DNA methyltransferase 1o functions during preimplantation development to preclude a profound level of epigenetic variation

Developmental Biology

Volumn 324, Issue 1, 2008, Pages 139-150

  Cirio, M Cecilia ^a   Martel, Josee ^b   Mann, Mellissa ^c   Toppings, Marc ^b   Bartolomei, Marisa ^c   Trasler, Jacquetta ^b   Chaillet, J Richard ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b MONTREAL CHILDREN S HOSPITAL   (Canada)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

DNA methylation; DNA methyltransferase; Embryogenesis; Epigenetics; Imprinting

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 1O; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; DNA METHYLATION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ANALYSIS; EPIGENETICS; GENOME IMPRINTING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN FUNCTION;

EID: 56049114840     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.09.015     Document Type: Article

References (43)

1. Boonen S.E., Porksen S., Mackay D.J., Oestergaard E., Olsen B., Brondum-Nielsen K., Temple I.K., and Hahnemann J.M. Clinical characterisation of the multiple maternal hypomethylation syndrome in siblings. Eur. J. Hum. Genet. 16 (2008) 453-461
2. Bourc'his D., Xu G.L., Lin C.S., Bollman B., and Bestor T.H. Dnmt3L and the establishment of maternal genomic imprints. Science 294 (2001) 2536-2539
3. Brandeis M., Kafri T., Ariel M., Chaillet J.R., McCarrey J., Razin A., and Cedar H. The ontogeny of allele-specific methylation associated with imprinted genes in the mouse. EMBO J. 12 (1993) 3669-3677
4. Cardoso M.C., and Leonhardt H. DNA methyltransferase is actively retained in the cytoplasm during early development. J. Cell Biol. 147 (1999) 25-32
5. Carlson L.L., Page A.W., and Bestor T.H. Properties and localization of DNA methyltransferase in preimplantation mouse embryos: implications for genomic imprinting. Genes Dev. 6 (1992) 2536-2541
6. Carr M.S., Yevtodiyenko A., Schmidt C.L., and Schmidt J.V. Allele-specific histone modifications regulate expression of the Dlk1-Gtl2 imprinted domain. Genomics 89 (2007) 280-290
7. Cattanach B.M., and Kirk M. Differential activity of maternally and paternally derived chromosome regions in mice. Nature 315 (1985) 496-498
8. Chung Y.G., Ratnam S., Chaillet J.R., and Latham K.E. Abnormal regulation of DNA methyltransferase expression in cloned mouse embryos. Biol. Reprod. 69 (2003) 146-153
9. Cirio M.C., Ratnam S., Ding F., Reinhart B., Navara C., and Chaillet J.R. Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints. BMC Dev. Biol. 8 (2008) 9
10. Clarke H.J., Oblin C., and Bustin M. Developmental regulation of chromatin composition during mouse embryogenesis: somatic histone H1 is first detectable at the 4-cell stage. Development 115 (1992) 791-799
11. Davis T.L., Tremblay K.D., and Bartolomei M.S. Imprinted expression and methylation of the mouse H19 gene are conserved in extraembryonic lineages. Dev. Genet. 23 (1998) 111-118
12. DeBaun M.R., Niemitz E.L., and Feinberg A.P. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am. J. Hum. Genet. 72 (2003) 156-160
13. Delaval K., Govin J., Cerqueira F., Rousseaux S., Khochbin S., and Feil R. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. Embo J. 26 (2007) 720-729
14. Doherty A.S., Mann M.R., Tremblay K.D., Bartolomei M.S., and Schultz R.M. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62 (2000) 1526-1535
15. Doherty A.S., Bartolomei M.S., and Schultz R.M. Regulation of stage-specific nuclear translocation of Dnmt1o during preimplantation mouse development. Dev. Biol. 242 (2002) 255-266
16. Fleming T.P., Sheth B., and Fesenko I. Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci. 6 (2001) D1000-D1007
17. Hata K., Okano M., Lei H., and Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129 (2002) 1983-1993
18. Hirasawa R., Chiba H., Kaneda M., Tajima S., Li E., Jaenisch R., and Sasaki H. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 22 (2008) 1607-1616
