The placenta: phenotypic and epigenetic modifications induced by Assisted Reproductive Technologies throughout pregnancy

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Choux, Cécile ^a   Carmignac, Virginie ^a   Bruno, Céline ^a   Sagot, Paul ^a   Vaiman, Daniel ^b   Fauque, Patricia ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b CNRS   (France)

Author keywords

Assisted Reproductive Technologies; Epigenetic; Imprinted gene; Placenta; Pregnancy

Indexed keywords

DNA METHYLATION; EMBRYO CULTURE; ENDOMETRIUM; EPIGENETICS; GENOME IMPRINTING; HORMONAL THERAPY; HUMAN; INFERTILITY THERAPY; INTRAUTERINE GROWTH RETARDATION; METABOLIC DISORDER; NONHUMAN; OVARY HYPERSTIMULATION; PHENOTYPIC PLASTICITY; PLACENTA; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PLACENTAL TRANSFER; PREECLAMPSIA; PREGNANCY OUTCOME; PRIORITY JOURNAL; RETROPOSON; REVIEW; SPONTANEOUS ABORTION; SUPEROVULATION; TROPHOBLAST;

EID: 84939493029     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0120-2     Document Type: Review

References (188)

1. Brandes M, Verzijden JC, Hamilton CJ, de Weys NP, de Bruin JP, Bots RS, et al. Is the fertility treatment itself a risk factor for early pregnancy loss? Reprod Biomed Online. 2011;22:192–9.
2. Chaveeva P, Carbone IF, Syngelaki A, Akolekar R, Nicolaides KH. Contribution of method of conception on pregnancy outcome after the 11–13 weeks scan. Fetal Diagn Ther. 2011;30:9–22.
3. Wang JX, Norman RJ, Wilcox AJ. Incidence of spontaneous abortion among pregnancies produced by assisted reproductive technology. Hum Reprod. 2004;19:272–7.
4. Delle Piane L, Lin W, Liu X, Donjacour A, Minasi P, Revelli A, et al. Effect of the method of conception and embryo transfer procedure on mid-gestation placenta and fetal development in an Ivf mouse model. Hum Reprod. 2010;25:2039–46.
5. Fauque P, Ripoche MA, Tost J, Journot L, Gabory A, Busato F, et al. Modulation of imprinted gene network in placenta results in normal development of in vitro manipulated mouse embryos. Hum Mol Genet. 2010;19:1779–90.
6. Van der Auwera I, D'Hooghe T. Superovulation of female mice delays embryonic and fetal development. Hum Reprod. 2001;16:1237–43.
7. Thomopoulos C, Tsioufis C, Michalopoulou H, Makris T, Papademetriou V, Stefanadis C. Assisted reproductive technology and pregnancy-related hypertensive complications: a systematic review. J Hum Hypertens. 2013;27:148–57.
8. Jackson RA, Gibson KA, Wu YW, Croughan MS. Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet Gynecol. 2004;103:551–63.
9. Pinborg A, Wennerholm UB, Romundstad LB, Loft A, Aittomaki K, Soderstrom-Anttila V, et al. Why do singletons conceived after assisted reproduction technology have adverse perinatal outcome? Systematic review and meta-analysis. Hum Reprod Update. 2013;19:87–104.
10. Bloise E, Lin W, Liu X, Simbulan R, Kolahi KS, Petraglia F, et al. Impaired placental nutrient transport in mice generated by in vitro fertilization. Endocrinology. 2012;153:3457–67.
11. Chen Z, Robbins KM, Wells KD, Rivera RM. Large offspring syndrome: a bovine model for the human loss-of-imprinting overgrowth syndrome Beckwith-Wiedemann. Epigenetics. 2013;8:591–601.
12. Grazul-Bilska AT, Johnson ML, Borowicz PP, Baranko L, Redmer DA, Reynolds LP. Placental development during early pregnancy in sheep: effects of embryo origin on fetal and placental growth and global methylation. Theriogenology. 2013;79:94–102.
13. Hiendleder S, Mund C, Reichenbach HD, Wenigerkind H, Brem G, Zakhartchenko V, et al. Tissue-specific elevated genomic cytosine methylation levels are associated with an overgrowth phenotype of bovine fetuses derived by in vitro techniques. Biol Reprod. 2004;71:217–23.
14. Hori N, Nagai M, Hirayama M, Hirai T, Matsuda K, Hayashi M, et al. Aberrant Cpg methylation of the imprinting control region Kvdmr1 detected in assisted reproductive technology-produced calves and pathogenesis of large offspring syndrome. Anim Reprod Sci. 2010;122:303–12.
15. Miles JR, Farin CE, Rodriguez KF, Alexander JE, Farin PW. Angiogenesis and morphometry of bovine placentas in late gestation from embryos produced in vivo or in vitro. Biol Reprod. 2004;71:1919–26.
