Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes

EMBO Journal

Volumn 29, Issue 11, 2010, Pages 1877-1888

  Wossidlo, Mark ^a   Arand, Julia ^a   Sebastiano, Vittorio ^b,d   Lepikhov, Konstantin ^a   Boiani, Michele ^b   Reinhardt, Richard ^c   Schöler, Hans ^b   Walter, Jörn ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

H2A.X; DNA demethylation; DNA repair; Epigenetic reprogramming; Mouse zygote

Indexed keywords

DNA POLYMERASE; HISTONE GAMMA H2AX; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE G1 PHASE; DNA METHYLATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME INHIBITION; FERTILIZATION IN VITRO; MALE; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SINGLE STRANDED DNA BREAK; SOMATIC CELL; ZYGOTE;

ANIMALS; CHROMOSOMES; CLONING, ORGANISM; CYTOSINE; DNA; DNA BREAKS; DNA DAMAGE; DNA METHYLATION; MAMMALS; MICE; NUCLEAR TRANSFER TECHNIQUES; ZYGOTE;

MAMMALIA;

EID: 77953596050     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.80     Document Type: Article

References (57)

1. Adenot PG, Mercier Y, Renard JP, Thompson EM (1997) Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124: 4615-4625
2. Aoki E, Schultz RM (1999) DNA replication in the 1-cell mouse embryo: stimulatory effect of histone acetylation. Zygote 7: 165-172
3. Aoki F, Worrad DM, Schultz RM (1997) Regulation of transcriptional activity during the first and second cell cycles in the preimplanta-tion mouse embryo. Dev Biol 181: 296-307
4. Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, Handa V, Doderlein G, Maltry N, Wu W, Lyko F, Niehrs C (2007) Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445: 671-675
5. Berger NA, Kurohara KK, Petzold SJ, Sikorski GW (1979) Aphidicolin inhibits eukaryotic DNA replication and repair\implications for involvement of DNA polymerase alpha in both processes. Biochem Biophys Res Commun 89: 218-225
6. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463: 1042-1047
7. Boiani M, Eckardt S, Scholer HR, McLaughlin KJ (2002) Oct4 distribution and level in mouse clones: consequences for plur-ipotency. Genes Dev 16: 1209-1219
8. Bouniol-Baly C, Nguyen E, Besombes D, Debey P (1997) Dynamic organization of DNA replication in one-cell mouse embryos: relationship to transcriptional activation. Exp Cell Res 236: 201-211
9. Bourc'his D, Proudhon C (2008) Sexual dimorphism in parental imprint ontogeny and contribution to embryonic development. Mol Cell Endocrinol 282: 87-94
10. Dantzer F, Nasheuer HP, Vonesch JL, de Murcia G, Menissier-de Murcia J (1998) Functional association of poly(ADP-ribose) polymerase with DNA polymerase alpha-primase complex: a link between DNA strand break detection and DNA replication. Nucleic Acids Res 26: 1891-1898
11. Derijck AA, van der Heijden GW, Giele M, Philippens ME, van Bavel CC, de Boer P (2006) gammaH2AX signalling during sperm chromatin remodelling in the mouse zygote. DNA Repair (Amst) 5: 959-971
12. Durkacz BW, Omidiji O, Gray DA, Shall S (1980) (ADP-ribose)n participates in DNA excision repair. Nature 283: 593-596
13. Engel N, Tront JS, Erinle T, Nguyen N, Latham KE, Sapienza C, Hoffman B, Liebermann DA (2009) Conserved DNA methylation in Gadd45a(\/\) mice. Epigenetics 4: 98-99
14. Farthing CR, Ficz G, Ng RK, Chan CF, Andrews S, Dean W, Hemberger M, Reik W (2008) Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet 4: e1000116
15. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004) H2AX: the histone guardian of the genome. DNA Repair (Amst) 3: 959-967
16. Ferreira J, Carmo-Fonseca M (1997) Genome replication in early mouse embryos follows a defined temporal and spatial order. J Cell Sci 110 (Pt 7): 889-897
17. Furuta T, Takemura H, Liao ZY, Aune GJ, Redon C, Sedelnikova OA, Pilch DR, Rogakou EP, Celeste A, Chen HT, Nussenzweig A, Aladjem MI, Bonner WM, Pommier Y (2003) Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 278: 20303-20312
18. Gehring M, Reik W, Henikoff S (2009) DNA demethylation by DNA repair. Trends Genet 25: 82-90
19. Godon C, Cordelieres FP, Biard D, Giocanti N, Megnin-Chanet F, Hall J, Favaudon V (2008) PARP inhibition versus PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res 36: 4454-4464
20. Hardeland U, Bentele M, Jiricny J, Schar P (2003) The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res 31: 2261-2271
21. Hayatsu H, Shiragami M (1979) Reaction of bisulfite with the 5-hydroxymethyl group in pyrimidines and in phage DNAs. Biochemistry 18: 632-637
22. Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, Rao A (2010) The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS One 5: e8888
23. Jin SG, Guo C, Pfeifer GP (2008) GADD45A does not promote DNA demethylation. PLoS Genet 4: e1000013