19. Howell C.Y., Bestor T.H., Ding F., Latham K.E., Mertineit C., Trasler J.M., and Chaillet J.R. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104 (2001) 829-838
20. Kaneda M., Okano M., Hata K., Sado T., Tsujimoto N., Li E., and Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429 (2004) 900-903
21. Khosla S., Dean W., Brown D., Reik W., and Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol. Reprod. 64 (2001) 918-926
22. Lewis A., Mitsuya K., Umlauf D., Smith P., Dean W., Walter J., Higgins M., Feil R., and Reik W. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36 (2004) 1291-1295
23. Liu H., Kim J.M., and Aoki F. Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131 (2004) 2269-2280
24. Lucifero D., Mertineit C., Clarke H.J., Bestor T.H., and Trasler J.M. Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79 (2002) 530-538
25. Mann M.R., Chung Y.G., Nolen L.D., Verona R.I., Latham K.E., and Bartolomei M.S. Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol. Reprod. 69 (2003) 902-914
26. McGrath J., and Solter D. Inability of mouse blastomere nuclei transferred to enucleated zygotes to support development in vitro. Science 226 (1984) 1317-1319
27. Murrell A., Heeson S., and Reik W. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet. 36 (2004) 889-893
28. Nagy A., Gertsenstein M., Vinterstern K., and Behringer R. Manipulation of Mouse Embryos: A Laboratory Manual (2003), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York 380-387
29. Norris M.L., Barton S.C., and Surani M.A. The differential roles of parental genomes in mammalian development. Oxf. Rev. Reprod. Biol. 12 (1990) 225-244
30. Pratt H.P., Ziomek C.A., Reeve W.J., and Johnson M.H. Compaction of the mouse embryo: an analysis of its components. J. Embryol. Exp. Morphol. 70 (1982) 113-132
31. Ratnam S., Mertineit C., Ding F., Howell C.Y., Clarke H.J., Bestor T.H., Chaillet J.R., and Trasler J.M. Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev. Biol. 245 (2002) 304-314
32. Reeve W.J., and Ziomek C.A. Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J. Embryol. Exp. Morphol. 62 (1981) 339-350
33. Reinhart B., Eljanne M., and Chaillet J.R. Shared role for differentially methylated domains of imprinted genes. Mol. Cell. Biol. 22 (2002) 2089-2098
34. Reinhart B., Paoloni-Giacobino A., and Chaillet J.R. Specific differentially methylated domain sequences direct the maintenance of methylation at imprinted genes. Mol. Cell. Biol. 26 (2006) 8347-8356
35. Santos F., Peters A.H., Otte A.P., Reik W., and Dean W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280 (2005) 225-236
36. Shemer R., Birger Y., Riggs A.D., and Razin A. Structure of the imprinted mouse Snrpn gene and establishment of its parental-specific methylation pattern. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10267-10272
37. Shi W., Krella A., Orth A., Yu Y., and Fundele R. Widespread disruption of genomic imprinting in adult interspecies mouse (Mus) hybrids. Genesis 43 (2005) 100-108
38. Surani M.A., Barton S.C., and Norris M.L. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308 (1984) 548-550
39. Toppings M., Castro C., Mills P.H., Reinhart B., Schatten G., Ahrens E.T., Chaillet J.R., and Trasler J.M. Profound phenotypic variation among mice deficient in the maintenance of genomic imprints. Hum. Reprod. 23 (2008) 807-818
40. Tremblay K.D., Duran K.L., and Bartolomei M.S. A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell. Biol. 17 (1997) 4322-4329
41. Tremblay K.D., Saam J.R., Ingram R.S., Tilghman S.M., and Bartolomei M.S. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9 (1995) 407-413
42. Verona R.I., Thorvaldsen J.L., Reese K.J., and Bartolomei M.S. The transcriptional status but not the imprinting control region determines allele-specific histone modifications at the imprinted H19 locus. Mol. Cell. Biol. 28 (2008) 71-82
43. Yang Y., Li T., Vu T.H., Ulaner G.A., Hu J.F., and Hoffman A.R. The histone code regulating expression of the imprinted mouse Igf2r gene. Endocrinology 144 (2003) 5658-5670