Evaluation of epigenetic marks in human embryos derived from IVF and ICSI

Human Reproduction

Volumn 25, Issue 9, 2010, Pages 2387-2395

  Santos, Fátima ^a   Hyslop, Louise ^b,c   Stojkovic, Petra ^c,e,h   Leary, Christine ^c,g   Murdoch, Alison ^b,c   Reik, Wolf ^a,f   Stojkovic, Miodrag ^c,e,h   Herbert, Mary ^b,c,d   Dean, Wendy ^a  

^a Laboratory of Molecular Signalling   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c Newcastle upon Tyne Hospitals NHS Trust   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e Spebo Medical ^*  (Serbia)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g HULL ROYAL INFIRMARY   (United Kingdom)

^h UNIVERSITY OF KRAGUJEVAC   (Serbia)

Author keywords

DNA methylation; epigenetics; human embryos; ICSI; IVF

Indexed keywords

ARTICLE; BLASTOCYST; BLASTOMERE; CHROMATIN; DNA METHYLATION; EMBRYO; EMBRYO TRANSFER; EPIGENETICS; FERTILIZATION IN VITRO; GENE EXPRESSION; GENE SEQUENCE; GENOME; GENOTYPE; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; NIDATION; ZYGOTE;

EID: 77955928920     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deq151     Document Type: Article

References (53)

