Epigenetics and Human Assisted Reproduction

John Huntriss

doi:10.1017/9781108611633.016

Chapter 15 - Epigenetics and Human Assisted Reproduction

Published online by Cambridge University Press: 24 December 2019

Kay Elder and

Brian Dale

John Huntriss

Show author details

Kay Elder: Affiliation:
Bourn Hall Clinic, Cambridge
Brian Dale: Affiliation:
Centre for Assisted Reproduction, Naples

Book contents

Get access

Summary

During mammalian development the growth of the fetus is regulated by genetic information that is inherited from both the sperm and the oocyte. Apart from the clear differences that are associated with the X and Y chromosomes, the parental genetic contributions to the embryo also differ via a system of ‘epigenetic’ marks. The differences in function between the parental genomes, how gametes and preimplantation embryos are reprogrammed, and how these delicate processes may be affected by ART and infertility will be described in this chapter. A full understanding of the cellular and molecular biology of human reproduction must include a study of epigenetics and genomic imprinting.

Type: Chapter
Information: In-Vitro Fertilization , pp. 331 - 357

DOI: https://doi.org/10.1017/9781108611633.016 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Primary Sources

Amor, DJ, Halliday, J (2008) A review of known imprinting syndromes and their association with assisted reproduction technologies. Human Reproduction 23(12): 2826–2834.CrossRef Google Scholar PubMed

ASRM Practice Committee Pages (2013) Blastocyst culture and transfer in clinical assisted reproduction: a committee opinion. Fertility and Sterility 99(3): 0015–0282.Google Scholar

Gosden, R, Trasler, J, Lucifero, D, Faddy, M (2003) Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 361(9373): 1975–1977.CrossRef Google Scholar PubMed

Huntriss, J, Picton, HM (2008) Epigenetic consequences of assisted reproduction and infertility on the human preimplantation embryo. Human Fertility 11(2): 85–94.CrossRef Google Scholar PubMed

Maher, ER, Afnan, M, Barratt, CL (2003) Epigenetic risks related to assisted reproductive technologies: epigenetics, imprinting, ART and icebergs? Human Reproduction 18(12): 2508–2511.Google Scholar

Manipalviratn, S, DeCherney, A, Segars, J (2009) Imprinting disorders and assisted reproductive technology. Fertility and Sterility 91(2): 305–315.CrossRef Google Scholar PubMed

Roseboom, TJ (2018) Developmental plasticity and its relevance to assisted human reproduction. Human Reproduction 33(4): 546–552.Google Scholar

Secondary Sources

Abeyta, MJ, Clark, AT, Rodriguez, RT, et al. (2004) Unique gene expression signatures of independently-derived human embryonic stem cell lines. Human Molecular Genetics 13: 601–608.CrossRef Google Scholar PubMed

Adewumi, O, Aflatoonian, B, Ahrlund-Richter, L, et al. (2007) Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nature Biotechnology 25: 803–816.Google Scholar

Albert, M, Peters, AH (2009) Genetic and epigenetic control of early mouse development. Current Opinion in Genetics and Development 19(2): 113–121.Google Scholar

Allegrucci, C, Wu, YZ, Thurston, A, et al. (2007) Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Human Molecular Genetics 16: 1253–1268.Google Scholar

Anckaert, E, Adriaenssens, T, Romero, S, Dremier, S, Smitz, J (2009a) Unaltered imprinting establishment of key imprinted genes in mouse oocytes after in vitro follicle culture under variable follicle-stimulating hormone exposure. International Journal of Developmental Biology 53(4): 541–548.CrossRef Google Scholar PubMed

Anckaert, E, Adriaenssens, T, Romero, S, Smitz, J (2009b) 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. Biology of Reproduction 81(4): 666–673.Google Scholar

Anteby, I, Cohen, E, Anteby, E, BenEzra, D (2001) Ocular manifestations in children born after in vitro fertilization. Archives of Ophthalmology 119(10): 1525–1529.CrossRef Google Scholar PubMed

Aoki, VW, Emery, BR, Liu, L, Carrell, DT (2006a) Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. Journal of Andrology 27: 890–898.CrossRef Google Scholar PubMed

Aoki, VW, Liu, L, Jones, KP, et al. (2006b) Sperm protamine 1/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertility and Sterility 86: 1408–1415.CrossRef Google Scholar PubMed

Aoki, VW, Moskovtsev, SI, Willis, J, et al. (2005) DNA integrity is compromised in protamine-deficient human sperm. Journal of Andrology 26: 741–748.Google Scholar

Apostolidou, S, Abu-Amero, S, O’Donoghue, K, et al. (2007) Elevated placental expression of the imprinted PHLDA2 gene is associated with low birth weight. Journal of Molecular Medicine 85: 379–387.CrossRef Google Scholar PubMed

Aravin, AA, Hannon, GJ (2008) Small RNA silencing pathways in germ and stem cells. Cold Spring Harbor Symposia on Quantitative Biology 73: 283–290.CrossRef Google Scholar PubMed

Aston, KI, Carrell, DT (2014) Prospects for clinically relevant epigenetic tests in the andrology laboratory. Asian Journal of Andrology 16(5): 782.CrossRef Google Scholar PubMed

Batcheller, A, Cardozo, E, Maguire, M, DeCherney, AH, Segars, JH (2011) Are there subtle genome-wide epigenetic alterations in normal offspring conceived by assisted reproductive technologies? Fertility and Sterility 96(6):1306–1311.Google Scholar

Beaujean, N, Hartshorne, G, Cavilla, J, et al. (2004) Non-conservation of mammalian preimplantation methylation dynamics. Current Biology 14(7): R266–267.CrossRef Google Scholar PubMed

Bell, AC, Felsenfeld, G (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405(6785): 482–485.Google Scholar

Benchaib, M, Braun, V, Ressnikof, D, et al. (2005) Influence of global sperm DNA methylation on IVF results. Human Reproduction 20: 768–773.Google Scholar

Bliek, J, Terhal, P, van den Bogaard, MJ, et al. (2006) Hypomethylation of the H19 gene causes not only Silver–Russell syndrome (SRS) but also isolated asymmetry or an SRS-like phenotype. American Journal of Human Genetics 78: 604–614.CrossRef Google Scholar

Blondin, P, Farin, PW, Crosier, AE, Alexander, JE, Farin, CE (2000) In vitro production of embryos alters levels of insulin-like growth factor-II messenger ribonucleic acid in bovine fetuses 63 days after transfer. Biology and Reproduction 62(2): 384–389.Google Scholar

Boissonnas, CC, Abdalaoui, HE, Haelewyn, V, et al. (2010) Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. European Journal of Human Genetics 18(1): 73–80.Google Scholar

Boissonnas, CC, Jouannet, P, Jammes, H (2013). Epigenetic disorders and male subfertility. Fertility and Sterility 99(3): 624–631.CrossRef Google Scholar PubMed

