Semin Reprod Med 2012; 30(02): 092-104
DOI: 10.1055/s-0032-1307417
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Role of ART in Imprinting Disorders

Ali Eroglu
1   Institute of Molecular Medicine and Genetics
2   Department of Medicine
3   Section of Reproductive Endocrinology, Infertility, and Genetics, Department of Obstetrics and Gynecology
4   Cancer Center
,
Lawrence C. Layman
1   Institute of Molecular Medicine and Genetics
3   Section of Reproductive Endocrinology, Infertility, and Genetics, Department of Obstetrics and Gynecology
5   Neuroscience Program, Medical College of Georgia, Georgia Health Sciences University, Augusta, Georgia
› Author Affiliations
Further Information

Publication History

Publication Date:
27 April 2012 (online)

Abstract

Assisted reproductive technologies (ART) offer revolutionary infertility treatments for millions of childless couples around the world. Currently, ART accounts for 1 to 3% of annual births in industrialized countries and continues to expand rapidly. Except for an increased incidence of premature births, these technologies are considered safe. However, new evidence published during the past decade has suggested an increased incidence of imprinting disorders in children conceived by ART. Specifically, an increased risk was reported for Beckwith-Wiedemann syndrome (BWS), Angelman syndrome (AS), Silver-Russell syndrome, and retinoblastoma. In contrast, some studies have found no association between ART and BWS, AS, Prader-Willi syndrome, transient neonatal diabetes mellitus, and retinoblastoma. The variability in ART protocols and the rarity of imprinting disorders complicate determining the causative relationship between ART and an increased incidence of imprinting disorders. Nevertheless, compelling experimental data from animal studies also suggest a link between increased imprinting disorders and ART. Further comprehensive, appropriately powered studies are needed to better address the magnitude of the risk for ART-associated imprinting disorders. Large longitudinal studies are particularly critical to evaluate long-term effects of ART not only during the perinatal period but also into adulthood. An important consideration is to determine if the implicated association between ART and imprinting disorders is actually related to the procedures or to infertility itself.

 
  • References

  • 1 Zegers-Hochschild F, Adamson GD, de Mouzon J , et al; International Committee for Monitoring Assisted Reproductive Technology; World Health Organization. International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) revised glossary of ART terminology, 2009. Fertil Steril 2009; 92 (5) 1520-1524
  • 2 Evers JL. Female subfertility. Lancet 2002; 360 (9327) 151-159
  • 3 Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 2003; 361 (9373) 1975-1977
  • 4 Koulischer L, Verloes A, Lesenfants S, Jamar M, Herens C. Genetic risk in natural and medically assisted procreation. Early Pregnancy 1997; 3 (3) 164-171
  • 5 DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet 2003; 72 (1) 156-160
  • 6 Maher ER, Brueton LA, Bowdin SC , et al. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet 2003; 40 (1) 62-64
  • 7 Gicquel C, Gaston V, Mandelbaum J, Siffroi JP, Flahault A, Le Bouc Y. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am J Hum Genet 2003; 72 (5) 1338-1341
  • 8 Halliday J, Oke K, Breheny S, Algar E. J Amor D. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet 2004; 75 (3) 526-528
  • 9 Chang AS, Moley KH, Wangler M, Feinberg AP, Debaun MR. Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients. Fertil Steril 2005; 83 (2) 349-354
  • 10 Rossignol S, Steunou V, Chalas C , et al. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region. J Med Genet 2006; 43 (12) 902-907
  • 11 Cox GF, Bürger J, Lip V , et al. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet 2002; 71 (1) 162-164
  • 12 Ørstavik KH, Eiklid K, van der Hagen CB , et al. Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am J Hum Genet 2003; 72 (1) 218-219
  • 13 Ludwig M, Katalinic A, Gross S, Sutcliffe A, Varon R, Horsthemke B. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J Med Genet 2005; 42 (4) 289-291
