How is epigenetic information maintained through DNA replication?

Springer Science and Business Media LLC - Tập 6 - Trang 1-7 - 2013
Varija N Budhavarapu1, Myrriah Chavez1, Jessica K Tyler1
1Department of Biochemistry and Molecular Biology, University of Texas MD Anderson Cancer Center, Houston, USA

Tóm tắt

DNA replication is a highly conserved process that accurately copies the genetic information from one generation to the next. The processes of chromatin disassembly and reassembly during DNA replication also have to be precisely regulated to ensure that the genetic material is compactly packaged to fit into the nucleus while also maintaining the epigenetic information that is carried by the histone proteins bound to the DNA, through cell divisions. Half of the histones that are deposited during replication are from the parental chromatin and carry the parental epigenetic information, while the other half of the histones are newly-synthesized. It has been of growing interest to understand how the parental pattern of epigenetic marks is re-established on the newly-synthesized histones, in a DNA sequence-specific manner, in order to maintain the epigenetic information through cell divisions. In this review we will discuss how histone chaperone proteins precisely coordinate the chromatin assembly process during DNA replication. We also discuss the recent evidence that histone-modifying enzymes, rather than the parental histones, are themselves epigenetic factors that remain associated with the DNA through replication to re-establish the epigenetic information on the newly-assembled chromatin.

Tài liệu tham khảo

Kornberg RD: Chromatin structure: a repeating unit of histones and DNA. Science. 1974, 184: 868-871.

Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ: Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997, 389: 251-260.

Andrews AJ, Luger K: Nucleosome structure(s) and stability: variations on a theme. Annu Rev Biophys. 2011, 40: 99-117.

Badeaux AI, Shi Y: Emerging roles for chromatin as a signal integration and storage platform. Nat Rev Mol Cell Biol. 2013, 14: 211-224.

Macalpine DM, Almouzni G: Chromatin and DNA Replication. Cold Spring Harb Perspect Biol. 2013, doi:10.1101/cshperspect.a010207

Tyler JK: Chromatin assembly. cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines. Eur J Biochem. 2002, 269: 2268-2274.

Worcel A, Han S, Wong ML: Assembly of newly replicated chromatin. Cell. 1978, 15: 969-977.

Stillman B: Chromatin assembly during SV40 DNA replication in vitro. Cell. 1986, 45: 555-565.

Campos EI, Fillingham J, Li G, Zheng H, Voigt P, Kuo WH, Seepany H, Gao Z, Day LA, Greenblatt JF, Reinberg D: The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol. 2010, 17: 1343-1351.

Alvarez F, Munoz F, Schilcher P, Imhof A, Almouzni G, Loyola A: Sequential establishment of marks on soluble histones H3 and H4. J Biol Chem. 2011, 286: 17714-17721.

Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT: The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature. 1999, 402: 555-560.

Ray-Gallet D, Quivy JP, Scamps C, Martini EM, Lipinski M, Almouzni G: HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell. 2002, 9: 1091-1100.

Xu M, Long C, Chen X, Huang C, Chen S, Zhu B: Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science. 2010, 328: 94-98.

Ahmad K, Henikoff S: Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A. 2002, 99 (Suppl 4): 16477-16484.

Smith S, Stillman B: Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell. 1989, 58: 15-25.

Huang S, Zhou H, Katzmann D, Hochstrasser M, Atanasova E, Zhang Z: Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc Natl Acad Sci U S A. 2005, 102: 13410-13415.

Fazly A, Li Q, Mer G, Horazdovsky B, Zhang Z: Histone chaperone Rtt106 promotes nucleosome formation using (H3-H4)2 tetramers. J Biol Chem. 2012, 287: 10753-10760.

Winkler DD, Zhou H, Dar MA, Zhang Z, Luger K: Yeast CAF-1 assembles histone (H3-H4)2 tetramers prior to DNA deposition. Nucleic Acids Res. 2012, 40: 10139-10149.

Liu WH, Roemer SC, Port AM, Churchill ME: CAF-1-induced oligomerization of histones H3/H4 and mutually exclusive interactions with Asf1 guide H3/H4 transitions among histone chaperones and DNA. Nucleic Acids Res. 2012, 40: 11229-11239.

Smith S, Stillman B: Stepwise assembly of chromatin during DNA replication in vitro. EMBO J. 1991, 10: 971-980.

Weintraub H, Worcel A, Alberts B: A model for chromatin based upon two symmetrically paired half-nucleosomes. Cell. 1976, 9: 409-417.

Jackson V: In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry. 1990, 29: 719-731.

Zhu B, Reinberg D: Epigenetic inheritance: uncontested?. Cell Res. 2011, 21: 435-441.

Gerard A, Koundrioukoff S, Ramillon V, Sergere JC, Mailand N, Quivy JP, Almouzni G: The replication kinase Cdc7-Dbf4 promotes the interaction of the p150 subunit of chromatin assembly factor 1 with proliferating cell nuclear antigen. EMBO Rep. 2006, 7: 817-823.

Moggs JG, Grandi P, Quivy JP, Jonsson ZO, Hubscher U, Becker PB, Almouzni G: A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol. 2000, 20: 1206-1218.

Shibahara K, Stillman B: Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 1999, 96: 575-585.

Quivy JP, Roche D, Kirschner D, Tagami H, Nakatani Y, Almouzni G: A CAF-1 dependent pool of HP1 during heterochromatin duplication. EMBO J. 2004, 23: 3516-3526.