Boonen, SE, Porksen, S, Mackay, DJ, et al. (2008) Clinical characterisation of the multiple maternal hypomethylation syndrome in siblings. European Journal of Human Genetics 16: 453–461.CrossRef Google Scholar PubMed

Borghol, N, Blachère, T, Lefèvre, A (2008) Transcriptional and epigenetic status of protamine 1 and 2 genes following round spermatid injection into mouse oocytes. Genomics 91(5): 415–422.CrossRef Google Scholar PubMed

Borghol, N, Lornage, J, Blachere, T, Sophie Garret, A, Lefevre, A (2006) Epigenetic status of the H19 locus in human oocytes following in vitro maturation. Genomics 87: 417–426.CrossRef Google Scholar PubMed

Bourc’his, D, Xu, GL, Lin, CS, Bollman, B, Bestor, TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294(5551): 2536–2539.Google Scholar

Bourque, DK, Avila, L, Peñaherrera, M, von Dadelszen, P, Robinson, WP (2010) Decreased placental methylation at the H19/IGF2 imprinting control region is associated with normotensive intrauterine growth restriction but not preeclampsia. Placenta 31(3): 197–202.CrossRef Google Scholar

Camprubi, C, Iglesias-Platas, I, Martin-Trujillo, A, et al. (2013) Stability of genomic imprinting and gestational-age dynamic methylation in complicated pregnancies conceived following assisted reproductive technologies. Biology of Reproduction 89(3): 50.Google Scholar

Carlone, DL, Lee, JH, Young, SR, et al. (2005) Reduced genomic cytosine methylation and defective cellular differentiation in embryonic stem cells lacking CpG binding protein. Molecular and Cellular Biology 25(12): 4881–4891.Google Scholar

Carlone, DL, Skalnik, DG (2001) CpG binding protein is crucial for early embryonic development. Molecular and Cellular Biology 21(22): 7601–7606.Google Scholar

Carrasco, B, Boada, M, Rodriguez, I, Coroleu, B, Barri, PN, Veiga, A (2013) Does culture medium influence offspring birth weight? Fertility and Sterility 100(5): 1283–1288.Google Scholar

Carrell, DT (2012) Epigenetics of the male gamete. Fertility and Sterility 97(2): 267–274.Google Scholar

Carrell, DT, Emery, BR, Hammoud, S (2007) Altered protamine expression and diminished spermatogenesis: what is the link? Human Reproduction Update 13: 313–327.Google Scholar

Cetin, I, Cozzi, V, Antonazzo, P (2003) Fetal development after assisted reproduction – a review. Placenta 24(Suppl. B): S104–113.CrossRef Google Scholar PubMed

Chang, AS, Moley, KH, Wangler, M, Feinberg, AP, Debaun, MR (2005) Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients. Fertility and Sterility 83: 349–354.Google Scholar

Charalambous, M, Ferron, SR, da Rocha, ST, et al. (2012) Imprinted gene dosage is critical for the transition to independent life. Cell Metabolism 15(2): 209–221.Google Scholar

Chatterjee, A, Saha, D, Niemann, H, Gryshkov, O, Gismacher, B, Hofmann, N (2017) Effects of cryopreservation on the epigenetic profile of cells. Cryobiology 74: 1–7.Google Scholar

Chen, Z, Hagen, DE, Elsik, CG, et al. (2015) Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction. Proceedings of the National Academy of Sciences of the USA 112(15): 4618–4623.CrossRef Google Scholar PubMed

Chen, Q, Yan, M, Cao, Z, et al. (2016) Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351(6271): 397–400.CrossRef Google Scholar PubMed

Chen, H, Zhang, L, Deng, T, et al. (2016) Effects of oocyte vitrification on epigenetic status in early bovine embryos. Theriogenology 86(3): 868–878.CrossRef Google Scholar PubMed

Cheng, KR, Fu, XW, Zhang, RN, Jia, GX, Hou, YP, Zhu, SE (2014) Effect of oocyte vitrification on deoxyribonucleic acid methylation of H19, Peg3, and Snrpn differentially methylated regions in mouse blastocysts. Fertility and Sterility 102(4): 1183–1190.Google Scholar

Chopra, M, Amor, DJ, Sutton, L, Algar, E, Mowat, D (2010) Russell-Silver syndrome due to paternal H19/IGF2 hypomethylation in a patient conceived using intracytoplasmic sperm injection. Reproductive Biomedicine Online 20(6): 843–847.Google Scholar

Chotalia, M, Smallwood, SA, Ruf, N, et al. (2009) Transcription is required for establishment of germline methylation marks at imprinted genes. Genes and Development 23(1): 105–117.Google Scholar

Choufani, S, Turinsky, AL, Melamed, N, et al. (2018) Impact of assisted reproduction, infertility, sex, and paternal factors on the placental DNA methylome. Human Molecular Genetics 28(3): 372–385.Google Scholar

Ciccone, DN, Su, H, Hevi, S, et al. (2009) KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461(7262): 415–418.Google Scholar

Coan, PM, Burton, GJ, Ferguson-Smith, AC (2005) Imprinted genes in the placenta; a review. Placenta 26: S10–20.Google Scholar

Constância, M, Pickard, B, Kelsey, G, Reik, W (1998) Imprinting mechanisms. Genome Research 8(9): 881–900.Google Scholar

Corry, GN, Tanasijevic, B, Barry, ER, Krueger, W, Rasmussen, TP (2009) Epigenetic regulatory mechanisms during preimplantation development. Birth Defects Research Part C Embryo Today 87(4): 297–313.Google Scholar

Cox, GF, Burger, J, Lip, V, et al. (2002) Intracytoplasmic sperm injection may increase the risk of imprinting defects. American Journal of Human Genetics 1(1): 162–164.CrossRef Google Scholar

Dahl, JA, Reiner, AH, Klungland, A, Wakayama, T, Collas, P (2010) Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos. PLoS One 5(2): e9150.Google Scholar

DeBaun, MR, Niemitz, EL, Feinberg, AP (2003) Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. American Journal of Human Genetics 72: 156–160.Google Scholar

De Munck, N, Petrussa, L, Verheyen, G, et al. (2015) Chromosomal meiotic segregation, embryonic developmental kinetics and DNA (hydroxy)methylation analysis consolidate the safety of human oocyte vitrification. Molecular Human Reproduction 21(6): 535–544.CrossRef Google Scholar PubMed

Denomme, MM, Mann, MR (2012) Genomic imprints as a model for the analysis of epigenetic stability during assisted reproductive technologies. Reproduction 144(4): 393–409.CrossRef Google Scholar

Denomme, MM, McCallie, BR, Parks, JC, Schoolcraft, WB, Katz-Jaffe, MG (2017) Alterations in the sperm histone retained epigenome are associated with unexplained male factor infertility and poor blastocyst development in donor oocyte IVF cycles. Human Reproduction 32(12): 2443–2455.CrossRef Google Scholar PubMed

