Dynamics of imprinted DNA methylation and gene transcription for imprinting establishment in mouse oocytes in relation to culture duration variability

Biology of Reproduction

Volumn 89, Issue 6, 2013, Pages

  Anckaert, Ellen ^a   Sánchez, Flor ^a   Billooye, Katy ^a   Smitz, Johan ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

DNA methylation; Follicle culture; Genomic imprinting; Oocyte maturation; Total mRNA

Indexed keywords

COMPLEMENTARY DNA; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3L; MESSENGER RNA; METHYLTRANSFERASE; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; UNCLASSIFIED DRUG; ZFP57 PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CULTURAL ANTHROPOLOGY; CUMULUS CELL; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOME IMPRINTING; IN VITRO STUDY; MARKER GENE; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION;

DNA METHYLATION; FOLLICLE CULTURE; GENOMIC IMPRINTING; OOCYTE MATURATION; TOTAL MRNA;

ANIMALS; CELLS, CULTURED; DNA METHYLATION; FEMALE; GENOMIC IMPRINTING; IN VITRO OOCYTE MATURATION TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; OOCYTES; OOGENESIS; PROTEINS; SNRNP CORE PROTEINS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84901273123     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.111641     Document Type: Article

References (42)

1. Smitz JEJ, Thompson JG, Gilchrist RB. The promise of in vitro maturation in assisted reproduction and fertility. Semin Reprod Med 2011; 29:24-37.
2. Xu M, Barrett SL, West-Farrell E, Kondapalli LA, Kiesewetter SE, Shea LD, Woodruff TK. In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum Reprod 2009; 24:2531-2540.
3. Smitz J, Dolmans MM, Donnez J, Fortune JE, Hovatta O, Jewgenow K, Picton HM, Plancha C, Shea LD, Stouffer RL, Telfer EE, Woodruff TK, et al. Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum Reprod Update 2010; 16:395-414.
4. Denomme MM, Mann MR. Genomic imprints as a model for the analysis of epigenetic stability during assisted reproductive technologies. Reproduction 2012; 144:393-409.
5. DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet 2003; 72:156-160.
6. Gicquel C, Gaston V, Mandelbaum J, Siffroi JP, Flahault A, Le Bouc Y. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am J Hum Genet 2003; 72:1338-1341.
7. Maher ER, Afnan M, Barratt CL. Epigenetic risks related to assisted reproductive technologies: epigenetics, imprinting, ART and icebergs? Hum Reprod 2003; 18:2508-2511.
8. Halliday J, Oke K, Breheny S, Algar E, Amor DJ. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet 2004; 75: 526-528.
9. Chang AS, Moley KH, Wangler M, Feinberg AP, Debaun MR. Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients. Fertil Steril 2005; 83:349-354.
10. Rossignol S, Steunou V, Chalas C, Kerjean A, Rigolet M, Viegas-Pequignot E, Jouannet P, Le Bouc Y, Gicquel C. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region. J Med Genet 2006; 43:902-907.
11. Sutcliffe AG, Peters CJ, Bowdin S, Temple K, Reardon W, Wilson L, Clayton-Smith J, Brueton LA, Bannister W, Maher ER. Assisted reproductive therapies and imprinting disorders: a preliminary British survey. Hum Reprod 2006; 21:1009-1011.
12. Bowdin S, Brueton L, Allen C, Harrison R, Kirby G, Maher ER, Afnan M, Kirkman-Brown J, Barratt C, Reardon W. A survey of assisted reproductive technology births and imprinting disorders. Hum Reprod 2007; 22:3237-3240.
13. Gomes MV, Gomes CC, Pinto W Jr, Ramos ES. Methylation pattern at the KvDMR in a child with Beckwith-Wiedemann syndrome conceived by ICSI. Am J Med Genet 2007; 143:625-629.
14. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001; 2:21-32.
15. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002; 3:662-673.
16. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004; 13: 839-849.
17. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. Oocyte growthdependent progression of maternal imprinting in mice. Genes Cells 2006; 11:353-361.
18. Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM, Chaillet JR. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 2001; 104:829-838.
19. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M, Tanaka S, Shiota K, et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 2007; 9:64-71.
20. Reese KJ, Lin S, Verona RI, Schultz RM, Bartolomei MS. Maintenance of paternal methylation and repression of the imprinted H19 gene requires MBD3. PLoS Genet 2007; 3:e137.
21. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P, Ferguson-Smith AC. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev Cell 2008; 15:547-557.
22. Anckaert E, De Rycke M, Smitz J. Culture of oocytes and risk of imprinting defects. Hum Reprod Update 2013; 19:52-66.
23. Anckaert E, Adriaenssens T, Romero S, Dremier S, Smitz J. Unaltered imprinting establishment of key imprinted genes in mouse oocytes after in vitro follicle culture under variable follicle-stimulating hormone exposure. Int J Dev Biol 2009; 53:541-548.
24. Anckaert E, Adriaenssens T, Romero S, Smitz J. Ammonium accumulation and use of mineral oil overlay do not alter imprinting establishment at three key imprinted genes in mouse oocytes grown and matured in a long-term follicle culture. Biol Reprod 2009; 81:666-673.
25. Anckaert E, Romero S, Adriaenssens T, Smitz J. Effects of low methyl donor levels in culture medium during mouse follicle culture on oocyte imprinting establishment. Biol Reprod 2010; 83:377-386.
26. Cortvrindt R, Smitz J. Follicle culture in reproductive toxicology: a tool for in-vitro testing of ovarian function. Hum Reprod Update 2002; 8:1-12.
27. Segers I, Adriaenssens T, Ozturk E, Smitz J. Acquisition and loss of oocyte meiotic and developmental competence during in vitro antral follicle growth in mouse. Fertil Steril 2010; 93:2695-2700.
28. Cortvrindt RG, Hu Y, Liu J, Smitz JE. Timed analysis of the nuclear maturation of oocytes in early preantral mouse follicle culture supplemented with recombinant gonadotropin. Fertil Steril 1998; 70:1114-1125.
29. Sánchez F, Adriaenssens T, Romero S, Smitz J. Quantification of oocytespecific transcripts in follicle-enclosed oocytes during antral development and maturation in vitro. Mol Hum Reprod 2009; 15:539-550.
30. Imamura T, Kerjean A, Heams T, Kupiec JJ, Thenevin C, Paldi A. Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo. J Biol Chem 2005; 280: 20171-20175.
31. Liang XW, Zhu JQ, Miao YL, Liu JH, Wei L, Lu SS, Hou Y, Schatten H, Lu KH, Sun QY. Loss of methylation imprint of Snrpn in postovulatory aging mouse oocyte. Biochem Biophys Res Commun 2008; 371:16-21.
32. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science 2001; 294: 2536-2539.
33. Hata K, Okano M, Lei H, Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002; 129:1983-1993.
34. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004; 429:900-903.
35. Trapphoff T, El Hajj N, Zechner U, Haaf T, Eichenlaub-Ritter U. DNA integrity, growth pattern, spindle formation, chromosomal constitution and imprinting patterns of mouse oocytes from vitrified pre-antral follicles. Hum Reprod 2010; 25:3025-3042.
36. Han W, Cauchi S, Herman JG, Spivack SD. DNA methylation mapping by tag-modified bisulfite genomic sequencing. Anal Biochem 2006; 355: 50-61.
37. Heinzmann J, Hansmann T, Herrmann D, Wrenzycki C, Zechner U, Haaf T, Niemann H. Epigenetic profile of developmentally important genes in bovine oocytes. Mol Reprod Dev 2011; 78:188-201.
38. Warnecke PM, Stirzaker C, Song J, Grunau C, Melki JR, Clark SJ. Identification and resolution of artifacts in bisulfite sequencing. Methods 2002; 27:101-107.
39. Guzman L, Ortega-Hrepich C, Albuz FK, Verheyen G, Devroey P, Smitz J, De Vos M. Developmental capacity of in vitro-matured human oocytes retrieved from polycystic ovary syndrome ovaries containing no follicles larger than 6 mm. Fertil Steril 2012; 98:503-507.
40. Bachvarova R. Gene expression during oogenesis and oocyte development in mammals. Dev Biol (N Y 1985) 1985; 1:453-524.
41. De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, Eppig JJ. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol 2004; 275: 447-458.
42. Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, Eppig JJ. Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev Biol 2007; 302:104-117.