Placenta
Volume 31, Issue 3 , Pages 197-202 , March 2010

Decreased Placental Methylation at the H19/IGF2 Imprinting Control Region is Associated with Normotensive Intrauterine Growth Restriction but not Preeclampsia

  • D.K. Bourque

      Affiliations

    • Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada
    • Child & Family Research Institute, University of British Columbia, Vancouver, BC, Canada
    • ,
  • L. Avila

      Affiliations

    • Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada
    • Child & Family Research Institute, University of British Columbia, Vancouver, BC, Canada
    • ,
  • M. Peñaherrera

      Affiliations

    • Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada
    • Child & Family Research Institute, University of British Columbia, Vancouver, BC, Canada
    • ,
  • P. von Dadelszen

      Affiliations

    • Child & Family Research Institute, University of British Columbia, Vancouver, BC, Canada
    • Department of Obstetrics and Gynaecology, Division of Maternal-Fetal Medicine, University of British Columbia, Vancouver, BC, Canada
    • ,
  • W.P. Robinson

      Affiliations

    • Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada
    • Child & Family Research Institute, University of British Columbia, Vancouver, BC, Canada
    • Corresponding Author InformationCorresponding author. Department of Medical Genetics, University of British Columbia, Child & Family Research Institute, 950 West 28th Avenue, Vancouver, BC V5Z 4H4, Canada. Tel.: +1 604 875 3229.

,Accepted 5 December 2009.