Denomme, MM, Zhang, L, Mann, MR (2011) Embryonic imprinting perturbations do not originate from superovulation-induced defects in DNA methylation acquisition. Fertility and Sterility 96(3): 734–738.e2.Google Scholar

de Castro Barbosa, T, Ingerslev, LR, Alm, PS, et al. (2016) High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Molecular Metabolism 5(3): 184–197.Google Scholar

De Vos, A, Janssens, R, Van de Velde, H, et al. (2015) The type of culture medium and the duration of in vitro culture do not influence birthweight of ART singletons. Human Reproduction 30(1): 20–27.Google Scholar

Derakhshan-Horeh, M, Abolhassani, F, Jafarpour, F, et al. (2016) Vitrification at Day 3 stage appears not to affect the methylation status of H19/IGF2 differentially methylated region of in vitro produced human blastocysts. Cryobiology 73(2): 168–174.CrossRef Google Scholar

Doherty, AS, Mann, MR, Tremblay, KD, Bartolomei, MS, Schultz, RM (2000) Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biology of Reproduction 62(6): 1526–1535.Google Scholar

Doornbos, ME, Maas, SM, McDonnell, J, Vermeiden, JP, Hennekam, RC (2007) Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Human Reproduction 22: 2476–2480.Google Scholar

Dumoulin, JC, Land, JA, Van Montfoort, AP, et al. (2010) Effect of in vitro culture of human embryos on birthweight of newborns. Human Reproduction 25(3): 605–612.Google Scholar

Eggermann, T, Perez de Nanclares, G, Maher, ER, et al. (2015) Imprinting disorders: a group of congenital disorders with overlapping patterns of molecular changes affecting imprinted loci. Clinical Epigenetics 7: 123.Google Scholar

Eskld, A, Monkerud, L, Tanbo, T (2013) Birthweight and placental weight; do changes in culture media used for IVF matter? Comparisons with spontaneous pregnancies in the corresponding time periods. Human Reproduction 28(12): 3207–3214.CrossRef Google Scholar

Fauque, P (2013) Superovulation: ovulation induction and epigenetic anomalies. Fertility and Sterility 99(3): 616–623.Google Scholar

Fauque, P, Jouannet, P, Lesaffre, C, et al. (2007) Assisted reproductive technology affects developmental kinetics, H19 imprinting control region methylation and H19 gene expression in individual mouse embryos. BMC Developmental Biology 7: 116.Google Scholar

Fauque, P, Mondon, F, Letourneur, F, et al. (2010b) In vitro fertilization and embryo culture strongly impact the placental transcriptome in the mouse model. PLoS One 5(2): e9218.Google Scholar

Fauque, P, Ripoche, MA, Tost, J, et al. (2010a) Modulation of imprinted gene network in placenta results in normal development of in vitro manipulated mouse embryos. Human Molecular Genetics 19(9): 1779–1790Google Scholar

Fenic, I, Hossain, HM, Sonnack, V, et al. (2008) In vivo application of histone deacetylase inhibitor trichostatin-a impairs murine male meiosis. Journal of Andrology 29: 172–185.Google Scholar

Fenic, I, Sonnack, V, Failing, K, Bergmann, M, Steger, K (2004) In vivo effects of histone-deacetylase inhibitor trichostatin-A on murine spermatogenesis Journal of Andrology 25: 811–818.Google Scholar

Fernandez-Gonzalez, R, Moreira, P, Bilbao, A, et al. (2004) Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proceedings of the National Academy of Sciences of the USA 101: 5880–5885.Google Scholar

Fortier, AL, Lopes, FL, Darricarrère, N, Martel, J, Trasler, JM (2008) Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Human Molecular Genetics 17(11): 1653–1665.Google Scholar

Fortier, AL, McGraw, S, Lopes, FL, et al. (2014) Modulation of imprinted gene expression following superovulation. Molecular and Cellular Endocrinology 388(1–2): 51–57.Google Scholar

Frost, RJ, Hamra, FK, Richardson, JA, Qi, X, BAssel-Duby, R, Olson, EN (2010) MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proceedings of the National Academy of Sciences of the USA 107: 11847–11852.Google Scholar

Gad, A, Schellander, K, Hoelker, M, Tesfaye, D (2012) Transcriptome profile of early mammalian embryos in response to culture environment. Animal Reproduction Science 134(1–2): 76–83.Google Scholar

Galli-Tsinopoulou, A, Emmanouilidou, E, Karagianni, P, et al. (2008) A female infant with Silver Russell Syndrome, mesocardia and enlargement of the clitoris. Hormones (Athens) 7: 77–81.Google Scholar

Gardner, DK, Kelly, RL (2017) Impact of the IVF laboratory environment on human preimplantation embryo phenotype. Journal of Developmental Origins of Health and Disease 8(4): 418–435.Google Scholar

Ge, ZJ, Liang, QX, Hou, Y, et al. (2014) Maternal obesity and diabetes may cause DNA methylation alteration in the spermatozoa of offspring in mice. Reproductive Biology and Endocrinology 12: 29.CrossRef Google Scholar PubMed

Geuns, E, De Rycke, M, Van Steirteghem, A, Leibaers, I (2003) Methylation imprints of the imprint control region of the SNRPN-gene in human gametes and preimplantation embryos. Human Molecular Genetics 12(22): 2873–2879.Google Scholar

Ghosh, J, Coutifaris, C, Sapienza, C, Mainigi, M (2017) Global DNA methylation levels are altered by modifiable clinical manipulations in assisted reproductive technologies. Clinical Epigenetics 9: 14.CrossRef Google Scholar PubMed

Gicquel, C, Gaston, V, Mandelbaum, J, et al. (2003) In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. American Journal of Human Genetics 72: 1338.CrossRef Google Scholar

Ginsburg, M, Snow, MH, McLaren, A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110: 521–528.Google Scholar

Gomes, MV, Huber, J, Ferriani, RA, Amaral Neto, AM, Ramos, ES (2009) Abnormal methylation at the KvDMR1 imprinting control region in clinically normal children conceived by assisted reproductive technologies. Molecular and Human Reproduction 15(8): 471–477.Google Scholar

Gross, N, Kroop, J, Khatib, H (2017) MicroRNA signaling in embryo development. Biology (Basel) 6(3): pii:E34.Google Scholar

Guo, H, Zhu, P, Yan, L, et al. (2014) The DNA methylation landscape of human early embryos. Nature 511: 606–610.Google Scholar

Halliday, J, Oke, K, Breheny, S, Algar, EJ Amor, D (2004) Beckwith-Wiedemann syndrome and IVF: a case-control study. American Journal of Human Genetics 75: 526–528.Google Scholar