  • 14 Bliek J, Terhal P, van den Bogaard MJ , et al. Hypomethylation of the H19 gene causes not only Silver-Russell syndrome (SRS) but also isolated asymmetry or an SRS-like phenotype. Am J Hum Genet 2006; 78 (4) 604-614
  • 15 Wakeling EL, Amero SA, Alders M , et al. Epigenotype-phenotype correlations in Silver-Russell syndrome. J Med Genet 2010; 47 (11) 760-768
  • 16 Young LE, Fernandes K, McEvoy TG , et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet 2001; 27 (2) 153-154
  • 17 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 (3) 918-926
  • 18 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 (6) 1526-1535
  • 19 Mann MR, Lee SS, Doherty AS , et al. Selective loss of imprinting in the placenta following preimplantation development in culture. Development 2004; 131 (15) 3727-3735
  • 20 Li T, Vu TH, Ulaner GA , et al. IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Mol Hum Reprod 2005; 11 (9) 631-640
  • 21 Farin PW, Piedrahita JA, Farin CE. Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 2006; 65 (1) 178-191
  • 22 Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007; 22 (1) 26-35
  • 23 Fortier AL, Lopes FL, Darricarrère N, Martel J, Trasler JM. Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Hum Mol Genet 2008; 17 (11) 1653-1665
  • 24 Jablonka E, Lamb MJ. The inheritance of acquired epigenetic variations. J Theor Biol 1989; 139 (1) 69-83
  • 25 Cavalli G, Paro R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 1998; 93 (4) 505-518
  • 26 Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001; 2 (1) 21-32
  • 27 Aguilera O, Fernández AF, Muñoz A, Fraga MF. Epigenetics and environment: a complex relationship. J Appl Physiol 2010; 109 (1) 243-251
  • 28 Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 2010; 21 (4) 214-222
  • 29 Waddington CH. The epigenotype. Endeavour 1942; 1: 18-20
  • 30 Riggs AD, Martiennssen RA, Russo VEA. Epigenetic Mechanisms of Gene Regulation. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1996
  • 31 Bird A. Perceptions of epigenetics. Nature 2007; 447 (7143) 396-398
  • 32 Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev 2009; 23 (7) 781-783
  • 33 Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet 2000; 9 (16) 2395-2402
  • 34 Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99 (3) 247-257
  • 35 Hermann A, Goyal R, Jeltsch A. The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J Biol Chem 2004; 279 (46) 48350-48359
  • 36 Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 2009; 10 (11) 805-811
  • 37 Ooi SK, O'Donnell AH, Bestor TH. Mammalian cytosine methylation at a glance. J Cell Sci 2009; 122 (Pt 16) 2787-2791
  • 38 Carey N, Marques CJ, Reik W. DNA demethylases: a new epigenetic frontier in drug discovery. Drug Discov Today 2011; 16 (15–16) 683-690
  • 39 Tahiliani M, Koh KP, Shen Y , et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324 (5929) 930-935
  • 40 Ito S, Shen L, Dai Q , et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011; 333 (6047) 1300-1303
  • 41 He YF, Li BZ, Li Z , et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011; 333 (6047) 1303-1307
  • 42 Saxonov S, Berg P, Brutlag DL. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A 2006; 103 (5) 1412-1417
  • 43 Larsen F, Gundersen G, Lopez R, Prydz H. CpG islands as gene markers in the human genome. Genomics 1992; 13 (4) 1095-1107
  • 44 Illingworth RS, Bird AP. CpG islands—'a rough guide.'. FEBS Lett 2009; 583 (11) 1713-1720
  • 45 Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci U S A 2002; 99 (6) 3740-3745
  • 46 Shen L, Kondo Y, Guo Y , et al. Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet 2007; 3 (10) 2023-2036
  • 47 Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science 1975; 187 (4173) 226-232
  • 48 Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci U S A 1964; 51: 786-794
  • 49 Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009; 10 (5) 295-304
  • 50 Kouzarides T. Chromatin modifications and their function. Cell 2007; 128 (4) 693-705
  • 51 Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 2009; 10 (1) 32-42
  • 52 Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293 (5532) 1074-1080
