Involvement of DOT1L in the remodeling of heterochromatin configuration during early preimplantation development in mice

Biology of Reproduction

Volumn 89, Issue 6, 2013, Pages

  Ooga, Masatoshi ^a   Suzuki, Masataka G ^a   Aoki, Fugaku ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Chromatin; DOT1L; Early development; Embryo; Epigenetics; H3K79 methylation; Heterochromatin; Histone modifications; Preimplantation embryo

Indexed keywords

DISRUPTOR OF TELOMERIC SILENCING 1; HISTONE H3; METHYLTRANSFERASE; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; ENZYME ACTIVITY; FEMALE; FERTILIZATION; HETEROCHROMATIN; HISTONE METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

CHROMATIN; DOT1L, EARLY DEVELOPMENT; EMBRYO; EPIGENETICS; H3K79 METHYLATION; HETEROCHROMATIN; HISTONE MODIFICATIONS; PREIMPLANTATION EMBRYO;

ANIMALS; BLASTOCYST; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLEAVAGE STAGE, OVUM; EMBRYONIC DEVELOPMENT; FEMALE; HEK293 CELLS; HETEROCHROMATIN; HUMANS; MALE; METHYLTRANSFERASES; MICE; MICE, INBRED C57BL; MICE, INBRED ICR;

EID: 84897984812     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.113258     Document Type: Article

References (44)