24. Kim SH, Kang YK, Koo DB, Kang MJ, Moon SJ, Lee KK, Han YM (2004) Differential DNA methylation reprogramming of various repetitive sequences in mouse preimplantation embryos. Biochem Biophys Res Commun 324: 58-63
25. Kriaucionis S, Heintz N (2009) The nuclear DNA base 5-hydroxy- methylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930
26. Krokan H, Wist E, Krokan RH (1981) Aphidicolin inhibits DNA synthesis by DNA polymerase alpha and isolated nuclei by a similar mechanism. Nucleic Acids Res 9: 4709-4719
27. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93
28. Lepikhov K, Walter J (2004) Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev Biol 4: 12
29. Liutkeviciute Z, Lukinavicius G, Masevicius V, Daujotyte D, Klimasauskas S (2009) Cytosine-5-methyltransferases add aldehydes to DNA. Nat Chem Biol 5: 400-402
30. Lundin C, North M, Erixon K, Walters K, Jenssen D, Goldman AS, Helleday T (2005) Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Res 33: 3799-3811
31. Malanga M, Althaus FR (2005) The role of poly(ADP-ribose) in the DNA damage signaling network. Biochem Cell Biol 83: 354-364
32. Matsumoto M, Yaginuma K, Igarashi A, Imura M, Hasegawa M, Iwabuchi K, Date T, Mori T, Ishizaki K, Yamashita K, Inobe M, Matsunaga T (2007) Perturbed gap-filling synthesis in nucleotide excision repair causes histone H2AX phosphorylation in human quiescent cells. J Cell Sci 120: 1104-1112
33. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T (2000) Demethylation of the zygotic paternal genome. Nature 403: 501-502
34. Morgan HD, Santos F, Green K, Dean W, Reik W (2005) Epigenetic reprogramming in mammals. Hum Mol Genet 14 Spec No 1: R47-R58
35. Nagy A (2003) Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
36. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M, Tanaka S, Shiota K, Nakano T (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9: 64-71
37. Okada Y, Yamagata K, Hong K, Wakayama T, Zhang Y (2010) A role for the elongator complex in zygotic paternal genome demethyl-ation. Nature 463: 554-558
38. Ooi SK, Bestor TH (2008) The colorful history of active DNA demethylation. Cell 133: 1145-1148
39. Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J (2000) Active demethylation of the paternal genome in the mouse zygote. Curr Biol 10: 475-478
40. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895
41. Ponferrada-Marin MI, Roldan-Arjona T, Ariza RR (2009) ROS1 5-methylcytosine DNA glycosylase is a slow-turnover catalyst that initiates DNA demethylation in a distributive fashion. Nucleic Acids Res 37: 4264-4274
42. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, Jacobsen SE, Reik W (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463: 1101-1105
43. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR (2008) DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135: 1201-1212
44. Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425-432
45. Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293: 1089-1093
46. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916
47. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphoryla-tion on serine 139. J Biol Chem 273: 5858-5868
48. Rougier N, Bourc'his D, Gomes DM, Niveleau A, Plachot M, Paldi A, Viegas-Pequignot E (1998) Chromosome methylation patterns during mammalian preimplantation development. Genes Dev 12: 2108-2113
49. Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127: 643-651
50. Santos F, Hendrich B, Reik W, Dean W (2002) Dynamic reprogram-ming of DNA methylation in the early mouse embryo. Dev Biol 241: 172-182
51. Sasaki H, Matsui Y (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9: 129-140
52. Schmitz KM, Schmitt N, Hoffmann-Rohrer U, Schafer A, Grummt I, Mayer C (2009) TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol Cell 33: 344-353
53. Sun QY, Schatten H (2007) Centrosome inheritance after fertilization and nuclear transfer in mammals. Adv Exp Med Biol 591: 58-71
54. Surani MA, Durcova-Hills G, Hajkova P, Hayashi K, Tee WW (2008) Germ line, stem cells, and epigenetic reprogramming. Cold Spring Harb Symp Quant Biol 73: 9-15
55. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by the MLL fusion partner TET1. Science 324: 930-935
56. Tierling S, Reither S, Walter J. Bisulfite sequencing of small DNA/cell samples http://www.epigenome-noe.net/researchtools/protocol.php?protid/14; 35, 12 Nov 2007
57. Ziegler-Birling C, Helmrich A, Tora L, Torres-Padilla ME (2009) Distribution of p53 binding protein 1 (53BP1) and phosphory-lated H2A.X during mouse preimplantation development in the absence of DNA damage. Int J Dev Biol 53: 1003-1011