16. Ptak GE, D'Agostino A, Toschi P, Fidanza A, Zacchini F, Czernik M, et al. Post-implantation mortality of in vitro produced embryos is associated with DNA methyltransferase 1 dysfunction in sheep placenta. Hum Reprod. 2013;28:298–305.
17. Sinclair KD, Young LE, Wilmut I, McEvoy TG. In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men. Hum Reprod. 2000;15 Suppl 5:68–86.
18. Young LE, Sinclair KD, Wilmut I. Large offspring syndrome in cattle and sheep. Rev Reprod. 1998;3:155–63.
19. Zhang Y, Zhang YL, Feng C, Wu YT, Liu AX, Sheng JZ, et al. Comparative proteomic analysis of human placenta derived from assisted reproductive technology. Proteomics. 2008;8:4344–56.
20. Huang Q, Li J, Wang F, Oliver MT, Tipton T, Gao Y, et al. Syncytin-1 modulates placental trophoblast cell proliferation by promoting G1/S transition. Cell Signal. 2013;25:1027–35.
21. Chelbi ST, Vaiman D. Genetic and epigenetic factors contribute to the onset of preeclampsia. Mol Cell Endocrinol. 2008;282:120–9.
22. Novakovic B, Saffery R. The ever growing complexity of placental epigenetics—role in adverse pregnancy outcomes and fetal programming. Placenta. 2012;33:959–70.
23. Nelissen EC, van Montfoort AP, Dumoulin JC, Evers JL. Epigenetics and the placenta. Hum Reprod Update. 2011;17:397–417.
24. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2:21–32.
25. Wilkins JF, Haig D. What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet. 2003;4:359–68.
26. Renfree MB, Hore TA, Shaw G, Graves JA, Pask AJ. Evolution of genomic imprinting: insights from marsupials and monotremes. Annu Rev Genomics Hum Genet. 2009;10:241–62.
27. Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, Wang C, et al. Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet. 2007;3:e55.
28. Barbaux S, Gascoin-Lachambre G, Buffat C, Monnier P, Mondon F, Tonanny MB, et al. A genome-wide approach reveals novel imprinted genes expressed in the human placenta. Epigenetics. 2012;7:1079–90.
29. Proudhon C, Duffie R, Ajjan S, Cowley M, Iranzo J, Carbajosa G, et al. Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol Cell. 2012;47:909–20.
30. Court F, Tayama C, Romanelli V, Martin-Trujillo A, Iglesias-Platas I, Okamura K, et al. Genome-wide parent-of-origin DNA methylation analysis reveals the intricacies of human imprinting and suggests a germline methylation-independent mechanism of establishment. Genome Res. 2014;24:554–69.
31. Angiolini E, Fowden A, Coan P, Sandovici I, Smith P, Dean W, et al. Regulation of placental efficiency for nutrient transport by imprinted genes. Placenta. 2006;27(Suppl A):S98–102.
32. Ferguson-Smith AC, Moore T, Detmar J, Lewis A, Hemberger M, Jammes H, et al. Epigenetics and imprinting of the trophoblast—a workshop report. Placenta. 2006;27(Suppl A):S122–6.
33. Messerschmidt DM. Should I, stay or should I go: protection and maintenance of DNA methylation at imprinted genes. Epigenetics. 2012;7:969–75.
34. Fowden AL, Coan PM, Angiolini E, Burton GJ, Constancia M. Imprinted genes and the epigenetic regulation of placental phenotype. Prog Biophys Mol Biol. 2011;106:281–8.
35. Varmuza S, Miri K. What does genetics tell us about imprinting and the placenta connection? Cell Mol Life Sci. 2015;72:51–72.
36. Rahnama F, Shafiei F, Gluckman PD, Mitchell MD, Lobie PE. Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology. 2006;147:5275–83.
37. Serman L, Vlahovic M, Sijan M, Bulic-Jakus F, Serman A, Sincic N, et al. The impact of 5-azacytidine on placental weight, glycoprotein pattern and proliferating cell nuclear antigen expression in rat placenta. Placenta. 2007;28:803–11.
38. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, et al. Placental-specific Igf-Ii Is a major modulator of placental and fetal growth. Nature. 2002;417:945–8.
39. Yin LJ, Zhang Y, Lv PP, He WH, Wu YT, Liu AX, et al. Insufficient maintenance DNA methylation is associated with abnormal embryonic development. BMC Med. 2012;10:26.
40. Banister CE, Koestler DC, Maccani MA, Padbury JF, Houseman EA, Marsit CJ. Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas. Epigenetics. 2011;6:920–7.
41. Salas M, John R, Saxena A, Barton S, Frank D, Fitzpatrick G, et al. Placental growth retardation due to loss of imprinting of Phlda2. Mech Dev. 2004;121:1199–210.
42. Diplas AI, Lambertini L, Lee MJ, Sperling R, Lee YL, Wetmur J, et al. Differential expression of imprinted genes in normal and Iugr human placentas. Epigenetics. 2009;4:235–40.