1. Yamagata K. Capturing epigenetic dynamics during pre-implantation development using live cell imaging. J Biochem 2008; 143:279-286.
2. Aguirre-Lavin T, Adenot P, Bonnet-Garnier A, Lehmann G, Fleurot R, Boulesteix C, Debey P, Beaujean N. 3D-FISH analysis of embryonic nuclei in mouse highlights several abrupt changes of nuclear organization during preimplantation development. BMC Dev Biol 2012; 12:30.
3. Probst AV, Santos F, Reik W, Almouzni G, Dean W. Structural differences in centromeric heterochromatin are spatially reconciled on fertilisation in the mouse zygote. Chromosoma 2007; 116:403-415.
4. Martin C, Beaujean N, Brochard V, Audouard C, Zink D, Debey P. Genome restructuring in mouse embryos during reprogramming and early development. Dev Biol 2006; 292:317-332.
5. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 2003; 13:1192-1200.
6. Santos F, Peters AH, Otte AP, Reik W, Dean W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol 2005; 280:225-236.
7. Bulut-Karslioglu A, Perrera V, Scaranaro M, de la Rosa-Velazquez IA, van de Nobelen S, Shukeir N, Popow J, Gerle B, Opravil S, Pagani M, Meidhof S, Brabletz T, et al. A transcription factor-based mechanism for mouse heterochromatin formation. Nat Struct Mol Biol 2012; 19: 1023-1030.
8. Martin C, Brochard V, Migne C, Zink D, Debey P, Beaujean N. Architectural reorganization of the nuclei upon transfer into oocytes accompanies genome reprogramming. Mol Reprod Dev 2006; 73: 1102-1111.
9. Cerda MC, Berrios S, Fernandez-Donoso R, Garagna S, Redi C. Organisation of complex nuclear domains in somatic mouse cells. Biol Cell 1999; 91:55-65.
10. Fadloun A, Eid A, Torres-Padilla ME. Mechanisms and dynamics of heterochromatin formation during mammalian development: closed paths and open questions. Curr Top Dev Biol 2013; 104:1-45.
11. Akiyama T, Suzuki O, Matsuda J, Aoki F. Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genet 2011; 7:e1002279.
12. Jones B, Su H, Bhat A, Lei H, Bajko J, Hevi S, Baltus GA, Kadam S, Zhai H, Valdez R, Gonzalo S, Zhang Y, et al. The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet 2008; 4:e1000190.
13. Nguyen AT, Zhang Y. The diverse functions of Dot1 and H3K79 methylation. Genes Dev 2011; 25:1345-1358.
14. van Leeuwen F, Gafken PR, Gottschling DE. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 2002; 109:745-756.
15. Shanower GA, Muller M, Blanton JL, Honti V, Gyurkovics H, Schedl P. Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 2005; 169:173-184.
16. Schubeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O'Neill LP, Turner BM, Delrow J, Bell SP, Groudine M. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 2004; 18:1263-1271.
17. Steger DJ, Lefterova MI, Ying L, Stonestrom AJ, Schupp M, Zhuo D, Vakoc AL, Kim JE, Chen J, Lazar MA, Blobel GA, Vakoc CR. DOT1L/ KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol Cell Biol 2008; 28: 2825-2839.
18. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008; 40:897-903.
19. Bitoun E, Oliver PL, Davies KE. The mixed-lineage leukemia fusion partner AF4 stimulates RNA polymerase II transcriptional elongation and mediates coordinated chromatin remodeling. Hum Mol Genet 2007; 16: 92-106.
20. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, Boateng MA, Dean K, Ryan OW, Golshani A, Johnston M, Greenblatt JF, Shilatifard A. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 2003; 11:721-729.
21. Kim SK, Jung I, Lee H, Kang K, Kim M, Jeong K, Kwon CS, Han YM, Kim YS, Kim D, Lee D. Human histone H3K79 methyltransferase DOT1L protein [corrected] binds actively transcribing RNA polymerase II to regulate gene expression. J Biol Chem 2012; 287:39698-39709.
22. Mohan M, Herz HM, Takahashi YH, Lin C, Lai KC, Zhang Y, Washburn MP, Florens L, Shilatifard A. Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev 2010; 24:574-589.
23. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, Mahowald M, Gottschling DE. Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 1998; 150: 613-632.
24. van Leeuwen F, Gottschling DE. Genome-wide histone modifications: gaining specificity by preventing promiscuity. Curr Opin Cell Biol 2002; 14:756-762.
25. Ooga M, Inoue A, Kageyama S, Akiyama T, Nagata M, Aoki F. Changes in H3K79 methylation during preimplantation development in mice. Biol Reprod 2008; 78:413-424.
26. Erbach GT, Lawitts JA, Papaioannou VE, Biggers JD. Differential growth of the mouse preimplantation embryo in chemically defined media. Biol Reprod 1994; 50:1027-1033.
27. Quinn P, Begley AJ. Effect of human seminal plasma and mouse accessory gland extracts on mouse fertilization in vitro. Aust J Biol Sci 1984; 37:147-152.
28. Zhang W, Hayashizaki Y, Kone BC. Structure and regulation of the mDot1 gene, a mouse histone H3 methyltransferase. Biochem J 2004; 377: 641-651.
29. Yamagata K, Yamazaki T, Yamashita M, Hara Y, Ogonuki N, Ogura A. Noninvasive visualization of molecular events in the mammalian zygote. Genesis 2005; 43:71-79.
30. Nashun B, Yukawa M, Liu H, Akiyama T, Aoki F. Changes in the nuclear deposition of histone H2A variants during pre-implantation development in mice. Development 2010; 137:3785-3794.
31. Inoue A, Aoki F. Role of the nucleoplasmin 2 C-terminal domain in the formation of nucleolus-like bodies in mouse oocytes. FASEB J 2010; 24: 485-494.
32. Moore GD, Ayabe T, Kopf GS, Schultz RM. Temporal patterns of gene expression of G1-S cyclins and cdks during the first and second mitotic cell cycles in mouse embryos. Mol Reprod Dev 1996; 45:264-275.
33. Reisenauer MR, Anderson M, Huang L, Zhang Z, Zhou Q, Kone BC, Morris AP, Lesage GD, Dryer SE, Zhang W. AF17 competes with AF9 for binding to Dot1a to up-regulate transcription of epithelial Na{Thorn} channel alpha. J Biol Chem 2009; 284:35659-35669.
34. Reisenauer MR, Wang SW, Xia Y, Zhang W. Dot1a contains three nuclear localization signals and regulates the epithelial Na{Thorn} channel (ENaC) at multiple levels. Am J Physiol Renal Physiol 2010; 299:F63-F76.
35. Min J, Feng Q, Li Z, Zhang Y, Xu RM. Structure of the catalytic domain of human DOT1L, a non-SET domain nucleosomal histone methyltransferase. Cell 2003; 112:711-723.
36. Maalouf WE, Liu Z, Brochard V, Renard JP, Debey P, Beaujean N, Zink D. Trichostatin A treatment of cloned mouse embryos improves constitutive heterochromatin remodeling as well as developmental potential to term. BMC Dev Biol 2009; 9:11.
37. Rybouchkin A, Kato Y, Tsunoda Y. Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biol Reprod 2006; 74:1083-1089.
38. Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui HT, Wakayama T. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun 2006; 340:183-189.
39. Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, Bernt KM, Cahan P, Marcarci BO, Unternaehrer J, Gupta PB, Lander ES, Armstrong SA, et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 2012; 483:598-602.
40. Stulemeijer IJ, Pike BL, Faber AW, Verzijlbergen KF, van Welsem T, Frederiks F, Lenstra TL, Holstege FC, Gasser SM, van Leeuwen F. Dot1 binding induces chromatin rearrangements by histone methylationdependent and-independent mechanisms. Epigenet Chromatin 2011; 4:2.
41. Abe K, Inoue A, Suzuki MG, Aoki F. Global gene silencing is caused by the dissociation of RNA polymerase II from DNA in mouse oocytes. J Reprod Dev 2010; 56:502-507.
42. Ng HH, Xu RM, Zhang Y, Struhl K. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 2002; 277:34655-34657.
43. Briggs SD, Xiao T, Sun ZW, Caldwell JA, Shabanowitz J, Hunt DF, Allis CD, Strahl BD. Gene silencing: trans-histone regulatory pathway in chromatin. Nature 2002; 418:498.
44. Shahbazian MD, Zhang K, Grunstein M. Histone H2B ubiquitylation controls processive methylation but not monomethylation by Dot1 and Set1. Mol Cell 2005; 19:271-277.