References 

  1. Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet. 2005;365:785–799
  2. Kaufmann P, Black S, Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod. 2003;69:1–7
  3. Granger JP, Alexander BT, Llinas MT, Bennett WA, Khalil RA. Pathophysiology of hypertension during preeclampsia linking placental ischemia with endothelial dysfunction. Hypertension. 2001;38:718–722
  4. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, et al. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta. 2006;27:56–61
  5. Kalousek DK, Vekemans M. Confined placental mosaicism. J Med Genet. 1996;33:529–533
  6. Yong PJ, Langlois S, von Dadelszen P, Robinson WP. The association between preeclampsia and placental trisomy 16 mosaicism. Prenat Diagn. 2006;26:956–961
  7. Fowden AL, Sibley C, Reik W, Constancia M. Imprinted genes, placental development and fetal growth. Horm Res. 2006;65:50–58
  8. 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:S98–S102
  9. Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005;14:R47–R58
  10. 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;62:1526–1535
  11. Mann MRW, 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;131:3727–3735
  12. Monk D, Arnaud P, Apostolidou S, Hills FA, Kelsey G, Stanier P, et al. Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci U S A. 2006;103:6623–6628
  13. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2:21–32
  14. Engel N, West AG, Felsenfeld G, Bartolomei MS. Antagonism between DNA hypermethylation and enhancer-blocking activity at the H19 DMD is uncovered by CpG mutations. Nat Genet. 2004;36:883–888
  15. Gicquel C, Rossignol S, Cabrol S, Houang M, Steunou V, Barbu V, et al. Epimutation of the telomeric imprinting center region on chromosome 11p15 in Silver–Russell syndrome. Nat Genet. 2005;37:1003–1007
  16. Weksberg R, Smith AC, Squire J, Sadowski PD. Beckwith–Wiedemann syndrome demonstrates a role for epigenetic control of normal development. Hum Mol Genet. 2003;12:R61–R68
  17. Weksberg R, Shuman C, Smith AC. Beckwith–Wiedemann syndrome. Am J Med Genet C Semin Med Genet. 2005;137:12–23
  18. 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
  19. Smilinich NJ, Day CD, Fitzpatrick GV, Caldwell GM, Lossie AC, Cooper PR, et al. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith–Wiedemann syndrome. Proc Natl Acad Sci U S A. 1999;96:8064–8069
  20. Schonherr N, Meyer E, Roos A, Schmidt A, Wollmann HA, Eggermann T. The centromeric 11p15 imprinting centre is also involved in Silver–Russell syndrome. J Med Genet. 2007;44:59–63
  21. 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;8:1129–1135
  22. Maher ER, Reik W. Beckwith–Wiedemann syndrome: imprinting in clusters revisited. J Clin Invest. 2000;105:247–252
  23. Wagschal A, Feil R. Genomic imprinting in the placenta. Cytogenet Genome Res. 2006;113:90–98
  24. Kramer MS, Platt RW, Wen SW, Joseph KS, Allen A, Abrahamowicz M, et al. A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics. 2001;108:e35
  25. Magee LA, Helewa M, Moutquin JM, von Dadelszen P. Diagnosis, evaluation, and management of the hypertensive disorders of pregnancy. J Obstet Gynaecol Can. 2008;30:S1–S48
  26. Audibert F, Friedman SA, Frangieh AY, Sibai BM. Clinical utility of strict diagnostic criteria for the HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome. Am J Obstet Gynecol. 1996;175:460–464
  27. Douglas KA, Redman CWG. Eclampsia in the United Kingdom. BMJ. 1994;309:1395–1400
  28. Lestou VS, Lomax BL, Barrett IJ, Kalousek DK. Screening of human placentas for chromosomal mosaicism using comparative genomic hybridization. Teratology. 1999;59:325–330
  29. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98:5116–5121
  30. Kerjean A, Dupont J-, Vasseur C, Le Tessier D, Cuisset L, Paldi A, et al. Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum Mol Genet. 2000;9:2183–2187
  31. Sievers S, Alemazkour K, Zahn S, Perlman EJ, Gillis AJ, Looijenga LH, et al. IGF2/H19 imprinting analysis of human germ cell tumors (GCTs) using the methylation-sensitive single-nucleotide primer extension method reflects the origin of GCTs in different stages of primordial germ cell development. Genes Chromosomes Cancer. 2005;44:256–264
  32. Takai D, Gonzales FA, Tsai YC, Thayer MJ, Jones PA. Large scale mapping of methylcytosines in CTCF-binding sites in the human H19 promoter and aberrant hypomethylation in human bladder cancer. Hum Mol Genet. 2001;10:2619–2626
  33. Penaherrera MS, Weindler S, Van Allen M, Yong SL, Metzger D, McGillivray B, et al. Methylation profiling in individuals with Silver–Russell Syndrome. American Journal of Medical Genetics, in press.
  34. Byun HM, Wong HL, Birnstein EA, Wolff EM, Liang G, Yang AS. Examination of IGF2 and H19 loss of imprinting in bladder cancer. Cancer Res. 2007;67:10753–10758
  35. Weksberg R, Nishikawa J, Caluseriu O, Fei Y-, Shuman C, Wei C, et al. Tumor development in the Beckwith–Wiedemann syndrome is associated with a variety of constitutional molecular 11p15 alterations including imprinting defects of KCNQ1OT1. Hum Mol Genet. 2001;10:2989–3000
  36. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001;293:1068–1070
  37. Abu-Amero SN, Ali Z, Bennett P, Vaughan JI, Moore GE. Expression of the insulin-like growth factors and their receptors in term placentas: a comparison between normal and IUGR births. Mol Reprod Dev. 1998;49:229–235
  38. Reik W, Constância M, Fowden A, Anderson N, Dean W, Ferguson-Smith A, et al. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol. 2003;547:35–44
  39. Constancia M, Kelsey G, Reik W. Resourceful imprinting. Nature. 2004;432:53–57
  40. 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;27:540–549
  41. 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. 2007;85:379–387
  42. Torricelli M, Giovannelli A, Leucci E, De Falco G, Reis FM, Imperatore A, et al. Labor (term and preterm) is associated with changes in the placental mRNA expression of corticotrophin-releasing factor. Reprod Sci. 2007;14:241–245
  43. Torricelli M, Giovannelli A, Leucci E, Florio P, De Falco G, Torres PB, et al. Placental neurokinin B mRNA expression increases at preterm labor. Placenta. 2007;28:1020–1023
  44. Torricelli M, Galleri L, Voltolini C, Biliotti G, Florio P, De Bonis M, et al. Changes of placental Kiss-1 mRNA expression and maternal/cord kisspeptin levels at preterm delivery. Reprod Sci. 2008;15:779–784
  45. Fajardy I, Moitrot E, Vambergue A, Vandersippe-Millot M, Deruelle P, Rousseaux J. Time course analysis of RNA stability in human placenta. BMC Mol Biol. 2009;10:21
  46. Wu Q, Ohsako S, Ishimura R, Suzuki JS, Tohyama C. Exposure of mouse preimplantation embryos to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol Reprod. 2004;70:1790–1797
  47. Haycock PC, Ramsay M. Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the h19 imprinting control region. Biol Reprod. 2009;81:618–627
  48. 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;417:945–948
  49. Sibley CP, Coan PM, Ferguson-Smith AC, Dean W, Hughes J, Smith P, et al. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci U S A. 2004;101:8204–8208
  50. Mayhew TM, Ohadike C, Baker PN, Crocker IP, Mitchell C, Ong SS. Stereological investigation of placental morphology in pregnancies complicated by pre-eclampsia with and without intrauterine growth restriction. Placenta. 2003;24:219–226
  51. 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;30:443–447
  52. 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;36:1291–1295
  53. Robinson WP, Peñaherrera MS, Jiang R, Avila L, Sloan J, McFadden DE, et al. Assessing the role of placental trisomy in preeclampsia and intrauterine growth restriction. Prenat Diagn. 2010;30:1–8

PII: S0143-4004(09)00393-2

doi: 10.1016/j.placenta.2009.12.003

Placenta
Volume 31, Issue 3 , Pages 197-202 , March 2010

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