Mitotic Bookmarking: Maintaining Post-mitotic Reprogramming of Transcription Reactivation

Overview

Journal Curr Mol Biol Rep

Specialty Biochemistry

Date 2016 Apr 5

PMID 27042400

Citations 19

Authors

Niraj Lodhi

Yingbiao Ji

Alexei Tulin

Affiliations

Soon will be listed here.

Abstract

Restoring chromatin structure with high fidelity after mitosis is critical for cell survival. Transcriptional reactivation of genes is the first step toward establishing identity of the daughter cell. During mitosis, chromatin bookmarking factors associated with specific chromatin regions ensure the restoration of the original gene expression pattern in daughter cells. Recent findings have provided new insights into the mechanisms, regulation, and biological significance of gene bookmarking in eukaryotes. In this review, we discuss how epigenetic factors, such as Poly(ADP-ribose) Polymerase-1, establish epigenetic memory in mitotic chromatin.

Citing Articles

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References

Meyer-Ficca M, Lonchar J, Credidio C, Ihara M, Li Y, Wang Z . Disruption of poly(ADP-ribose) homeostasis affects spermiogenesis and sperm chromatin integrity in mice. Biol Reprod. 2009; 81(1):46-55. PMC: 3110478. DOI: 10.1095/biolreprod.108.075390. View

Sultan M, Schulz M, Richard H, Magen A, Klingenhoff A, Scherf M . A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science. 2008; 321(5891):956-60. DOI: 10.1126/science.1160342. View

Thomas C, Tulin A . Poly-ADP-ribose polymerase: machinery for nuclear processes. Mol Aspects Med. 2013; 34(6):1124-37. PMC: 3750069. DOI: 10.1016/j.mam.2013.04.001. View

Dovat S, Ronni T, Russell D, Ferrini R, Cobb B, Smale S . A common mechanism for mitotic inactivation of C2H2 zinc finger DNA-binding domains. Genes Dev. 2002; 16(23):2985-90. PMC: 187490. DOI: 10.1101/gad.1040502. View

Ng R, Gurdon J . Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol. 2007; 10(1):102-9. DOI: 10.1038/ncb1674. View

Schiewer M, Goodwin J, Han S, Brenner J, Augello M, Dean J . Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov. 2012; 2(12):1134-49. PMC: 3519969. DOI: 10.1158/2159-8290.CD-12-0120. View

Ishihara K, Oshimura M, Nakao M . CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol Cell. 2006; 23(5):733-42. DOI: 10.1016/j.molcel.2006.08.008. View

Kelly T, Jones P . Role of nucleosomes in mitotic bookmarking. Cell Cycle. 2011; 10(3):370-1. DOI: 10.4161/cc.10.3.14734. View

Ferreira R, Ohneda K, Yamamoto M, Philipsen S . GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol Cell Biol. 2005; 25(4):1215-27. PMC: 548021. DOI: 10.1128/MCB.25.4.1215-1227.2005. View

10.

Ji Y, Tulin A . The roles of PARP1 in gene control and cell differentiation. Curr Opin Genet Dev. 2010; 20(5):512-8. PMC: 2942995. DOI: 10.1016/j.gde.2010.06.001. View

11.

Bai P, Canto C . The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab. 2012; 16(3):290-5. DOI: 10.1016/j.cmet.2012.06.016. View

12.

Ji Y, Tulin A . Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res. 2009; 37(11):3501-13. PMC: 2699505. DOI: 10.1093/nar/gkp218. View

13.

Tanenbaum M, Stern-Ginossar N, Weissman J, Vale R . Regulation of mRNA translation during mitosis. Elife. 2015; 4. PMC: 4548207. DOI: 10.7554/eLife.07957. View

14.

Kouskouti A, Talianidis I . Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J. 2004; 24(2):347-57. PMC: 545808. DOI: 10.1038/sj.emboj.7600516. View

15.

Ji Y, Tulin A . Poly(ADP-ribose) controls DE-cadherin-dependent stem cell maintenance and oocyte localization. Nat Commun. 2012; 3:760. PMC: 3319983. DOI: 10.1038/ncomms1759. View

16.

Shen W, Wang D, Ye B, Shi M, Zhang Y, Zhao Z . A possible role of Drosophila CTCF in mitotic bookmarking and maintaining chromatin domains during the cell cycle. Biol Res. 2015; 48:27. PMC: 4485355. DOI: 10.1186/s40659-015-0019-6. View

17.

Lai Y, Chang C, Pawlik K, Zhou D, Renfrow M, Townes T . SRY (sex determining region Y)-box2 (Sox2)/poly ADP-ribose polymerase 1 (Parp1) complexes regulate pluripotency. Proc Natl Acad Sci U S A. 2012; 109(10):3772-7. PMC: 3309723. DOI: 10.1073/pnas.1108595109. View

18.

Kotova E, Lodhi N, Jarnik M, Pinnola A, Ji Y, Tulin A . Drosophila histone H2A variant (H2Av) controls poly(ADP-ribose) polymerase 1 (PARP1) activation in chromatin. Proc Natl Acad Sci U S A. 2011; 108(15):6205-10. PMC: 3076809. DOI: 10.1073/pnas.1019644108. View

19.

Dey A, Nishiyama A, Karpova T, McNally J, Ozato K . Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol Biol Cell. 2009; 20(23):4899-909. PMC: 2785733. DOI: 10.1091/mbc.e09-05-0380. View

20.

Szyf M . Nongenetic inheritance and transgenerational epigenetics. Trends Mol Med. 2015; 21(2):134-44. DOI: 10.1016/j.molmed.2014.12.004. View