43. Kumar N, Leverence J, Bick D, Sampath V. Ontogeny of growth-regulating genes in the placenta. Placenta. 2012;33:94–9.
44. McMinn J, Wei M, Schupf N, Cusmai J, Johnson EB, Smith AC, et al. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta. 2006;27:540–9.
45. Apostolidou S, Abu-Amero S, O'Donoghue K, Frost J, Olafsdottir O, Chavele KM, et al. Elevated placental expression of the imprinted Phlda2 gene is associated with low birth weight. J Mol Med (Berl). 2007;85:379–87.
46. Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C, et al. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (Sga) placentae. Dev Biol. 2008;320:79–91.
47. Koukoura O, Sifakis S, Soufla G, Zaravinos A, Apostolidou S, Jones A, et al. Loss of imprinting and aberrant methylation of Igf2 in placentas from pregnancies complicated with fetal growth restriction. Int J Mol Med. 2011;28:481–7.
48. Bourque DK, Avila L, Penaherrera M, von Dadelszen P, Robinson WP. Decreased placental methylation at the H19/Igf2 imprinting control region is associated with normotensive intrauterine growth restriction but not preeclampsia. Placenta. 2010;31:197–202.
49. Ruebner M, Strissel PL, Langbein M, Fahlbusch F, Wachter DL, Faschingbauer F, et al. Impaired cell fusion and differentiation in placentae from patients with intrauterine growth restriction correlate with reduced levels of herv envelope genes. J Mol Med (Berl). 2010;88:1143–56.
50. Ruebner M, Strissel PL, Ekici AB, Stiegler E, Dammer U, Goecke TW, et al. Reduced syncytin-1 expression levels in placental syndromes correlates with epigenetic hypermethylation of the Ervw-1 promoter region. PLoS One. 2013;8:e56145.
51. Reamon-Buettner SM, Buschmann J, Lewin G. Identifying placental epigenetic alterations in an intrauterine growth restriction (Iugr) rat model induced by gestational protein deficiency. Reprod Toxicol. 2014;45:117–24.
52. Ferreira JC, Choufani S, Grafodatskaya D, Butcher DT, Zhao C, Chitayat D, et al. Wnt2 promoter methylation in human placenta is associated with low birthweight percentile in the neonate. Epigenetics. 2011;6:440–9.
53. Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of line-1 repetitive elements. PLoS One. 2011;6:e25254.
54. Kanayama N, Takahashi K, Matsuura T, Sugimura M, Kobayashi T, Moniwa N, et al. Deficiency in P57kip2 expression induces preeclampsia-like symptoms in mice. Mol Hum Reprod. 2002;8:1129–35.
55. Blair JD, Yuen RK, Lim BK, McFadden DE, von Dadelszen P, Robinson WP. Widespread DNA hypomethylation at gene enhancer regions in placentas associated with early-onset pre-eclampsia. Mol Hum Reprod. 2013;19:697–708.
56. Khalkhali-Ellis Z. Maspin: the new frontier. Clin Cancer Res. 2006;12:7279–83.
57. Dokras A, Gardner LM, Kirschmann DA, Seftor EA, Hendrix MJ. The tumour suppressor gene maspin is differentially regulated in cytotrophoblasts during human placental development. Placenta. 2002;23:274–80.
58. Chelbi ST, Mondon F, Jammes H, Buffat C, Mignot TM, Tost J, et al. Expressional and epigenetic alterations of placental serine protease inhibitors: serpina3 is a potential marker of preeclampsia. Hypertension. 2007;49:76–83.
59. Chelbi ST, Wilson ML, Veillard AC, Ingles SA, Zhang J, Mondon F, et al. Genetic and epigenetic mechanisms collaborate to control serpina3 expression and its association with placental diseases. Hum Mol Genet. 2012;21:1968–78.
60. Huang Q, Chen H, Li J, Oliver M, Ma X, Byck D, et al. Epigenetic and non-epigenetic regulation of syncytin-1 expression in human placenta and cancer tissues. Cell Signal. 2014;26:648–56.
61. Yu L, Chen M, Zhao D, Yi P, Lu L, Han J, et al. The H19 gene imprinting in normal pregnancy and pre-eclampsia. Placenta. 2009;30:443–7.
62. Anton L, Brown AG, Bartolomei MS, Elovitz MA. Differential methylation of genes associated with cell adhesion in preeclamptic placentas. PLoS One. 2014;9:e100148.
63. Lazaraviciute G, Kauser M, Bhattacharya S, Haggarty P. A systematic review and meta-analysis of dna methylation levels and imprinting disorders in children conceived by Ivf/Icsi compared with children conceived spontaneously. Hum Reprod Update. 2014;20(6):840–52.
64. Vermeiden JP, Bernardus RE. Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection? Fertil Steril. 2013;99:642–51.