Hammoud, SS, Purwar, J, Pflueger, C, Cairns, BR, Carrell, DT (2010) Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertility and Sterility 94(5): 1728–1733.Google Scholar

Hammoud, SS, Nix, DA, Hammoud, AO, Gibson, M, Cairns, BR, Carrell, DT (2011) Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Human Reproduction 26: 2558–2569.Google Scholar

Hammoud, SS, Nix, DA, Zhang, H, Purwar, K, Carrell, DT, Cairns, BR (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460: 473–478.Google Scholar

Hata, K, Okano, M, Lei, H, Li, E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129(8): 1983–1993.Google Scholar

Hayashi, S, Yang, J, Christenson, L, Yanagimachi, R, Hecht, NB (2003) Mouse preimplantation embryos developed from oocytes injected with round spermatids or spermatozoa have similar but distinct patterns of early messenger RNA expression. Biology of Reproduction 69: 1170–1176.Google Scholar

Hiendleder, S, Mund, C, Reichenbach, HD, et al. (2004) Tissue-specific elevated genomic cytosine methylation levels are associated with an overgrowth phenotype of bovine fetuses derived by in vitro techniques. Biology of Reproduction 71(1): 217–223.Google Scholar

Hill, PW, Amouroux, R, Hajkova, P (2014) DNA demethylation, Tet proteins and 5-hydroxymethylcytosine in epigenetic reprogramming: an emerging complex story. Genomics 104(5): 324–333.CrossRef Google Scholar PubMed

Hirasawa, R, Chiba, H, Kaneda, M, et al. (2008) Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes and Development 22(12): 1607–1616.CrossRef Google Scholar PubMed

Hiura, H, Obata, Y, Komiyama, J, Shirai, M, Kono, T (2006) Oocyte growth-dependent progression of maternal imprinting in mice. Genes to Cells 11(4): 353–361.CrossRef Google Scholar PubMed

Hiura, H, Okae, H, Chiba, H, et al. (2014) Imprinting methylation errors in ART. Reproductive Medicine and Biology 13(4): 193–202.Google Scholar

Hiura, H, Okae, H, Miyauchi, N, et al. (2012) Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Human Reproduction 27(8): 2541–2548.Google Scholar

Holm, TM, Jackson-Grusby, L, Brambrink, T, et al. (2005) Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell 8: 275–285.Google Scholar

Hotaling, J, Carrell, DT (2014) Clinical genetic testing for male factor infertility: current applications and future directions. Andrology 2(3): 339–350.Google Scholar

Houshdaran, S, Cortessis, VK, Siegmund, K, et al. (2007) Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS One 2(12): e1289.Google Scholar

Huffman, SR, Pak, Y, Rivera, RM (2015) Superovulation induces alterations in the epigenome of zygotes, and results in differences in gene expression at the blastocyst stage in mice. Molecular Reproduction and Development 82(3): 207–217.Google Scholar

Huntriss, J (2011) Epigenetics and assisted reproduction. In: Elder, K, Dale, B (eds.) In-Vitro Fertilization, 3rd edn. Cambridge University Press, Cambridge, UK, pp. 252–267.Google Scholar

Huntriss, J, Balen, AH, Sinclair, KD, Brison, DR, Picton, HM; Royal College of Obstetricians Gynaecologists (2018) Epigenetics and Reproductive Medicine: Scientific Impact Paper No. 57. BJOG 125(13): e43–e54.Google Scholar

Huntriss, JD, Hemmings, KE, Hinkins, M, et al. (2013) Variable imprinting of the MEST gene in human preimplantation embryos. European Journal of Human Genetics 21(1): 40–47.Google Scholar

Huntriss, J, Picton, HM (2008) Epigenetic consequences of assisted reproduction and infertility on the human preimplantation embryo. Human Fertility (Cambridge) 11(2): 85–94.Google Scholar

Ibala-Romdhane, S, Al-Khtib, M, Khoueiry, R, Blachére, T, Guerin, JF, Lefévre, A (2011) Analysis of H19 methylation in control and abnormal human embryos, sperm and oocytes. European Journal of Human Genetics 19(11): 1138–1143.Google Scholar

Imamura, T, Kerjean, A, Heams, T, et al. (2005) Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo. Journal of Biological Chemistry 280: 20171–20175.Google Scholar

Isles, AR, Holland, AJ (2005) Imprinted genes and mother-offspring interactions. Early Human Development 81: 73–77.Google Scholar

Jenkins, TG, Aston, KI, Pflueger, C, Cairns, BR, Carrell, DT (2014) Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility. PLoS Genetics 10(7): e1004458.Google Scholar

Jenkins, TG, James, ER, Alonso, DF, et al. (2017) Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology 5(6): 1089–1099.Google Scholar

Johnson, JP, Schoof, J, Beischel, L, et al. (2018) Detection of a case of Angelman syndrome caused by an imprinting error in 949 pregnancies analyzed for AS following IVF. Journal of Assisted Reproduction and Genetics 35(6): 981–984.Google Scholar

Kagami, M, Nagai, T, Fukami, M, Yamazawa, K, Ogata, T (2007) Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. Journal of Assisted Reproduction and Genetics 24: 131–136.Google Scholar

Källén, B, Finnström, O, Lindam, A, et al. (2010) Congenital malformations in infants born after in vitro fertilization in Sweden. Birth Defects Research A: Clinical and Molecular Teratology 88(3): 137–143.Google Scholar

Källén, B, Finnström, O, Nygren, KG, Olausson, PO (2005) In vitro fertilization (IVF) in Sweden: infant outcome after different IVF fertilization methods. Fertility and Sterility 84: 611–617.Google Scholar

Kanber, D, Berulava, T, Ammerpohl, O, et al. (2009a) The human retinoblastoma gene is imprinted. PLoS Genetics 5(12): e1000790.Google Scholar

Kanber, D, Buiting, K, Zeschnigk, M, Ludwig, M, Horsthemke, B (2009b) Low frequency of imprinting defects in ICSI children born small for gestational age. European Journal of Human Genetics 17(1): 22–29.CrossRef Google Scholar PubMed

Kerjean, A, Couvert, P, Heams, T, et al. (2003) In vitro follicular growth affects oocyte imprinting establishment in mice. European Journal of Human Genetics 11: 493–496.Google Scholar

Khosla, S, Dean, W, Brown, D, Reik, W, Feil, R (2001) Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biology of Reproduction 64: 918–926.Google Scholar

Khoueiry, R, Ibala-Rhomdane, S, Al-Khtib, M, et al. (2012) Abnormal methylation of KCNQ1OT1 and differential methylation of H19 imprinting control regions in human ICSI embryos. Zygote 21: 1–10.Google Scholar

Khoueiry, R, Ibala-Rhomdane, S, Méry, L, et al. (2008) Dynamic CpG methylation of the KCNQ1OT1 gene during maturation of human oocytes. Journal of Medical Genetics 45(9): 583–588.Google Scholar