  • 53 Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications. Annu Rev Biochem 2011; 80: 473-499
  • 54 The ENCODE; ENCODE Project Consortium. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 2004; 306 (5696) 636-640
  • 55 Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009; 136 (4) 629-641
  • 56 Kaikkonen MU, Lam MT, Glass CK. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res 2011; 90 (3) 430-440
  • 57 Fabbri M, Garzon R, Cimmino A , et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 2007; 104 (40) 15805-15810
  • 58 Friedman JM, Jones PA, Liang G. The tumor suppressor microRNA-101 becomes an epigenetic player by targeting the polycomb group protein EZH2 in cancer. Cell Cycle 2009; 8 (15) 2313-2314
  • 59 Noonan EJ, Place RF, Pookot D , et al. miR-449a targets HDAC-1 and induces growth arrest in prostate cancer. Oncogene 2009; 28 (14) 1714-1724
  • 60 Chuang JC, Jones PA. Epigenetics and microRNAs. Pediatr Res 2007; 61 (5 Pt 2) 24R-29R
  • 61 Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010; 466 (7308) 835-840
  • 62 Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136 (4) 642-655
  • 63 Grewal SI. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 2010; 20 (2) 134-141
  • 64 Kapranov P, Cheng J, Dike S , et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007; 316 (5830) 1484-1488
  • 65 Khalil AM, Guttman M, Huarte M , et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009; 106 (28) 11667-11672
  • 66 Guttman M, Amit I, Garber M , et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009; 458 (7235) 223-227
  • 67 Plath K, Mlynarczyk-Evans S, Nusinow DA, Panning B. Xist RNA and the mechanism of X chromosome inactivation. Annu Rev Genet 2002; 36: 233-278
  • 68 Silva J, Mak W, Zvetkova I , et al. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 2003; 4 (4) 481-495
  • 69 Moazed D. Small RNAs in transcriptional gene silencing and genome defence. Nature 2009; 457 (7228) 413-420
  • 70 Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS. Non-coding RNAs: regulators of disease. J Pathol 2010; 220 (2) 126-139
  • 71 Barton SC, Surani MA, Norris ML. Role of paternal and maternal genomes in mouse development. Nature 1984; 311 (5984) 374-376
  • 72 McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 1984; 37 (1) 179-183
  • 73 Cattanach BM, Kirk M. Differential activity of maternally and paternally derived chromosome regions in mice. Nature 1985; 315 (6019) 496-498
  • 74 Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 1984; 308 (5959) 548-550
  • 75 Mann JR, Lovell-Badge RH. Inviability of parthenogenones is determined by pronuclei, not egg cytoplasm. Nature 1984; 310 (5972) 66-67
  • 76 Hunter P. The silence of genes. Is genomic imprinting the software of evolution or just a battleground for gender conflict?. EMBO Rep 2007; 8 (5) 441-443
  • 77 DeChiara TM, Robertson EJ, Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 1991; 64 (4) 849-859
  • 78 Barlow DP, Stöger R, Herrmann BG, Saito K, Schweifer N. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 1991; 349 (6304) 84-87
  • 79 Bartolomei MS, Zemel S, Tilghman SM. Parental imprinting of the mouse H19 gene. Nature 1991; 351 (6322) 153-155
  • 80 Nicholls RD, Knoll JH, Butler MG, Karam S, Lalande M. Genetic imprinting suggested by maternal heterodisomy in nondeletion Prader-Willi syndrome. Nature 1989; 342 (6247) 281-285
  • 81 Henry I, Bonaiti-Pellié C, Chehensse V , et al. Uniparental paternal disomy in a genetic cancer-predisposing syndrome. Nature 1991; 351 (6328) 665-667
  • 82 Das R, Hampton DD, Jirtle RL. Imprinting evolution and human health. Mamm Genome 2009; 20 (9–10) 563-572
  • 83 Morison IM, Ramsay JP, Spencer HG. A census of mammalian imprinting. Trends Genet 2005; 21 (8) 457-465
  • 84 Thorvaldsen JL, Bartolomei MS. SnapShot: imprinted gene clusters. Cell 2007; 130 (5) 958
  • 85 Royo H, Cavaillé J. Non-coding RNAs in imprinted gene clusters. Biol Cell 2008; 100 (3) 149-166
  • 86 Wutz A, Smrzka OW, Schweifer N, Schellander K, Wagner EF, Barlow DP. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature 1997; 389 (6652) 745-749