Sarraf SA, Stancheva I: Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell. 2004, 15: 595-605.

Grewal SI, Jia S: Heterochromatin revisited. Nat Rev Genet. 2007, 8: 35-46.

Xu M, Wang W, Chen S, Zhu B: A model for mitotic inheritance of histone lysine methylation. EMBO Rep. 2012, 13: 60-67.

Li F, Martienssen R, Cande WZ: Coordination of DNA replication and histone modification by the Rik1-Dos2 complex. Nature. 2011, 475: 244-248.

Muchardt C, Guilleme M, Seeler JS, Trouche D, Dejean A, Yaniv M: Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep. 2002, 3: 975-981.

Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G: Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet. 2002, 30: 329-334.

Milutinovic S, Zhuang Q, Szyf M: Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification. J Biol Chem. 2002, 277: 20974-20978.

Esteve PO, Chin HG, Smallwood A, Feehery G, Gangisetty O, Karpf AR, Carey MF, Pradhan S: Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev. 2006, 20: 3089-3103.

Poot RA, Bozhenok L, van den Berg DL, Steffensen S, Ferreira F, Grimaldi M, Gilbert N, Ferreira J, Varga-Weisz PD: The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol. 2004, 6: 1236-1244.

Zentner GE, Henikoff S: Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol. 2013, 20: 259-266.

Groth A, Rocha W, Verreault A, Almouzni G: Chromatin challenges during DNA replication and repair. Cell. 2007, 128: 721-733.

Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF: Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science. 1997, 277: 1996-2000.

Fujita N, Watanabe S, Ichimura T, Tsuruzoe S, Shinkai Y, Tachibana M, Chiba T, Nakao M: Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J Biol Chem. 2003, 278: 24132-24138.

Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, Reinberg D: Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev. 1999, 13: 1924-1935.

Le Guezennec X, Vermeulen M, Brinkman AB, Hoeijmakers WA, Cohen A, Lasonder E, Stunnenberg HG: MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol. 2006, 26: 843-851.

Hendrich B, Guy J, Ramsahoye B, Wilson VA, Bird A: Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev. 2001, 15: 710-723.

Barr H, Hermann A, Berger J, Tsai HH, Adie K, Prokhortchouk A, Hendrich B, Bird A: Mbd2 contributes to DNA methylation-directed repression of the Xist gene. Mol Cell Biol. 2007, 27: 3750-3757.

Kaji K, Nichols J, Hendrich B: Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells. Development. 2007, 134: 1123-1132.

Baubec T, Ivanek R, Lienert F, Schubeler D: Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell. 2013, 153: 480-492.

Helbling Chadwick L, Chadwick BP, Jaye DL, Wade PA: The Mi-2/NuRD complex associates with pericentromeric heterochromatin during S phase in rapidly proliferating lymphoid cells. Chromosoma. 2009, 118: 445-457.

Sims JK, Wade PA: Mi-2/NuRD complex function is required for normal S phase progression and assembly of pericentric heterochromatin. Mol Biol Cell. 2011, 22: 3094-3102.

Pesavento JJ, Yang H, Kelleher NL, Mizzen CA: Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol Cell Biol. 2008, 28: 468-486.

Scharf AN, Barth TK, Imhof A: Establishment of histone modifications after chromatin assembly. Nucleic Acids Res. 2009, 37: 5032-5040.

Oda H, Okamoto I, Murphy N, Chu J, Price SM, Shen MM, Torres-Padilla ME, Heard E, Reinberg D: Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol Cell Biol. 2009, 29: 2278-2295.

Sweet SM, Li M, Thomas PM, Durbin KR, Kelleher NL: Kinetics of re-establishing H3K79 methylation marks in global human chromatin. J Biol Chem. 2010, 285: 32778-32786.

Lanzuolo C, Lo Sardo F, Diamantini A, Orlando V: PcG complexes set the stage for epigenetic inheritance of gene silencing in early S phase before replication. PLoS Genet. 2011, 7: e1002370.

Lanzuolo C, Lo Sardo F, Orlando V: Concerted epigenetic signatures inheritance at PcG targets through replication. Cell Cycle. 2012, 11: 1296-12300.

Petruk S, Sedkov Y, Johnston DM, Hodgson JW, Black KL, Kovermann SK, Beck S, Canaani E, Brock HW, Mazo A: TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell. 2012, 150: 922-933.

Zee BM, Levin RS, Xu B, LeRoy G, Wingreen NS, Garcia BA: In vivo residue-specific histone methylation dynamics. J Biol Chem. 2010, 285: 3341-3350.

Francis NJ, Follmer NE, Simon MD, Aghia G, Butler JD: Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell. 2009, 137: 110-122.

Krajewski WA, Nakamura T, Mazo A, Canaani E: A motif within SET-domain proteins binds single-stranded nucleic acids and transcribed and supercoiled DNAs and can interfere with assembly of nucleosomes. Mol Cell Biol. 2005, 25: 1891-1899.

Lo SM, Follmer ME, Lengsfeld BM, Madamba EV, Seong S, Grau DJ, Francis NJ: A bridging model for persistence of a polycomb group protein complex through DNA replication in vitro. Mol Cell. 2012, 46: 784-796.

Lo SM, McElroy KA, Francis NJ: Chromatin modification by PSC occurs at one PSC per nucleosome and does not require the acidic patch of histone H2A. PLoS One. 2012, 7: e47162.

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