Kim, KP, Thurston, A, Mummery, C, et al. (2007) Gene-specific vulnerability to imprinting variability in human embryonic stem cell lines. Genome Research 17: 1731–1742.Google Scholar

Kimber, SJ, Sneddon, SF, Bloor, DJ, et al. (2008) Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction 135(5): 635–647.Google Scholar

Kishigami, S, Van Thuan, N, Hikichi, T, et al. (2006) Epigenetic abnormalities of the mouse paternal zygotic genome associated with microinsemination of round spermatids. Developmental Biology 289: 195–205.Google Scholar

Klaver, R, Gromoll, J (2014) Bringing epigenetics into the diagnostics of the andrology laboratory: challenges and perspectives. Asian Journal of Andrology 16(5): 669–674.Google Scholar

Kleijkers, SH, Eijssen, LM, Coonen, E, et al.(2015a) Differences in gene expression profiles between human preimplantation embryos cultured in two different IVF culture media. Human Reproduction 30(10): 2303–2311.Google Scholar

Kleijkers, SH, van Montfoort, AP, Smits, LJ, et al. (2015b) Age of G-1 PLUS v5 embryo culture medium is inversely associated with birthweight of the newborn. Human Reproduction 30(6): 1352–1357.Google Scholar

Kobayashi, H, Hiura, H, John, RM, et al. (2009) DNA methylation errors at imprinted loci after assisted conception originate in the parental sperm. European Journal of Human Genetics 17(12): 1582–1591.Google Scholar

Kobayashi, H, Sato, A, Otsu, E, et al. (2007) Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Human Molecular Genetics 16: 2542–2551.Google Scholar

Kono, T (2009) Genetic modification for bimaternal embryo development. Reproduction and Fertility Development 21(1): 31–36.Google Scholar

Kurihara, Y, Kawamura, Y, Uchijima, Y, et al. (2008) Maintenance of genomic methylation patterns during preimplantation development requires the somatic form of DNA methyltransferase 1. Developmental Biology 313(1): 335–346.Google Scholar

Lane, M, Gardner, DK (1994) Increase in postimplantation development of cultured mouse embryos by amino acids and induction of fetal retardation and exencephaly by ammonium ions. Journal of Reproduction & Fertility 102(2): 305–312.Google Scholar

Lane, M, Gardner, DK (2003) Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biology of Reproduction 69: 1109–1117.Google Scholar

Lazaraviciute, G, Kauser, M, Bhattacharya, S, Haggarty, P (2014) A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Human Reproduction Update 20(6): 840–852.Google Scholar

Lee, I, Finger, PT, Grifo, JA, et al. (2004) Retinoblastoma in a child conceived by in vitro fertilisation. British Journal of Ophthalmology 88(8): 1098–1099.Google Scholar

Lee, MG, Wynder, C, Cooch, N, Shiekhattar, R (2005) An essential role for CoREST in nucleosomal histone-3-lysine-4 demethylation. Nature 437: 432–435.Google Scholar

Lee, YS, Latham, KE, Vandevoort, CA (2008) Effects of in vitro maturation on gene expression in rhesus monkey oocytes. Physiological Genomics 35(2): 145–158.Google Scholar

Lees-Murdock, DJ, Lau, HT, Castrillon, DH, De Felici, M, Walsh, CP (2008) DNA methyltransferase loading, but not de novo methylation, is an oocyte-autonomous process stimulated by SCF signalling. Developmental Biology 321(1): 238–250.CrossRef Google Scholar

Lees-Murdock, DJ, Walsh, CP (2008) DNA methylation reprogramming in the germ line. Advances in Experimental Medicine and Biology 626: 1–15.Google Scholar

Li, G, Yu, Y, Fan, Y, et al. (2017) Genome wide abnormal DNA methylome of human blastocyst in assisted reproductive technology. Journal of Genetics and Genomics 44(10): 475–481.Google Scholar

Li, T, Vu, TH, Ulaner, GA, et al. (2005) IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Molecular Human Reproduction 11: 631–640.Google Scholar

Li, X, Ito, M, Zhou, F, et al. (2008) A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Developmental Cell 15(4): 547–557.Google Scholar

Liang, XW, Zhu, JQ, Miao, YL, et al. (2008) Loss of methylation imprint of Snrpn in postovulatory aging mouse oocyte. Biochemical and Biophysical Research Communications 371(1): 16–21.Google Scholar

Liang, Y, Fu, XW, Li, JJ, Yuan, DS, Zhu, SE (2014) DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos: effect of oocyte vitrification. Zygote 22(2): 138–145.Google Scholar

Lim, D, Bowdin, SC, Tee, L, et al. (2009) Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies. Human Reproduction 24(3): 741–747.Google Scholar

Lin, S, Li, M, Lian, Y, Chen, L, Liu, P (2013) No effect of embryo culture media on birthweight and length of newborns. Human Reproduction 28(7): 1762–1767.Google Scholar

Lucifero, D, La Salle, S, Bourc’his, D, et al. (2007) Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Developmental Biology 7: 36.CrossRef Google Scholar PubMed

Lucifero, D, Mann, MR, Bartolomei, MS, Trasler, JM (2004) Gene-specific timing and epigenetic memory in oocyte imprinting. Human Molecular Genetics 13(8): 839–849.Google Scholar

Ludwig, M, Katalinic, A, Gross, S, et al. (2005) Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. Journal of Medical Genetics 42: 289–291.Google Scholar

Luedi, PP, Dietrich, FS, Weidman, JR, et al. (2007) Computational and experimental identification of novel human imprinted genes. Genome Research 17(12): 1723–1730.Google Scholar

Maas, K, Galinka, E, Thornton, K, Penzias, AS, Sakkas, D (2016) No change in live birthweight of IVF singleton deliveries over an 18-year period despite significant clinical and laboratory changes. Human Reproduction 31(9): 1987–1996.Google Scholar

Mackay, DJ, Boonen, SE, Clayton-Smith, J, et al. (2006) A maternal hypomethylation syndrome presenting as transient neonatal diabetes mellitus. Human Genetics 120: 262–269.Google Scholar

Maher, ER, Brueton, LA, Bowdin, SC, et al. (2003) Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). Journal of Medical Genetics 40: 62–64.Google Scholar

Maher, ER, Reik, W (2000) Beckwith-Wiedemann syndrome: imprinting in clusters revisited. Journal of Clinical Investigation 105(3): 247–252.Google Scholar

Mainigi, MA, Sapienza, C, Butts, S, Coutifaris, C (2016) A molecular perspective on procedures and outcomes with assisted reproductive technologies. Cold Spring Harbor Perspectives in Medicine 6(4): a023416.Google Scholar

Malter, HE, Cohen, J (2002) Ooplasmic transfer: animal models assist human studies. Reproductive Biomedicine Online 5(1): 26–35.CrossRef Google Scholar PubMed