  • 87 Yang T, Adamson TE, Resnick JL , et al. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat Genet 1998; 19 (1) 25-31
  • 88 Thorvaldsen JL, Duran KL, Bartolomei MS. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev 1998; 12 (23) 3693-3702
  • 89 Williamson CM, Turner MD, Ball ST , et al. Identification of an imprinting control region affecting the expression of all transcripts in the Gnas cluster. Nat Genet 2006; 38 (3) 350-355
  • 90 Feil R, Walter J, Allen ND, Reik W. Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development 1994; 120 (10) 2933-2943
  • 91 Falls JG, Pulford DJ, Wylie AA, Jirtle RL. Genomic imprinting: implications for human disease. Am J Pathol 1999; 154 (3) 635-647
  • 92 Paulsen M, Ferguson-Smith AC. DNA methylation in genomic imprinting, development, and disease. J Pathol 2001; 195 (1) 97-110
  • 93 Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 2005; 278 (2) 440-458
  • 94 Hajkova P, Ancelin K, Waldmann T , et al. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 2008; 452 (7189) 877-881
  • 95 Hajkova P, Erhardt S, Lane N , et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002; 117 (1–2) 15-23
  • 96 Lee J, Inoue K, Ono R , et al. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 2002; 129 (8) 1807-1817
  • 97 Yamazaki Y, Mann MR, Lee SS , et al. Reprogramming of primordial germ cells begins before migration into the genital ridge, making these cells inadequate donors for reproductive cloning. Proc Natl Acad Sci U S A 2003; 100 (21) 12207-12212
  • 98 Surani MA, Hayashi K, Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell 2007; 128 (4) 747-762
  • 99 Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008; 9 (2) 129-140
  • 100 Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 2000; 9 (19) 2885-2894
  • 101 Obata Y, Kono T. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J Biol Chem 2002; 277 (7) 5285-5289
  • 102 Ueda T, Abe K, Miura A , et al. The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 2000; 5 (8) 649-659
  • 103 Kato Y, Kaneda M, Hata K , et al. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet 2007; 16 (19) 2272-2280
  • 104 Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 2006; 11 (4) 353-361
  • 105 Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004; 13 (8) 839-849
  • 106 Obata Y, Kono T. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J Biol Chem 2002; 277 (7) 5285-5289
  • 107 Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature 2000; 403 (6769) 501-502
  • 108 Oswald J, Engemann S, Lane N , et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol 2000; 10 (8) 475-478
  • 109 Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002; 241 (1) 172-182
  • 110 Rossant J, Sanford JP, Chapman VM, Andrews GK. Undermethylation of structural gene sequences in extraembryonic lineages of the mouse. Dev Biol 1986; 117 (2) 567-573
  • 111 Kerjean A, Dupont JM, Vasseur C , et al. Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum Mol Genet 2000; 9 (14) 2183-2187
  • 112 Geuns E, Hilven P, Van Steirteghem A, Liebaers I, De Rycke M. Methylation analysis of KvDMR1 in human oocytes. J Med Genet 2007; 44 (2) 144-147
  • 113 Khoueiry R, Ibala-Rhomdane S, Méry L , et al. Dynamic CpG methylation of the KCNQ1OT1 gene during maturation of human oocytes. J Med Genet 2008; 45 (9) 583-588
  • 114 Geuns E, De Rycke M, Van Steirteghem A, Liebaers I. Methylation imprints of the imprint control region of the SNRPN-gene in human gametes and preimplantation embryos. Hum Mol Genet 2003; 12 (22) 2873-2879
  • 115 El-Maarri O, Buiting K, Peery EG , et al. Maternal methylation imprints on human chromosome 15 are established during or after fertilization. Nat Genet 2001; 27 (3) 341-344
  • 116 Ecker DJ, Stein P, Xu Z , et al. Long-term effects of culture of preimplantation mouse embryos on behavior. Proc Natl Acad Sci U S A 2004; 101 (6) 1595-1600
  • 117 Schieve LA, Rasmussen SA, Buck GM, Schendel DE, Reynolds MA, Wright VC. Are children born after assisted reproductive technology at increased risk for adverse health outcomes?. Obstet Gynecol 2004; 103 (6) 1154-1163
  • 118 Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med 2002; 346 (10) 725-730