65. van Montfoort AP, Hanssen LL, de Sutter P, Viville S, Geraedts JP, de Boer P. Assisted reproduction treatment and epigenetic inheritance. Hum Reprod Update. 2012;18:171–97.
66. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000;62:1526–35.
67. Fauque P, Jouannet P, Lesaffre C, Ripoche MA, Dandolo L, Vaiman D, et al. Assisted reproductive technology affects developmental kinetics, H19 imprinting control region methylation and H19 gene expression in individual mouse embryos. BMC Dev Biol. 2007;7:116.
68. Liang XW, Cui XS, Sun SC, Jin YX, Heo YT, Namgoong S, et al. Superovulation induces defective methylation in line-1 retrotransposon elements in blastocyst. Reprod Biol Endocrinol. 2013;11:69.
69. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, et al. Selective loss of imprinting in the placenta following preimplantation development in culture. Development. 2004;131:3727–35.
70. Market-Velker BA, Fernandes AD, Mann MR. Side-by-side comparison of five commercial media systems in a mouse model: suboptimal in vitro culture interferes with imprint maintenance. Biol Reprod. 2010;83:938–50.
71. 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. 2010;19:36–51.
72. 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.
73. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod. 2001;64:918–26.
74. de Waal E, Mak W, Calhoun S, Stein P, Ord T, Krapp C, et al. In vitro culture increases the frequency of stochastic epigenetic errors at imprinted genes in placental tissues from mouse concepti produced through assisted reproductive technologies. Biol Reprod. 2014;90:22.
75. Fauque P, Mondon F, Letourneur F, Ripoche MA, Journot L, Barbaux S, et al. In vitro fertilization and embryo culture strongly impact the placental transcriptome in the mouse model. PLoS One. 2010;5:e9218.
76. Hossain MM, Tesfaye D, Salilew-Wondim D, Held E, Proll MJ, Rings F, et al. Massive deregulation of Mirnas from nuclear reprogramming errors during trophoblast differentiation for placentogenesis in cloned pregnancy. BMC Genomics. 2014;15:43.
77. Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, et al. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet. 2009;18:3769–78.
78. Yamagishi S, Matsui T, Nakamura K, Yoshida T, Shimizu K, Takegami Y, et al. Pigment-epithelium-derived factor (Pedf) inhibits angiotensin-ii-induced vascular endothelial growth factor (Vegf) expression in molt-3 T cells through anti-oxidative properties. Microvasc Res. 2006;71:222–6.
79. 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;17:1653–65.
80. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell. 2005;123:917–29.
81. Giritharan G, Delle Piane L, Donjacour A, Esteban FJ, Horcajadas JA, Maltepe E, et al. In vitro culture of mouse embryos reduces differential gene expression between inner cell mass and trophectoderm. Reprod Sci. 2012;19:243–52.
82. Giritharan G, Talbi S, Donjacour A, Di Sebastiano F, Dobson AT, Rinaudo PF. Effect of in vitro fertilization on gene expression and development of mouse preimplantation embryos. Reproduction. 2007;134:63–72.
83. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3l and the establishment of maternal genomic imprints. Science. 2001;294:2536–9.
84. Mercier E, Lissalde-Lavigne G, Gris JC. Jak2 V617f mutation in unexplained loss of first pregnancy. N Engl J Med. 2007;357:1984–5.
85. Vatin M, Bouvier S, Bellazi L, Montagutelli X, Laissue P, Ziyyat A, et al. Polymorphisms of human placental alkaline phosphatase are associated with in vitro fertilization success and recurrent pregnancy loss. Am J Pathol. 2014;184:362–8.
86. Pereza N, Ostojic S, Volk M, Kapovic M, Peterlin B. Matrix metalloproteinases 1, 2, 3 and 9 functional single-nucleotide polymorphisms in idiopathic recurrent spontaneous abortion. Reprod Biomed Online. 2012;24:567–75.
87. Haouzi D, Assou S, Dechanet C, Anahory T, Dechaud H, De Vos J, et al. Controlled ovarian hyperstimulation for in vitro fertilization alters endometrial receptivity in humans: protocol effects. Biol Reprod. 2010;82:679–86.
88. Horcajadas JA, Riesewijk A, Polman J, van Os R, Pellicer A, Mosselman S, et al. Effect of controlled ovarian hyperstimulation in Ivf on endometrial gene expression profiles. Mol Hum Reprod. 2005;11:195–205.
89. Ertzeid G, Storeng R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod. 2001;16:221–5.
90. Farhi J, Ben-Haroush A, Andrawus N, Pinkas H, Sapir O, Fisch B, et al. High serum oestradiol concentrations in Ivf cycles increase the risk of pregnancy complications related to abnormal placentation. Reprod Biomed Online. 2010;21:331–7.
91. Imudia AN, Awonuga AO, Doyle JO, Kaimal AJ, Wright DL, Toth TL, et al. Peak serum estradiol level during controlled ovarian hyperstimulation is associated with increased risk of small for gestational age and preeclampsia in singleton pregnancies after in vitro fertilization. Fertil Steril. 2012;97:1374–9.
