Beckwith-Wiedemann and Silver-Russell syndromes: Opposite developmental imbalances in imprinted regulators of placental function and embryonic growth

Clinical Genetics

Volumn 84, Issue 4, 2013, Pages 326-334

  Jacob, Kj ^a,b   Robinson, W P ^a,c   Lefebvre, L ^a,b  

^a Department of Medical Genetics ^*  (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Beckwith Wiedemann syndrome; Genomic imprinting; Imprinted genes; Silver Russell syndrome

Indexed keywords

ARTICLE; ASCL2 GENE; BECKWITH WIEDEMANN SYNDROME; CDKN1C GENE; CHROMOSOME 11P; EMBRYO GROWTH; EPIGENETICS; GENE; GENE CLUSTER; GENE EXPRESSION; GENE MAPPING; GENETIC DISORDER; GENOME IMPRINTING; GENOTYPE; H19 GENE; IGF2 GENE; MEST GENE; NONHUMAN; PHENOTYPE; PHLDA2 GENE; PLACENTA FUNCTION; PRIORITY JOURNAL; SILVER RUSSELL SYNDROME;

BECKWITH-WIEDEMANN SYNDROME; GENOMIC IMPRINTING; IMPRINTED GENES; SILVER-RUSSELL SYNDROME;

ANIMALS; BECKWITH-WIEDEMANN SYNDROME; CHROMOSOMES, HUMAN, PAIR 11; EMBRYONIC DEVELOPMENT; FEMALE; GENOMIC IMPRINTING; HUMANS; PHENOTYPE; PLACENTA; PREGNANCY; SILVER-RUSSELL SYNDROME;

EID: 84883789858     PISSN: 00099163     EISSN: 13990004     Source Type: Journal    
DOI: 10.1111/cge.12143     Document Type: Article

References (90)

