Poly(ADP-ribosylation) regulates chromatin organization through histone H3 modification and DNA methylation of the first cell cycle of mouse embryos

Biochemical and Biophysical Research Communications

Volumn 434, Issue 1, 2013, Pages 15-21

  Osada, Tomoharu ^a,b   Rydén, Anna Margareta ^c   Masutani, Mitsuko ^c  

^a LSI MEDIENCE CORPORATION   (Japan)

^b MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

DNA methylation; Fertilization; Histone modification; Poly(ADP ribosylation); Post translational modification

Indexed keywords

HISTONE H3; LYSINE; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE; CHROMATIN; DNA METHYLATION; ELECTRON MICROSCOPY; EMBRYO; EPIGENETICS; FEMALE; HISTONE MODIFICATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PROCESSING; ULTRASTRUCTURE; UPREGULATION;

ANIMALS; CELL CYCLE; CHROMATIN; DNA METHYLATION; FEMALE; HISTONES; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; PHENANTHRENES; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84876798514     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.03.074     Document Type: Article

References (37)

1. Sugimura T., Miwa M. Poly(ADP-ribose): historical perspective. Mol. Cell. Biochem. 1994, 138:5-12.
2. Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 2006, 7:517-528.
3. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342:249-268.
4. Gottschalk A.J., Timinszky G., Kong S.E., et al. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl. Acad. Sci. USA 2009, 106:13770-13774.
5. Rouleau M., Aubin R.A., Poirier G.G. Poly(ADP-ribosyl)ated chromatin domains: access granted. J. Cell Sci. 2004, 117:815-825.
6. Timinszky G., Till S., Hassa P.O., et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 2009, 16:923-929.
7. Krishnakumar R., Gamble M.J., Frizzell K.M., et al. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 2008, 319:819-821.
8. Liu H.L., Hara K.T., Aoki F. Role of the first mitosis in the remodeling of the parental genomes in mouse embryos. Cell Res. 2005, 15:127-132.
9. Bouniol C., Nguyen E., Debey P. Endogenous transcription occurs at the 1-cell stage in the mouse embryos. Exp. Cell Res. 1995, 218:57-62.
10. Henery C.C., Miranda M., Wiekowski M., et al. Repression of gene expression at the beginning of mouse development. Dev. Biol. 1995, 169:448-460.
11. Schultz R.M. Regulation of zygotic gene activation in the mouse. BioEssay 1993, 15:531-538.
12. Tadros W., Lipshitz H.D. The maternal-to-zygotic transition: a play in two acts. Development 2009, 136:3033-3042.
13. Schultz R.M. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Update 2002, 8:323-331.
14. McKay D.W., Clarke H.J. The ability to organize sperm DNA into functional chromatin is acquired during meiotic maturation in murine oocytes. Dev. Biol. 1997, 186:73-84.
15. Williams G.T., Shall S., Ford C.C. NAD turnover during early development of Xenopus laevis. Biochim. Biophys. Acta 1983, 762:272-280.
16. Epel D. The initiation of development at fertilization. Cell Differ. Dev. 1990, 29:1-12.
17. Osada T., Ogino H., Hino T., et al. PolyADP-ribosylation is required for pronuclear fusion during postfertilization in mice. PLoS One 2010, 5:e12526.
18. Osada T., Masutani M. PolyADP-ribosylation in postfertilization and genome reprogramming: implications for carcinogenesis. Polymerization 2012, InTech, New York, 10.5772/46097. Gomes, A.D.S. Gomes (Eds.).
19. Masutani M., Suzuki H., Kamada N., et al. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. USA 1999, 96:2301-2304.
20. Toyoda Y., Yokoyama M., Hoshi T. Studies on the fertilization of mouse eggs in vitro. J. Anim. Reprod. 1971, 16:147-151.
21. Osada T., Toyoda A., Moisyadi S., et al. Production of inbred and hybrid transgenic mice carrying lathe (>200kb) foreign DNA fragments by intracytoplasmic sperm injection. Mol. Reprod. Dev. 2005, 72:329-335.
22. Summers M.C., McGinnis L.K., Lawitts J.A., et al. IVF of mouse ova in a simplex optimized medium supplemented with amino acids. Hum. Reprod. 2000, 15:1791-1801.
23. Whitten W.K., Biggers J.D. Complete development in vitro of the pre-implantation stages of the mouse in a simple chemically defined medium. J. Reprod. Fertil. 1968, 17:399-401.
24. Simerly C., Schatten G. Techniques for localization of specific molecules in oocytes and embryos. Methods Enzymol. 1993, 225:516-553.
25. Perkins E., Sun D., Nguyeb A., et al. Novel inhibitors of poly(ADP-ribose) polymerase/PARP1 and PARP2 identified using a cell-based screen in yeast. Cancer Res. 2001, 61:4175-4183.
26. Erfurth F.E., Popovic R., Grembecka J., et al. MLL protects CpG clusters from methylation within the Hoxa9 gene, maintaining transcript expression. Proc. Natl. Acad. Sci. USA 2008, 105:7517-7522.
27. Vaissiere T., Swan C., Herceg Z. Epigenetic interplay between histone modification and DNA methylation in gene silencing. Mutat. Res. 2008, 659:40-48.
28. Mayer W., Niveleau A., Walter J., et al. Demethylation of the zygotic paternal genome. Nature 2000, 402:501-502.
29. Quenet D., Gasser V., Fouillen L., et al. The histone subcode: poly(ADP-ribose) polymerase-1 (Parp-1) and Parp-2 control cell differentiation by regulating the transfcriptional intermediary factor TIF beta and heterochromatin protein HP1alpha. FASEB J. 2008, 22:3853-3865.
30. Boulikas T. Poly(ADP-ribosylated) histones in chromatin replication. J. Biol. Chem. 1980, 265:14638-14647.
31. Huber A., Bai P., de Murcia M., et al. PARP-1, PARP-2 and ATM in the DNA damage response: functional synergy in mouse development. DNA Repair 2004, 3:1103-1108.
32. Poirier G.G., de Murcia G., Jongstra-Bilen J., et al. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc. Acad. Natl. Sci. USA 1982, 79:3423-3427.
33. Tulin A., Spradling A. Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 2003, 299:560-562.
34. Cao R., Zhang Y. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol. Cell 2004, 2:57-67.
35. Nakamura T., Arai Y., Umehara H., et al. PGC/Stella protects against demethylation in early embryogenesis. Nat. Cell Biol. 2007, 9:64-71.
36. Caiafa P., Guastafierro T., Zampieri M. Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns. FASEB J. 2009, 23:672-678.
37. Barreto G., Schafer A., Marhold J., et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.