92. Pelinck MJ, Keizer MH, Hoek A, Simons AH, Schelling K, Middelburg K, et al. Perinatal outcome in singletons after modified natural cycle Ivf and standard Ivf with ovarian stimulation. Eur J Obstet Gynecol Reprod Biol. 2010;148:56–61.
93. Hu XL, Feng C, Lin XH, Zhong ZX, Zhu YM, Lv PP, et al. High maternal serum estradiol environment in the first trimester is associated with the increased risk of small-for-gestational-age birth. J Clin Endocrinol Metab. 2014;99:2217–24.
94. Mainigi MA, Olalere D, Burd I, Sapienza C, Bartolomei M, Coutifaris C. Peri-implantation hormonal milieu: elucidating mechanisms of abnormal placentation and fetal growth. Biol Reprod. 2014;90:26.
95. Henningsen AK, Pinborg A, Lidegaard O, Vestergaard C, Forman JL, Andersen AN. Perinatal outcome of singleton siblings born after assisted reproductive technology and spontaneous conception: Danish national sibling-cohort study. Fertil Steril. 2011;95:959–63.
96. Pelkonen S, Koivunen R, Gissler M, Nuojua-Huttunen S, Suikkari AM, Hyden-Granskog C, et al. Perinatal outcome of children born after frozen and fresh embryo transfer: the finnish cohort study 1995-2006. Hum Reprod. 2010;25:914–23.
97. Romundstad LB, Romundstad PR, Sunde A, von During V, Skjaerven R, Gunnell D, et al. Effects of technology or maternal factors on perinatal outcome after assisted fertilisation: a population-based cohort study. Lancet. 2008;372:737–43.
98. Pinborg A, Loft A, Aaris Henningsen AK, Rasmussen S, Andersen AN. Infant outcome of 957 singletons born after frozen embryo replacement: the Danish National Cohort Study 1995-2006. Fertil Steril. 2010;94:1320–7.
99. Pinborg A, Henningsen AA, Loft A, Malchau SS, Forman J, Andersen AN. Large baby syndrome in singletons born after frozen embryo transfer (Fet): is it due to maternal factors or the cryotechnique? Hum Reprod. 2014;29:618–27.
100. Sazonova A, Kallen K, Thurin-Kjellberg A, Wennerholm UB, Bergh C. Obstetric outcome in singletons after in vitro fertilization with cryopreserved/thawed embryos. Hum Reprod. 2012;27:1343–50.
101. Amor DJ, Xu JX, Halliday JL, Francis I, Healy DL, Breheny S, et al. Pregnancies conceived using assisted reproductive technologies (Art) have low levels of pregnancy-associated plasma protein-a (Papp-a) leading to a high rate of false-positive results in first trimester screening for Down syndrome. Hum Reprod. 2009;24:1330–8.
102. Bellver J, Casanova C, Garrido N, Lara C, Remohi J, Pellicer A, et al. Additive Effect of factors related to assisted conception on the reduction of maternal serum pregnancy-associated plasma protein a concentrations and the increased false-positive rates in first-trimester Down syndrome screening. Fertil Steril. 2013;100:1314–20.
103. Engels MA, Kooij M, Schats R, Twisk JW, Blankenstein MA, van Vugt JM. First-trimester serum marker distribution in singleton pregnancies conceived with assisted reproduction. Prenat Diagn. 2010;30:372–7.
104. Geipel A, Gembruch U, Berg C. Are first-trimester screening markers altered in assisted reproductive technologies pregnancies? Curr Opin Obstet Gynecol. 2011;23:183–9.
105. Tul N, Novak-Antolic Z. Serum Papp-a levels at 10-14 weeks of gestation are altered in women after assisted conception. Prenat Diagn. 2006;26:1206–11.
106. Fournier T, Handschuh K, Tsatsaris V, Guibourdenche J, Evain-Brion D. Role of nuclear receptors and their ligands in human trophoblast invasion. J Reprod Immunol. 2008;77:161–70.
107. Zhabin SG, Gorin VS, Judin NS. Review: immunomodulatory activity of pregnancy-associated plasma protein-A. J Clin Lab Immunol. 2003;52:41–50.
108. Giorgetti C, Vanden Meerschaut F, De Roo C, Saunier O, Quarello E, Hairion D, et al. Multivariate analysis identifies the estradiol level at ovulation triggering as an independent predictor of the first trimester pregnancy-associated plasma protein-a level in Ivf/Icsi pregnancies. Hum Reprod. 2013;28:2636–42.
109. Gjerris AC, Loft A, Pinborg A, Christiansen M, Tabor A. First-trimester screening markers are altered in pregnancies conceived after Ivf/Icsi. Ultrasound Obstet Gynecol. 2009;33:8–17.