1. Amor DJ, Halliday J. A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum Reprod 2008;23:2826-2834.
2. Barker DJ. Developmental origins of adult health and disease. J Epidemiol Community Health 2004;58:114-115.
3. Beaujean N, Hartshorne G, Cavilla J, Taylor J, Gardner J, Wilmut I, Meehan R, Young L. Non-conservation of mammalian preimplantation methylation dynamics. Curr Biol 2004;14:R266-R267.
4. Borghol N, Lornage J, Blachere T, Sophie Garret A, Lefevre A. Epigenetic status of the H19 locus in human oocytes following in vitro maturation. Genomics 2006;87:417-426.
5. Bowdin S, Allen C, Kirby G, Brueton L, Afnan M, Barratt C, Kirkman-Brown J, Harrison R, Maher ER, Reardon W. A survey of assisted reproductive technology births and imprinting disorders. Hum Reprod 2007;22:3237-3240.
6. Chian RC, Lim JH, Tan SL. State of the art in in-vitro oocyte maturation. Curr Opin Obstet Gynecol 2004;16:211-219.
7. Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, Horsthemke B. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet 2002;71:162-164.
8. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 2000; 9:2885-2894.
9. Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA 2001;98:13734-13738.
10. 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.
11. De Mouzon J, Lancaster P, Nygren KG, Sullivan E, Zegers-Hochschild F, Mansour R, Ishihara O, Adamson D. World collaborative report on assisted reproductive technology, 2002. Hum Reprod 2009; 24:2310-2320.
12. Doornbos ME, Maas SM, McDonnell J, Vermeiden JP, Hennekam RC. Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Hum Reprod 2007;22:2476-2480.
13. Fortier AL, Lopes FL, Darricarrere N, Martel J, Trasler JM. Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Hum Mol Genet 2008;17:1653-1665.
14. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T. The methyl-CpG-binding protein MeCP2 Links DNA methylation to histone methylation. J Biol Chem 2003;278:4035-4040.
15. Fulka H, Mrazek M, Tepla O, Fulka J Jr. DNA methylation pattern in human zygotes and developing embryos. Reproduction 2004;128:703-708.
16. Gardner DK, Schoolcraft WB. In vitro culture of human blastocysts. In: Jansen R, Mortimer D (ed)., Towards Reproductive Certainty: Infertility and Genetics Beyond 1999. Carnforth: Parthenon Press, 1999.
17. 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.
18. Gomes MV, Huber J, Ferriani RA, Amaral Neto AM, Ramos ES. Abnormal methylation at the KvDMR1 imprinting control region in clinically normal children conceived by assisted reproductive technologies. Mol Hum Reprod 2009;15:471-477.
19. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani M. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002;117:15.
20. Halliday J, Oke K, Breheny S, Algar E, David JA. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet 2004; 75:526-528.
21. Hemberger M, Dean W, Reik W. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat Rev Mol Cell Biol 2009;10:526-537.
22. Hiendleder S, Wirtz M, Mund C, Klempt M, Reichenbach HD, Stojkovic M, Weppert M, Wenigerkind H, Elmlinger M, Lyko F et al. Tissue-specific effects of in vitro fertilization procedures on genomic cytosine methylation levels in overgrown and normal sized bovine fetuses. Biol Reprod 2006;75:17-23.
23. Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, Jacobsen SE. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 2004;112:308-315.
24. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293:1074-1080.
25. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007;8:253-262.
26. Khosla S, Dean W, Reik W, Feil R. Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Update 2001;7:419-427.
27. Li JY, Lees-Murdock DJ, Xu GL, Walsh CP. Timing of establishment of paternal methylation imprints in the mouse. Genomics 2004; 84:952-960.
28. Lucifero D, Chaillet JR, Trasler JM. Potential significance of genomic imprinting defects for reproduction and assisted reproductive technology. Hum Reprod Update 2004a;10:3-18.
29. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004b; 13:839-849.
30. Maatouk DM, Kellam LD, Mann MR, Lei H, Li E, Bartolomei MS, Resnick JL. DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 2006;133:3411-3418.
31. Maher ER, Afnan M, Barratt CL. Epigenetic risks related to assisted reproductive technologies: epigenetics, imprinting, ART and icebergs? Hum Reprod 2003;18:2508-2511.
32. Manipalviratn S, DeCherney A, Segars J. Imprinting disorders and assisted reproductive technology. Fertil Steril 2009;91:305-315.
33. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, Bartolomei MS. Selective loss of imprinting in the placenta following preimplantation development in culture. Development 2004; 131:3727-3735.
34. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet 2009; 19:36-51.
35. Moll AC, Imhof SM, Cruysberg JR, Schouten-van Meeteren AY, Boers M, Van Leeuwen FE. Incidence of retinoblastoma in children born after in vitro fertilisation. Lancet 2003;361:309-310.
36. Monk M, Boubelik M, Lehnert S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 1987; 99:371-382.
37. Morgan HD, Jin XL, Li A, Whitelaw E, O'Neill C. The culture of zygotes to the blastocyst stage changes the postnatal expression of an epigentically labile allele, agouti viable yellow, in mice. Biol Reprod 2008;79:618-623.
38. Niemitz EL, Feinberg AP. Epigenetics and assisted reproductive technology: a call for investigation. Am J Hum Genet 2004;74:599-609.
39. Orstavik KH, Eiklid K, Van Der Hagen CB, Spetalen S, Kierulf K, Skjeldal O, Buiting K. Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am J Hum Genet 2003;72:218-219.
40. Palermo GD, Neri QV, Takeuchi T, Rosenwaks Z. ICSI: where we have been and where we are going. Semin Reprod Med 2009;27:191-201.
41. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001;2:21-32.
42. Rivera RM, Stein P, Weaver JR, Mager J, Schultz RM, Bartolomei MS. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet 2008;17:1-14.
43. Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002;241:172-182.
44. Santos F, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 2003; 13:1116-1121.
45. 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.
46. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008;9:129-140.
47. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
48. Shovlin TC, Durcova-Hills G, Surani A, McLaren A. Heterogeneity in imprinted methylation patterns of pluripotent embryonic germ cells derived from pre-migratory mouse germ cells. Dev Biol 2008;313:674-681.
49. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403:41-45.
50. Tamaru H, Selker EU. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 2001;414:277-283.
51. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 2003; 34:75-79.
52. Whitelaw NC, Whitelaw E. Transgenerational epigenetic inheritance in health and disease. Curr Opin Genet Dev 2008;18:273-279.
53. Young LE, Beaujean N. DNA methylation in the preimplantation embryo: the differing stories of the mouse and sheep. Anim Reprod Sci 2004; 82-83:61-78.