Mann, MR, Lee, SS, Doherty, AS, et al. (2004) Selective loss of imprinting in the placenta following preimplantation development in culture. Development 131: 3727–3735.Google Scholar

Manning, M, Lissens, W, Bonduelle, M, et al. (2000) Study of DNA-methylation patterns at chromosome 15q11-q13 in children born after ICSI reveals no imprinting defects. Molecular Human Reproduction 6: 1049–1053.Google Scholar

Manning, M, Lissens, W, Liebaers, I, Van Steirteghem, A, Weidner, W (2001a) Imprinting analysis in spermatozoa prepared for intracytoplasmic sperm injection (ICSI). International Journal of Andrology 24(2): 87–94.Google Scholar

Manning, M, Lissens, W, Weidner, W, Liebaers, I (2001b) DNA methylation analysis in immature testicular sperm cells at different developmental stages. Urology International 67(2): 151–155.Google Scholar

Mantikou, E, Jonker, MJ, Wong, KM, et al. (2016) Factors affecting the gene expression of in vitro cultured human preimplantation embryos. Human Reproduction 31(2): 298–311.Google Scholar

Marees, T, Dommering, CJ, Imhof, SM, et al. (2009) Incidence of retinoblastoma in Dutch children conceived by IVF: an expanded study. Human Reproduction 24(12): 3220–3224.Google Scholar

Market-Velker, BA, Fernandes, AD, Mann, MR (2010) Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biology of Reproduction 83(6): 938–950.Google Scholar

Market-Velker, BA, Zhang, L, Magri, LS, Bonvissuto, AC, Mann, MR (2010) Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Human Molecular Genetics 19(1): 36–51.Google Scholar

Marques, CJ, Carvalho, F, Sousa, M, Barros, A (2004) Genomic imprinting in disruptive spermatogenesis. Lancet 363: 1700–1702.Google Scholar

Marques, CJ, Costa, P, Vaz, B, et al. (2008) Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Molecular Human Reproduction 14(2): 67–74.Google Scholar

Marques, CJ, Francisco, T, Sousa, S, et al. (2010) Methylation defects of imprinted genes in human testicular spermatozoa. Fertility and Sterility 94(2): 585–594.Google Scholar

McMinn, J, Wei, M, Schupf, N, et al. (2006) Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta 27: 540–549.Google Scholar

Melamed, N, Choufani, S, Wilkins-Haug, LE, Koren, G, Weksberg, R (2015) Comparison of genome-wide and gene-specific DNA methylation between ART and naturally conceived pregnancies. Epigenetics 10(6): 474–483.Google Scholar

Ménézo, Y, Elder, K, Benkhalifa, M, Dale, B (2010) DNA methylation and gene expression in IVF. Reproductive Biomedicine Online 20(6): 709–710.Google Scholar

Ménézo, Y, Dale, B, Elder, K (2018) Time to re-evaluate ART protocols in the light of advances in knowledge about methylation and epigenetics: an opinion paper. Human Fertility (Cambridge) 21(3): 156–162.Google Scholar

Meschede, D, De Geyter, C, Nieschlag, E, Horst, J (1995) Genetic risk in micromanipulative assisted reproduction. Human Reproduction 10: 2880–2886.Google Scholar

Moll, AC, Imhof, SM, Cruysberg, JR, et al. (2003) Incidence of retinoblastoma in children born after in-vitro fertilisation. Lancet 361(9354): 309–310.Google Scholar

Monk, M, Boubelik, M, Lehnert, S (1987) Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99(3): 371–382.Google Scholar

Moore, T, Haig, D (1991) Genomic imprinting in mammalian development: a parental tug of war. Trends in Genetics 7: 45–49.Google Scholar

Morgan, HD, Santos, F, Green, K, Dean, W, Reik, W (2005) Epigenetic reprogramming in mammals. Human Molecular Genetics 14(Spec No 1): R47–58.Google Scholar

Morison, IM, Ramsay, JP, Spencer, HG (2005) A census of mammalian imprinting. Trends in Genetics 21: 457–465.Google Scholar

Morison, IM, Reeve, AE (1998) A catalogue of imprinted genes and parent-of-origin effects in humans and animals. Human Molecular Genetics 7: 1599–1609.Google Scholar

Mussa, A, Molinatto, C, Cerrato, F, et al. (2017) Assisted reproductive techniques and risk of Beckwith-Wiedemann Syndrome Pediatrics 140(1): pii e20164311.Google Scholar

Nakamura, T, Arai, Y, Umehara, H, et al. (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nature Cell Biology 9(1): 64–71.Google Scholar

Nelissen, EC, Van Montfoort, AP, Coonen, E, et al. (2012) Further evidence that culture media affect perinatal outcome: findings after transfer of fresh and cryopreserved embryos. Human Reproduction 27(7): 1966–1976.Google Scholar

Obata, Y, Kaneko-Ishino, T, Koide, T, et al. (1998) Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development 125: 1553–1560.Google Scholar

Obata, Y, Kono, T (2002) Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. Journal of Biological Chemistry 277: 5285–5289.Google Scholar

O’Doherty, AM, O’Shea, LC, Fair, T (2012) Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biology of Reproduction 86(3): 67.Google Scholar

Odom, LN, Segars, J (2010) Imprinting disorders and assisted reproductive technology. Current Opinion in Endocrinology, Diabetes, and Obesity 17(6): 517–522.Google Scholar

Ohno, M, Aoki, N, Sasaki, H (2001) Allele-specific detection of nascent transcripts by fluorescence in situ hybridization reveals temporal and culture-induced changes in Igf2 imprinting during pre-implantation mouse development. Genes to Cells 6: 249–259.Google Scholar

Okada, Y, Scott, G, Ray, MK, Mishina, Y, Zhang, Y (2007) Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature 450(7166):119–123.Google Scholar

Okae, H, Chiba, H, Hiura, H, et al. (2014) Genome-wide analysis of DNA methylation dynamics during early human development. PLoS Genetics 10(12): e1004868.Google Scholar

Omisanjo, OA, Biermann, K, Hartmann, S, et al. (2007) DNMT1 and HDAC1 gene expression in impaired spermatogenesis and testicular cancer. Histochemistry and Cell Biology 127: 175–181.Google Scholar

Ørstavik, KH, Eiklid, K, van der Hagen, CB, et al. (2003) Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. American Journal of Human Genetics 72: 218–219.Google Scholar

Ostermeier, GC, Dix, DJ, Miller, DD, Khatri, P, Krawetz, SA (2002) Spermatozoal RNA profiles of normal fertile men. Lancet 360(9335): 772–777.Google Scholar

Pantoja, C, de Los Rios, L, Matheu, A, Antequera, F, Serrano, M (2005) Inactivation of imprinted genes induced by cellular stress and tumorigenesis. Cancer Research 65: 26–33.Google Scholar