110. Bourgain C, Devroey P. The endometrium in stimulated cycles for Ivf. Hum Reprod Update. 2003;9:515–22.
111. Borghese B, Mondon F, Noel JC, Fayt I, Mignot TM, Vaiman D, et al. Gene expression profile for ectopic versus eutopic endometrium provides new insights into endometriosis oncogenic potential. Mol Endocrinol. 2008;22:2557–62.
112. Szczepanska M, Wirstlein P, Luczak M, Jagodzinski PP, Skrzypczak J. Reduced expression of Hoxa10 in the midluteal endometrium from infertile women with minimal endometriosis. Biomed Pharmacother. 2010;64:697–705.
113. Wu Y, Halverson G, Basir Z, Strawn E, Yan P, Guo SW. Aberrant methylation at Hoxa10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis. Am J Obstet Gynecol. 2005;193:371–80.
114. Kim JJ, Taylor HS, Lu Z, Ladhani O, Hastings JM, Jackson KS, et al. Altered expression of Hoxa10 in endometriosis: potential role in decidualization. Mol Hum Reprod. 2007;13:323–32.
115. Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod. 2009;80:79–85.
116. Chavatte-Palmer P, Camous S, Jammes H, Le Cleac'h N, Guillomot M, Lee RS. Review: placental perturbations induce the developmental abnormalities often observed in bovine somatic cell nuclear transfer. Placenta. 2012;33(Suppl):S99–S104.
117. Suemizu H, Aiba K, Yoshikawa T, Sharov AA, Shimozawa N, Tamaoki N, et al. Expression profiling of placentomegaly associated with nuclear transplantation of mouse Es cells. Dev Biol. 2003;253:36–53.
118. Eskild A, Romundstad PR, Vatten LJ. Placental weight and birthweight: does the association differ between pregnancies with and without preeclampsia? Am J Obstet Gynecol. 2009;201:595. e1-5.
119. Haavaldsen C, Samuelsen SO, Eskild A. The association of maternal age with placental weight: a population-based study of 536,954 pregnancies. BJOG. 2011;118:1470–6.
120. Nelson DB, Ziadie MS, McIntire DD, Rogers BB, Leveno KJ. Placental pathology suggesting that preeclampsia is more than one disease. Am J Obstet Gynecol. 2014;210:66. e1-7.
121. Haavaldsen C, Tanbo T, Eskild A. Placental weight in singleton pregnancies with and without assisted reproductive technology: a population study of 536,567 pregnancies. Hum Reprod. 2012;27:576–82.
122. Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, et al. Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol. 2010;588:527–38.
123. Eckert JJ, Porter R, Watkins AJ, Burt E, Brooks S, Leese HJ, et al. Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS One. 2012;7:e52791.
124. Sun C, Velazquez MA, Marfy-Smith S, Sheth B, Cox A, Johnston DA, et al. Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development. 2014;141:1140–50.
125. Constancia M, Kelsey G, Reik W. Resourceful imprinting. Nature. 2004;432:53–7.
126. Grazul-Bilska AT, Johnson ML, Borowicz PP, Bilski JJ, Cymbaluk T, Norberg SS, et al. Placental development during early pregnancy in sheep: effects of embryo origin on vascularization. Reproduction. 2014;147(5):639–48.
127. Miles JR, Farin CE, Rodriguez KF, Alexander JE, Farin PW. Effects of embryo culture on angiogenesis and morphometry of bovine placentas during early gestation. Biol Reprod. 2005;73:663–71.
128. Fidanza A, Toschi P, Zacchini F, Czernik M, Palmieri C, Scapolo P, et al. Impaired placental vasculogenesis compromises the growth of sheep embryos developed in vitro. Biol Reprod. 2014;91:21.
129. Nelissen EC, Dumoulin JC, Busato F, Ponger L, Eijssen LM, Evers JL, et al. Altered gene expression in human placentas after Ivf/Icsi. Hum Reprod. 2014;29(12):2821–31.
130. Zhang Y, Cui Y, Zhou Z, Sha J, Li Y, Liu J. Altered global gene expressions of human placentae subjected to assisted reproductive technology treatments. Placenta. 2010;31:251–8.
131. Varrault A, Gueydan C, Delalbre A, Bellmann A, Houssami S, Aknin C, et al. Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth. Dev Cell. 2006;11:711–22.
132. Al Adhami H, Evano B, Le Digarcher A, Gueydan C, Dubois E, Parrinello H, et al. A systems-level approach to parental genomic imprinting: the imprinted gene network includes extracellular matrix genes and regulates cell cycle exit and differentiation. Genome Res. 2015;25:353–67.
133. Iglesias-Platas I, Martin-Trujillo A, Petazzi P, Guillaumet-Adkins A, Esteller M, Monk D. Altered expression of the imprinted transcription factor Plagl1 deregulates a network of genes in the human Iugr placenta. Hum Mol Genet. 2014;23(23):6275–85.
