D, Bluy L, Benkirane M, Kiernan RE. Identification of histone 3 variant 2 interacting factors. Nucleic Acids Res. 2014;42(6):3542–50. Pubmed Central PMCID: 3973350.
Richet N, Liu D, Legrand P, Velours C, Corpet A, Gaubert A, et al. 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. 2015;43(3):1905–17. Pubmed Central PMCID: 4330383.
Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, et al. Regulation of replication fork progression through histone supply and demand. Science. 2007;318(5858):1928–31.
Campisi J. d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007;8(9):729–40.
Campisi J. Cellular senescence as a tumor-suppressor mechanism. Trends Cell Biol. 2001;11(11):S27–31.
Braig M, Schmitt CA. Oncogene-induced senescence: putting the brakes on tumor development. Cancer Res. 2006;66(6):2881–4.
Pang JH, Chen KY. Global change of gene expression at late G1/S boundary may occur in human IMR-90 diploid fibroblasts during senescence. J Cell Physiol. 1994;160(3):531–8.
Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell. 2003;113(6):703–16.
Sherr CJ, McCormick F. The RB and p53 pathways in cancer. Cancer Cell. 2002;2(2):103–12.
Geng Y, Lee YM, Welcker M, Swanger J, Zagozdzon A, Winer JD, et al. Kinase-independent function of cyclin E. Mol Cell. 2007;25(1):127–39.
O'Sullivan RJ, Kubicek S, Schreiber SL, Karlseder J. Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nat Struct Mol Biol. 2010;17(10):1218–25. Pubmed Central PMCID: 2951278.
Zhang R, Poustovoitov MV, Ye X, Santos HA, Chen W, Daganzo SM, et al. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev Cell. 2005;8(1):19–30.
Zhang R, Chen W, Adams PD. Molecular dissection of formation of senescence-associated heterochromatin foci. Mol Cell Biol. 2007;27(6):2343–58. Pubmed Central PMCID: 1820509.
Funayama R, Saito M, Tanobe H, Ishikawa F. Loss of linker histone H1 in cellular senescence. J Cell Biol. 2006;175(6):869–80. Pubmed Central PMCID: 2064697.
Angelov D, Molla A, Perche PY, Hans F, Cote J, Khochbin S, et al. The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol Cell. 2003;11(4):1033–41.
Dollard C, Ricupero-Hovasse SL, Natsoulis G, Boeke JD, Winston F. SPT10 and SPT21 are required for transcription of particular histone genes in Saccharomyces cerevisiae. Mol Cell Biol. 1994;14(8):5223–8. Pubmed Central PMCID: 359041.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Paik, J., Giovinazzi, S., Gunjan, A. (2016). Coordination of DNA Replication and Histone Synthesis During S Phase. In: Kaplan, D. (eds) The Initiation of DNA Replication in Eukaryotes. Springer, Cham. https://doi.org/10.1007/978-3-319-24696-3_11
Download citation
DOI: https://doi.org/10.1007/978-3-319-24696-3_11
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-24694-9
Online ISBN: 978-3-319-24696-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)