Pastor, WA, Stroud, H, Nee, K, et al. (2014) MORC1 represses transposable elements in the mouse male germline. Nature Communications 12(5): 5795.Google Scholar

Poplinski, A, Tüttelmann, F, Kanber, D, Horsthemke, B, Gromoll, J (2010) Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. International Journal of Andrology 33(4): 642–649.Google Scholar

Probst, AV, Santos, F, Reik, W, Almouzni, G, Dean, W (2007) Structural differences in centromeric heterochromatin are spatially reconciled on fertilisation in the mouse zygote. Chromosoma 116(4): 403–415.Google Scholar

Qiao, J, Chen, Y, Yan, LY, et al. (2009) Changes in histone methylation during human oocyte maturation and IVF- or ICSI-derived embryo development. Fertility and Sterility 93(5): 1628–1636.Google Scholar

Rajender, S, Avery, K, Agarwal, A (2011) Epigenetics, spermatogenesis and male infertility. Mutation Research 727: 62–71.Google Scholar

Reik, W, Dean, W, Walter, J (2001) Epigenetic reprogramming in mammalian development. Science 293(5532): 1089–1093.Google Scholar

Reik, W, Maher, ER (1997) Imprinting in clusters: lessons from Beckwith-Wiedemann syndrome. Trends in Genetics 13(8): 330–334.Google Scholar

Reik, W, Walter, J (2001) Genomic imprinting: parental influence on the genome. Nature Reviews (Genetics) 2: 21–32.Google Scholar

Renard, JP, Baldacci, P, Richouxduranthon, V, Pournin, S, Babinet, C (1994) A maternal factor affecting mouse blastocyst formation. Development 120: 797–802.Google Scholar

Rivera, RM, Ross, JW (2013) Epigenetics in fertilization and preimplantation development. Prog Biophys Mol Biol 113(3): 423–432.Google Scholar

Rossignol, S, Steunou, V, Chalas, C, et al. (2006) The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region. Journal of Medical Genetics 43: 902–907.Google Scholar

Rugg-Gunn, PJ, Ferguson-Smith, AC, Pedersen, RA (2005) Epigenetic status of human embryonic stem cells. Nature Genetics 37: 585–587.Google Scholar

Sagirkaya, H, Misirlioglu, M, Kaya, A, et al. (2006) Developmental and molecular correlates of bovine preimplantation embryos. Reproduction 131: 895–904.Google Scholar

Sagirkaya, H, Misirlioglu, M, Kaya, A, et al. (2007) Developmental potential of bovine oocytes cultured in different maturation and culture conditions. Animal Reproduction Science 101: 225–240.Google Scholar

Saenz-de-Juano, MD, Peñaranda, DS, Marco-Jiménez, F, Vicente, JS (2014) Does vitrification alter the methylation pattern of OCT4 promoter in rabbit late blastocyst? Cryobiology 69(1): 178–180.Google Scholar

Sanchez-Albisua, I, Borell-Kost, S, Mau-Holzmann, UA, Licht, P, Krägeloh-Mann, I (2007) Increased frequency of severe major anomalies in children conceived by intracytoplasmic sperm injection. Developments in Medical Child Neurology 49(2): 129–134.Google Scholar

Santi, D, De Vincentis, S, Magnani, E, Spaggiari, G (2017) Impairment of sperm DNA methylation in male infertility: a meta-analytic study. Andrology 5(4): 695–703.Google Scholar

Santos, F, Hendrich, B, Reik, W, Dean, W (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Developmental Biology 241(1): 172–182.Google Scholar

Santos, F, Hyslop, L, Stojkovic, P, et al. (2010) Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Human Reproduction 25(9): 2387–2395.Google Scholar

Sasaki, H, Ferguson-Smith, AC, Shum, AS, Barton, SC, Surani, MA (1995) Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos. Development. 121(12): 4195–4202.Google Scholar

Sato, A, Otsu, E, Negishi, H, Utsunomiya, T, Arima, T (2007) Aberrant DNA methylation of imprinted loci in superovulated oocytes. Human Reproduction 22: 26–35.Google Scholar

Schwarzer, C, Esteves, TC, Arauzo-Bravo, MJ, et al. (2012) ART culture conditions change the probability of mouse embryo gestation through defined cellular and molecular responses. Human Reproduction 27(9): 2627–2640.Google Scholar

Shamanski, FL, Kimura, Y, Lavoir, MC, Pedersen, RA, Yanagimachi, R (1999) Status of genomic imprinting in mouse spermatids. Human Reproduction 14: 1050–1056.Google Scholar

Sharma, U, Conine, CC, Shea, JM, et al. (2016) Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351(6271): 391–396.Google Scholar

Shea, JM, Serra, RW, Carone, BR, et al.(2015) Genetic and epigenetic variation, but not diet, shape the sperm methylome. Developmental Cell 35(6): 750–758.Google Scholar

Shi, W, Haaf, T (2002) Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure. Molecular Reproduction and Development 63: 329–334.Google Scholar

Shi, Y, Lan, F, Matson, C, et al.(2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941–953.Google Scholar

Sikienka, K, Erek, S, Godmann, M, et al. (2015) Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350(6261): aab2006.Google Scholar

Skaar, DA, Li, Y, Bernal, AJ, Hoyo, C, Murphy, SK, Jirtle, RL (2012) The human imprintome: regulatory mechanisms, methods of ascertainment, and roles in disease susceptibility. ILAR Journal/National Research Council, Institute of Laboratory Animal Resources 53(3–4): 341–358.Google Scholar

Smallwood, SA, Kelsey, G (2012) Genome-wide analysis of DNA methylation in low cell numbers by reduced representation bisulfite sequencing. Methods in Molecular Biology 925: 187–197.Google Scholar

Smallwood, SA, Tomizawa, S, Krueger, F, et al. (2011) Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nature Genetics 43(8): 811–814.Google Scholar

Smith, ZD, Chan, MM, Humm, KC, et al. (2014) DNA methylation dynamics of the human preimplantation embryo. Nature 511: 611–615.Google Scholar

Song, S, Ghosh, J, Mainigi, M, et al. (2015) DNA methylation differences between in vitro- and in vivo-conceived children are associated with ART procedures rather than infertility. Clinical Epigenetics 7: 41.Google Scholar

Soubry, A, Hoyo, C, Jirtle, RL, Murphy, SK (2014) A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. BioEssays: News and Reviews in Molecular, Cellular And Developmental Biology 36(4): 359–371.Google Scholar

Stouder, C, Deutsch, S, Paoloni-Giacobino, A (2009) Superovulation in mice alters the methylation pattern of imprinted genes in the sperm of the offspring. Reproductive Toxicology 28(4): 536–541.Google Scholar

Stuppia, L, Franzago, M, Ballerini, P, Gatta, V, Antonucci, I (2015) Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clinical Epigenetics 7: 120.Google Scholar