134. Camprubi C, Iglesias-Platas I, Martin-Trujillo A, Salvador-Alarcon C, Rodriguez MA, Barredo DR, et al. Stability of genomic imprinting and gestational-age dynamic methylation in complicated pregnancies conceived following assisted reproductive technologies. Biol Reprod. 2013;89:50.
135. Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W, Walter J, et al. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet. 2004;36:1291–5.
136. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 2006;441:349–53.
137. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, et al. Control of developmental regulators by polycomb in human embryonic stem cells. Cell. 2006;125:301–13.
138. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007;447:425–32.
139. Melamed N, Choufani S, Wilkins-Haug LE, Koren G, Weksberg R. Comparison of genome-wide and gene-specific DNA methylation between art and naturally conceived pregnancies. Epigenetics. 2015;10(6):474–83.
140. Shi X, Ni Y, Zheng H, Chen S, Zhong M, Wu F, et al. Abnormal methylation patterns at the Igf2/H19 imprinting control region in phenotypically normal babies conceived by assisted reproductive technologies. Eur J Obstet Gynecol Reprod Biol. 2011;158:52–5.
141. Wong EC, Hatakeyama C, Robinson WP, Ma S. DNA methylation at H19/Igf2 Icr1 in the placenta of pregnancies conceived by in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril. 2011;95:2524–6. e1-3.
142. Rancourt RC, Harris HR, Michels KB. Methylation levels at imprinting control regions are not altered with ovulation induction or in vitro fertilization in a birth cohort. Hum Reprod. 2012;27:2208–16.
143. Tierling S, Souren NY, Gries J, Loporto C, Groth M, Lutsik P, et al. Assisted reproductive technologies do not enhance the variability of DNA methylation imprints in human. J Med Genet. 2010;47:371–6.
144. Nelissen EC, Dumoulin JC, Daunay A, Evers JL, Tost J, van Montfoort AP. Placentas from pregnancies conceived by Ivf/Icsi have a reduced dna methylation level at the H19 and mest differentially methylated regions. Hum Reprod. 2013;28:1117–26.
145. Turan N, Katari S, Gerson LF, Chalian R, Foster MW, Gaughan JP, et al. Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet. 2010;6:e1001033.
146. Zechner U, Pliushch G, Schneider E, El Hajj N, Tresch A, Shufaro Y, et al. Quantitative methylation analysis of developmentally important genes in human pregnancy losses after art and spontaneous conception. Mol Hum Reprod. 2010;16:704–13.
147. Yuen RK, Avila L, Penaherrera MS, von Dadelszen P, Lefebvre L, Kobor MS, et al. Human placental-specific epipolymorphism and its association with adverse pregnancy outcomes. PLoS One. 2009;4:e7389.
148. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261:412–7.
149. Isles AR, Holland AJ. Imprinted genes and mother-offspring Interactions. Early Hum Dev. 2005;81:73–7.
150. Nathanielsz PW. Animal models that elucidate basic principles of the developmental origins of adult diseases. ILAR J. 2006;47:73–82.
151. Reynolds LP, Caton JS. Role of the pre- and post-natal environment in developmental programming of health and productivity. Mol Cell Endocrinol. 2012;354:54–9.
152. Gillman MW. Developmental origins of health and disease. N Engl J Med. 2005;353:1848–50.
153. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359:61–73.
154. Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes. 2001;50:2279–86.
155. Simmons RA. Developmental origins of adult disease. Pediatr Clin North Am. 2009;56:449–66. Table of Contents.
156. Barker DJ, Osmond C, Thornburg KL, Kajantie E, Eriksson JG. The lifespan of men and the shape of their placental surface at birth. Placenta. 2011;32:783–7.
157. Eriksson JG, Kajantie E, Thornburg KL, Osmond C, Barker DJ. Mother's body size and placental size predict coronary heart disease in men. Eur Heart J. 2011;32:2297–303.
158. Barker DJ, Bull AR, Osmond C, Simmonds SJ. Fetal and placental size and risk of hypertension in adult life. BMJ. 1990;301:259–62.
159. Hart R, Norman RJ. The longer-term health outcomes for children born as a result of Ivf treatment: part I—general health outcomes. Hum Reprod Update. 2013;19:232–43.
160. Ceelen M, van Weissenbruch MM, Prein J, Smit JJ, Vermeiden JP, Spreeuwenberg M, et al. Growth during infancy and early childhood in relation to blood pressure and body fat measures at age 8-18 years of Ivf children and spontaneously conceived controls born to subfertile parents. Hum Reprod. 2009;24:2788–95.
161. Ceelen M, van Weissenbruch MM, Roos JC, Vermeiden JP, van Leeuwen FE. Delemarre-van de Waal HA. Body composition in children and adolescents born after in vitro fertilization or spontaneous conception. J Clin Endocrinol Metab. 2007;92:3417–23.