1. Abu-Amero S, Monk D, Frost J, Preece M, Stanier P, Moore GE. The genetic aetiology of Silver-Russell syndrome. J Med Genet 2008: 45: 193-199.
2. Eggermann T, Wollmann HA, Kuner R et al. Molecular studies in 37 Silver-Russell syndrome patients: frequency and etiology of uniparental disomy. Hum Genet 1997: 100: 415-419.
3. Kotzot D, Schmitt S, Bernasconi F et al. Uniparental disomy 7 in Silver-Russell syndrome and primordial growth retardation. Hum Mol Genet 1995: 4: 583-587.
4. Preece MA, Price SM, Davies V et al. Maternal uniparental disomy 7 in Silver-Russell syndrome. J Med Genet 1997: 34: 6-9.
5. Eggermann T, Spengler S, Begemann M et al. Deletion of the paternal allele of the imprinted MEST/PEG1 region in a patient with Silver-Russell syndrome features. Clin Genet 2012: 81: 298-300.
6. Lefebvre L, Viville S, Barton SC, Ishino F, Keverne EB, Surani MA. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat Genet 1998: 20: 163-169.
7. Eggermann T, Meyer E, Obermann C et al. Is maternal duplication of 11p15 associated with Silver-Russell syndrome? J Med Genet 2005: 42: e26.
8. Gicquel C, Rossignol S, Cabrol S et al. Epimutation of the telomeric imprinting center region on chromosome 11p15 in Silver-Russell syndrome. Nat Genet 2005: 37: 1003-1007.
9. Weksberg R, Shuman C, Beckwith JB. Beckwith-Wiedemann syndrome. Eur J Hum Genet 2010: 18: 8-14.
10. Bartolomei MS, Webber AL, Brunkow ME, Tilghman SM. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev 1993: 7: 1663-1673.
11. Ferguson-Smith AC, Sasaki H, Cattanach BM, Surani MA. Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 1993: 362: 751-755.
12. Tremblay KD, Saam JR, Ingram RS, Tilghman SM, Bartolomei MS. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat Genet 1995: 9: 407-413.
13. Li J-Y, Lees-Murdock DJ, Xu G-L, Walsh CP. Timing of establishment of paternal methylation imprints in the mouse. Genomics 2004: 84: 952-960.
14. Bell AC, Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000: 405: 482-485.
15. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000: 405: 486-489.
16. Smilinich NJ, Day CD, Fitzpatrick GV 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 USA 1999: 96: 8064-8069.
17. Lee MP, DeBaun MR, Mitsuya K et al. Loss of imprinting of a paternally expressed transcript, with antisense orientation to KVLQT1, occurs frequently in Beckwith-Wiedemann syndrome and is independent of insulin-like growth factor II imprinting. Proc Natl Acad Sci USA 1999: 96: 5203-5208.
18. Fitzpatrick GV, Soloway PD, Higgins MJ. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat Genet 2002: 32: 426-431.
19. Oh R, Ho R, Mar L et al. Epigenetic and phenotypic consequences of a truncation disrupting the imprinted domain on distal mouse chromosome 7. Mol Cell Biol 2008: 28: 1092-1103.
20. Bonaldi A, Mazzeu JF, Costa SS et al. Microduplication of the ICR2 domain at chromosome 11p15 and familial Silver-Russell syndrome. Am J Med Genet A 2011: 155A: 2479-2483.
21. Schönherr 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 2006: 44: 59-63.
22. Demars J, Gicquel C. Epigenetic and genetic disturbance of the imprinted 11p15 region in Beckwith-Wiedemann and Silver-Russell syndromes. Clin Genet 2012: 81: 350-361.
23. DeChiara TM, Robertson EJ, Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 1991: 64: 849-859.
24. Lee JE, Pintar J, Efstratiadis A. Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis. Development 1990: 110: 151-159.
25. Redline RW, Chernicky CL, Tan HQ, Ilan J. Differential expression of insulin-like growth factor-II in specific regions of the late (post day 9.5) murine placenta. Mol Reprod Dev 1993: 36: 121-129.
26. Eggenschwiler J, Ludwig T, Fisher P, Leighton PA, Tilghman SM, Efstratiadis A. Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev 1997: 11: 3128-3142.
27. DeChiara TM, Efstratiadis A, Robertson EJ. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 1990: 345: 78-80.
28. Moore T, Constancia M, Zubair M et al. Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc Natl Acad Sci USA 1997: 94: 12509-12514.
29. Constância M, Hemberger M, Hughes J et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002: 417: 945-948.
30. Monk D, Sanches R, Arnaud P et al. Imprinting of IGF2 P0 transcript and novel alternatively spliced INS-IGF2 isoforms show differences between mouse and human. Hum Mol Genet 2006: 15: 1259-1269.
31. Brannan CI, Dees EC, Ingram RS, Tilghman SM. The product of the H19 gene may function as an RNA. Mol Cell Biol 1990: 10: 28-36.
32. Pachnis V, Brannan CI, Tilghman SM. The structure and expression of a novel gene activated in early mouse embryogenesis. EMBO J 1988: 7: 673-681.
33. Keniry A, Oxley D, Monnier P et al. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nature 2012: 14: 659-665.
34. Poirier F, Chan CT, Timmons PM, Robertson EJ, Evans MJ, Rigby PW. The murine H19 gene is activated during embryonic stem cell differentiation in vitro and at the time of implantation in the developing embryo. Development 1991: 113: 1105-1114.
35. Hao Y, Crenshaw T, Moulton T, Newcomb E, Tycko B. Tumour-suppressor activity of H19 RNA. Nature 1993: 365: 764-767.
36. Yoshimizu T, Miroglio A, Ripoche M-A et al. The H19 locus acts in vivo as a tumor suppressor. Proc Natl Acad Sci USA 2008: 105: 12417-12422.
37. Moulton T, Crenshaw T, Hao Y et al. Epigenetic lesions at the H19 locus in Wilms' tumour patients. Nat Genet 1994: 7: 440-447.