  • 119 Svensson J, Björnståhl A, Ivarsson SA. Increased risk of Silver-Russell syndrome after in vitro fertilization?. Acta Paediatr 2005; 94 (8) 1163-1165
  • 120 Sutcliffe AG, Peters CJ, Bowdin S , et al. Assisted reproductive therapies and imprinting disorders—a preliminary British survey. Hum Reprod 2006; 21 (4) 1009-1011
  • 121 Moll AC, Imhof SM, Cruysberg JR, Schouten-van Meeteren AY, Boers M, van Leeuwen FE. Incidence of retinoblastoma in children born after in-vitro fertilisation. Lancet 2003; 361 (9354) 309-310
  • 122 Schieve LA, Meikle SF, Ferre C, Peterson HB, Jeng G, Wilcox LS. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med 2002; 346 (10) 731-737
  • 123 Reik W, Constância M, Fowden A , et al. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 2003; 547 (Pt 1) 35-44
  • 124 Amor DJ, Halliday J. A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum Reprod 2008; 23 (12) 2826-2834
  • 125 Junien C. Beckwith-Wiedemann syndrome, tumourigenesis and imprinting. Curr Opin Genet Dev 1992; 2 (3) 431-438
  • 126 Weksberg R, Shuman C, Smith AC. Beckwith-Wiedemann syndrome. Am J Med Genet C Semin Med Genet 2005; 137C (1) 12-23
  • 127 Lidegaard O, Pinborg A, Andersen AN. Imprinting diseases and IVF: Danish National IVF cohort study. Hum Reprod 2005; 20 (4) 950-954
  • 128 Källén B, Finnström O, Nygren KG, Olausson PO. In vitro fertilization (IVF) in Sweden: risk for congenital malformations after different IVF methods. Birth Defects Res A Clin Mol Teratol 2005; 73 (3) 162-169
  • 129 Bowdin S, Allen C, Kirby G , et al. A survey of assisted reproductive technology births and imprinting disorders. Hum Reprod 2007; 22 (12) 3237-3240
  • 130 Kishino T, Lalande M, Wagstaff J. UBE3A/E6-AP mutations cause Angelman syndrome. Nat Genet 1997; 15 (1) 70-73
  • 131 Clayton-Smith J, Laan L. Angelman syndrome: a review of the clinical and genetic aspects. J Med Genet 2003; 40 (2) 87-95
  • 132 Abu-Amero S, Wakeling EL, Preece M, Whittaker J, Stanier P, Moore GE. Epigenetic signatures of Silver-Russell syndrome. J Med Genet 2010; 47 (3) 150-154
  • 133 Netchine I, Rossignol S, Dufourg MN , et al. 11p15 imprinting center region 1 loss of methylation is a common and specific cause of typical Russell-Silver syndrome: clinical scoring system and epigenetic-phenotypic correlations. J Clin Endocrinol Metab 2007; 92 (8) 3148-3154
  • 134 Kagami M, Nagai T, Fukami M, Yamazawa K, Ogata T. Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J Assist Reprod Genet 2007; 24 (4) 131-136
  • 135 Moll AC, Kuik DJ, Bouter LM , et al. Incidence and survival of retinoblastoma in The Netherlands: a register based study 1862–1995. Br J Ophthalmol 1997; 81 (7) 559-562
  • 136 Greger V, Passarge E, Höpping W, Messmer E, Horsthemke B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma. Hum Genet 1989; 83 (2) 155-158
  • 137 Ohtani-Fujita N, Dryja TP, Rapaport JM , et al. Hypermethylation in the retinoblastoma gene is associated with unilateral, sporadic retinoblastoma. Cancer Genet Cytogenet 1997; 98 (1) 43-49
  • 138 Anteby I, Cohen E, Anteby E, BenEzra D. Ocular manifestations in children born after in vitro fertilization. Arch Ophthalmol 2001; 119 (10) 1525-1529
  • 139 Lee I, Finger PT, Grifo JA, Rausen AR, Rebarber A, Barad DH. Retinoblastoma in a child conceived by in vitro fertilisation. Br J Ophthalmol 2004; 88 (8) 1098-1099
  • 140 Bradbury BD, Jick H. In vitro fertilization and childhood retinoblastoma. Br J Clin Pharmacol 2004; 58 (2) 209-211
  • 141 Schofield PN, Joyce JA, Lam WK , et al. Genomic imprinting and cancer; new paradigms in the genetics of neoplasia. Toxicol Lett 2001; 120 (1–3) 151-160
  • 142 Lapunzina P, Monk D. The consequences of uniparental disomy and copy number neutral loss-Of-heterozygosity during human development and cancer. Biology of the cell/under the auspices of the European Cell Biology Organization. Bio Cell 2011; 103: 303-317
  • 143 Doornbos ME, Maas SM, McDonnell J, Vermeiden JP, Hennekam RC. Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Human Reproduction 2007; 22: 2476-2480
  • 144 Lim D, Bowdin SC, Tee L , et al. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies. Human reproduction 2009; 24: 741-747