162. Ceelen M, van Weissenbruch MM, Vermeiden JP, van Leeuwen FE. Delemarre-van de Waal HA. Growth and development of children born after in vitro fertilization. Fertil Steril. 2008;90:1662–73.
163. Miles HL, Hofman PL, Peek J, Harris M, Wilson D, Robinson EM, et al. In vitro fertilization improves childhood growth and metabolism. J Clin Endocrinol Metab. 2007;92:3441–5.
164. Sakka SD, Loutradis D, Kanaka-Gantenbein C, Margeli A, Papastamataki M, Papassotiriou I, et al. Absence of insulin resistance and low-grade inflammation despite early metabolic syndrome manifestations in children born after in vitro fertilization. Fertil Steril. 2010;94:1693–9.
165. Portha B, Fournier A, Kioon MD, Mezger V, Movassat J. Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility. Biochimie. 2014;97:1–15.
166. Oliver VF, Miles HL, Cutfield WS, Hofman PL, Ludgate JL, Morison IM. Defects in imprinting and genome-wide DNA methylation are not common in the in vitro fertilization population. Fertil Steril. 2012;97:147–53. e7.
167. Puumala SE, Nelson HH, Ross JA, Nguyen RH, Damario MA, Spector LG. Similar DNA methylation levels in specific imprinting control regions in children conceived with and without assisted reproductive technology: a cross-sectional study. BMC Pediatr. 2012;12:33.
168. Whitelaw N, Bhattacharya S, Hoad G, Horgan GW, Hamilton M, Haggarty P. Epigenetic status in the offspring of spontaneous and assisted conception. Hum Reprod. 2014;29:1452–8.
169. Rexhaj E, Paoloni-Giacobino A, Rimoldi SF, Fuster DG, Anderegg M, Somm E, et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest. 2013;123:5052–60.
170. de Waal E, Yamazaki Y, Ingale P, Bartolomei M, Yanagimachi R, McCarrey JR. Primary epimutations introduced during intracytoplasmic sperm injection (Icsi) are corrected by germline-specific epigenetic reprogramming. Proc Natl Acad Sci U S A. 2012;109:4163–8.
171. Ruiz-Alonso M, Blesa D, Diaz-Gimeno P, Gomez E, Fernandez-Sanchez M, Carranza F, et al. The endometrial receptivity array for diagnosis and personalized embryo transfer as a treatment for patients with repeated implantation failure. Fertil steril. 2013;100:818–24.
172. Maheshwari A, Bhattacharya S. Elective frozen replacement cycles for all: ready for prime time? Hum Reprod. 2013;28:6–9.
173. Petrussa L, Van de Velde H, De Rycke M. Dynamic regulation of DNA methyltransferases in human oocytes and preimplantation embryos after assisted reproductive technologies. Mol Hum Reprod. 2014;20:861–74.
174. Gluckman PD, Lillycrop KA, Vickers MH, Pleasants AB, Phillips ES, Beedle AS, et al. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci U S A. 2007;104:12796–800.
175. Malassine A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003;9:531–9.
176. Wang H, Dey SK. Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet. 2006;7:185–99.
177. Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet. 2001;2:538–48.
178. Basso O, Weinberg CR, Baird DD, Wilcox AJ, Olsen J. Subfecundity as a correlate of preeclampsia: a study within the Danish National Birth Cohort. Am J Epidemiol. 2003;157:195–202.
179. Pandian Z, Bhattacharya S, Templeton A. Review of unexplained infertility and obstetric outcome: a 10 year review. Hum Reprod. 2001;16:2593–7.
180. Horsthemke B, Ludwig M. Assisted reproduction: the epigenetic perspective. Hum Reprod Update. 2005;11:473–82.
181. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon Cpg island context. PLoS Genet. 2009;5:e1000602.
182. Schroeder DI, Blair JD, Lott P, Yu HO, Hong D, Crary F, et al. The human placenta methylome. Proc Natl Acad Sci U S A. 2013;110:6037–42.
183. Wu FR, Liu Y, Shang MB, Yang XX, Ding B, Gao JG, et al. Differences in H3k4 trimethylation in in vivo and in vitro fertilization mouse preimplantation embryos. Genet Mol Res. 2012;11:1099–108.
184. Rosenbluth EM, Shelton DN, Sparks AE, Devor E, Christenson L, Van Voorhis BJ. Microrna expression in the human blastocyst. Fertil Steril. 2013;99:855–61. e3.
185. Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010;31(Suppl):S33–9.
186. Feil D, Lane M, Roberts CT, Kelley RL, Edwards LJ, Thompson JG, et al. Effect of culturing mouse embryos under different oxygen concentrations on subsequent fetal and placental development. J Physiol. 2006;572:87–96.
187. Wang Z, Xu L, He F. Embryo vitrification affects the methylation of the H19/Igf2 differentially methylated domain and the expression of H19 and Igf2. Fertil Steril. 2010;93:2729–33.
188. 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;15:471–7.