Sujit, KM,Sarkar, S, Singh, V, et al (2018) Genome-wide differential methylation analyses identifies methylation signatures of male infertility. Human Reproduction 33(12): 2256–2267.Google Scholar

Sun, BW, Yang, AC, Feng, Y, et al. (2006) Temporal and parental-specific expression of imprinted genes in a newly derived Chinese human embryonic stem cell line and embryoid bodies. Human Molecular Genetics 15: 65–75.Google Scholar

Sunde, A, Brison, D, Dumoulin, J, et al. (2016) Time to take human embryo culture seriously. Human Reproduction 31(10): 2174–2182.Google Scholar

Sutcliffe, AG, Peters, CJ, Bowdin, S, et al. (2006) Assisted reproductive therapies and imprinting disorders: a preliminary British survey. Human Reproduction 21: 1009–1011.Google Scholar

Suzuki, J Jr, Therrien, J, Filion, F, et al. (2009) In vitro culture and somatic cell nuclear transfer affect imprinting of SNRPN gene in pre- and post-implantation stages of development in cattle. BMC Developmental Biology 9: 9.Google Scholar

Svensson, J, Bjornstahl, A, Ivarsson, SA (2005) Increased risk of Silver–Russell syndrome after in vitro fertilization? Acta Paediatrica 94: 1163–1165.Google Scholar

Tee, L, Lim, DH, Dias, RP, et al. (2013) Epimutation profiling in Beckwith-Wiedemann syndrome: relationship with assisted reproductive technology. Clinical Epigenetics 5(1): 23.Google Scholar

Tenorio, J, Ramanelli, V, Martin-Trujillo, A, et al. (2016) Clinical and molecular analyses of Beckwith-Wiedemann syndrome: Comparison between spontaneous conception and assisted reproduction techniques. American Journal of Medical Genetics 170(10): 2740–2749.Google Scholar

Torregrosa, N, Dominguez-Fandos, D, Camejo, MI, et al. (2006) Protamine 2 precursors, protamine 1/protamine 2 ratio, DNA integrity and other sperm parameters in infertile patients. Human Reproduction 21: 2084–2089.Google Scholar

Trapphoff, T, El Hjj, N, Zechner, U, Haaf, T, Eichenlaub-Ritter, U (2010) DNA integrity, growth pattern, spindle formation, chromosomal constitution and imprinting patterns of mouse oocytes from vitrified pre-antral follicles. Human Reproduction 25(12): 3025–3042.Google Scholar

Van der Auwera, I, D’Hooghe, T (2001) Superovulation of female mice delays embryonic and fetal development. Human Reproduction 16(6):1237–1243.Google Scholar

Vermeiden, JP, Bernardus, RE (2013) Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection? Fertility and Sterility 99(3): 642–651.Google Scholar

Walter, J, Paulsen, M (2003) Imprinting and disease. Seminars in Cell and Developmental Biology 14: 101–110.Google Scholar

Wang, Z, Xu, L, He, F (2010) Embryo vitrification affects the methylation of the H19/Igf2 differentially methylated domain and the expression of H19 and Igf2. Fertility and Sterility 93(8): 2729–2733.Google Scholar

White, CR, Denomme, MM, Tekpetey, FR, Feyles, V, Power, SG, Mann, MR (2015) High frequency of imprinted methylation errors in human preimplantation embryos. Scientific Reports 5: 17311.Google Scholar

Whitelaw, N, Bhattacharya, S, Hoad, G, Horgan, GW, Hamilton, M, Haggarty, P (2014) Epigenetic status in the offspring of spontaneous and assisted conception. Human Reproduction 29(7): 1452–1458.Google Scholar

Yamazaki, T, Yamagata, K, Baba, T (2007) Time-lapse and retrospective analysis of DNA methylation in mouse preimplantation embryos by live cell imaging. Developmental Biology 304: 409–419.Google Scholar

Yan, LY, Yan, J, Qiao, J, Zhao, PL, Liu, P (2010) Effects of oocyte vitrification on histone modifications. Reproduction Fertility and Development 22(6): 920–925.Google Scholar

Yao, J, Geng, L, Huang, R, et al. (2017) Effect of vitrification on in vitro development and imprinted gene Grb10 in mouse embryos. Reproduction 154(3): 97–105.Google Scholar

Young, LE, Fernandes, K, McEvoy, TG, et al. (2001) Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nature Genetics 27: 153–154.Google Scholar

Young, LE, Sinclair, KD, Wilmut, I (1998) Large offspring syndrome in cattle and sheep. Reviews of Reproduction 3(3): 155–163.Google Scholar

Yuan, S, Schuster, A, Tang, C, et al. (2016) Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development 143(4): 635–647.Google Scholar

Zaitseva, I, Zaitsev, S, Alenina, N, Bader, M, Krivokharchenko, A (2007) Dynamics of DNA-demethylation in early mouse and rat embryos developed in vivo and in vitro. Molecular Reproduction and Development 74(10): 1255–1261.Google Scholar

Zandstra, H, Brentjens, LBPM, Spauwen, B, Touwslager, RNH (2018) Association of culture medium with growth, weight and cardiovascular development of IVF children at the age of 9 years. Human Reproduction 33(9): 1645–1656.Google Scholar

Zandstra, H, Van Montfoort, AP, Dumoulin, JC (2015) Does the type of culture medium used influence birthweight of children born after IVF? Human Reproduction 30(11): 2693.Google Scholar

Zhao, XM, Du, WH, Hao, HS, et al. (2012) Effect of vitrification on promoter methylation and the expression of pluripotency and differentiation genes in mouse blastocysts. Molecular Reproduction and Development 79(7): 445–450.Google Scholar

Zhao, XM, Ren, JJ, Du, WH, et al. (2013) Effect of vitrification on promoter CpG island methylation patterns and expression levels of DNA methyltransferase 1o, histone acetyltransferase 1, and deacetylase 1 in metaphase II mouse oocytes. Fertility and Sterility 100(1): 256–261.Google Scholar

Zhu, J, Li, M, Chen, L, Liu, P, Qiao, J (2014b) The protein source in embryo culture media influences birthweight: a comparative study between G1 v5 and G1-PLUS v5. Human Reproduction 29(7): 1387–1392.Google Scholar

Zhu, J, Lin, S, Li, M, et al. (2014a) Effect of in vitro culture period on birthweight of singleton newborns. Human Reproduction 29(3): 448–454.Google Scholar

Zhu, P, Guo, H, Ren, Y, et al. (2018) Single-cell DNA methylome sequencing of human preimplantation embryos. Nature Genetics 50(1): 12–19.Google Scholar

Ziyyat, A, Lefevre, A (2001) Differential gene expression in pre-implantation embryos from mouse oocytes injected with round spermatids or spermatozoa. Human Reproduction 16: 1449–1456.Google Scholar