38. Taniguchi T, Sullivan MJ, Ogawa O, Reeve AE. Epigenetic changes encompassing the IGF2/H19 locus associated with relaxation of IGF2 imprinting and silencing of H19 in Wilms tumor. Proc Natl Acad Sci USA 1995: 92: 2159-2163.
39. Ainscough JF, Koide T, Tada M, Barton S, Surani MA. Imprinting of Igf2 and H19 from a 130kb YAC transgene. Development 1997: 124: 3621-3632.
40. Gabory A, Ripoche M-A, Le Digarcher A et al. H19 acts as a trans regulator of the imprinted gene network controlling growth in mice. Development 2009: 136: 3413-3421.
41. Pfeifer K, Leighton PA, Tilghman SM. The structural H19 gene is required for transgene imprinting. Proc Natl Acad Sci USA 1996: 93: 13876-13883.
42. Kono T, Sotomaru Y, Katsuzawa Y, Dandolo L, Dandolo L. Mouse parthenogenetic embryos with monoallelic H19 expression can develop to day 17.5 of gestation. Dev Biol 2002: 243: 294-300.
43. Cai X, Cullen BR. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 2007: 13: 313-316.
44. Mineno J, Okamoto S, Ando T et al. The expression profile of microRNAs in mouse embryos. Nucleic Acids Res 2006: 34: 1765-1771.
45. Smits G, Mungall AJ, Griffiths-Jones S et al. Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat Genet 2008: 40: 971-976.
46. Ripoche MA, Kress C, Poirier F, Dandolo L. Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev 1997: 11: 1596-1604.
47. Azzi S, Rossignol S, Steunou V et al. Multilocus methylation analysis in a large cohort of 11p15-related foetal growth disorders (Russell-Silver and Beckwith-Wiedemann syndromes) reveals simultaneous loss of methylation at paternal and maternal imprinted loci. Hum Mol Genet 2009: 18: 4724-4733.
48. Demars J, Rossignol S, Netchine I et al. New insights into the pathogenesis of Beckwith-Wiedemann and Silver-Russell syndromes: contribution of small copy number variations to 11p15 imprinting defects. Hum Mutat 2011: 32: 1171-1182.
49. Berteaux N, Aptel N, Cathala G et al. A novel H19 antisense RNA overexpressed in breast cancer contributes to paternal IGF2 expression. Mol Cell Biol 2008: 28: 6731-6745.
50. Tran VG, Court F, Duputié A et al. H19 antisense RNA can up-regulate Igf2 transcription by activation of a novel promoter in mouse myoblasts. PLoS One 2012: 7: e37923.
51. Guillemot F, Caspary T, Tilghman SM et al. Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat Genet 1995: 9: 235-242.
52. Guillemot F, Nagy A, Auerbach A, Rossant J, Joyner AL. Essential role of Mash-2 in extraembryonic development. Nature 1994: 371: 333-336.
53. Rossant J, Guillemot F, Tanaka M, Latham K, Gertenstein M, Nagy A. Mash2 is expressed in oogenesis and preimplantation development but is not required for blastocyst formation. Mech Dev 1998: 73: 183-191.
54. Lefebvre L, Mar L, Bogutz A et al. The interval between Ins2 and Ascl2 is dispensable for imprinting centre function in the murine Beckwith-Wiedemann region. Hum Mol Genet 2009: 18: 4255-4267.
55. Oh-McGinnis R, Bogutz AB, Lefebvre L. Partial loss of Ascl2 function affects all three layers of the mature placenta and causes intrauterine growth restriction. Dev Biol 2011: 351: 277-286.
56. Alders M, Hodges M, Hadjantonakis AK et al. The human Achaete-Scute homologue 2 (ASCL2, HASH2) maps to chromosome 11p15.5, close to IGF2 and is expressed in extravillus trophoblasts. Hum Mol Genet 1997: 6: 859-867.
57. Miyamoto T, Hasuike S, Jinno Y et al. The human ASCL2 gene escaping genomic imprinting and its expression pattern. J Assist Reprod Genet 2002: 19: 240-244.
58. Westerman B. The human achaete scute homolog 2 gene contains two promotors, generating overlapping transcripts and encoding two proteins with different nuclear localization. Placenta 2001: 22: 511-518.
59. Eggermann T. Silver-Russell and Beckwith-Wiedemann syndromes: opposite (epi)mutations in 11p15 result in opposite clinical pictures. Horm Res 2009: 71 (Suppl. 2): 30-35.
60. Matsuoka S, Edwards MC, Bai C et al. p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev 1995: 9: 650-662.
61. Westbury J, Watkins M, Ferguson-Smith AC, Smith J. Dynamic temporal and spatial regulation of the cdk inhibitor p57(kip2) during embryo morphogenesis. Mech Dev 2001: 109: 83-89.
62. Andrews SC, Wood MD, Tunster SJ et al. Cdkn1c (p57Kip2) is the major regulator of embryonic growth within its imprinted domain on mouse distal chromosome 7. BMC Dev Biol 2007: 7: 53.
63. Tunster SJ, Van de Pette M, John RM. Fetal overgrowth in the Cdkn1c mouse model of Beckwith-Wiedemann syndrome. Dis Model Mech 2011: 4: 814-821.
64. Yan Y, Frisén J, Lee MH, Massagué J, Barbacid M. Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev 1997: 11: 973-983.
65. Zhang P, Liégeois NJ, Wong C et al. Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 1997: 387: 151-158.
66. Simmons DG, Natale DRC, Begay V, Hughes M, Leutz A, Cross JC. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008: 135: 2083-2091.
67. Zhang P, Wong C, DePinho RA, Harper JW, Elledge SJ. Cooperation between the Cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development. Genes Dev 1998: 12: 3162-3167.
68. Caspary T, Cleary MA, Perlman EJ, Zhang P, Elledge SJ, Tilghman SM. Oppositely imprinted genes p57 (Kip2) and igf2 interact in a mouse model for Beckwith-Wiedemann syndrome. Genes Dev 1999: 13: 3115-3124.
69. Bhogal B, Arnaudo A, Dymkowski A, Best A, Davis TL. Methylation at mouse Cdkn1c is acquired during postimplantation development and functions to maintain imprinted expression. Genomics 2004: 84: 961-970.
70. Yatsuki H, Joh K, Higashimoto K et al. Domain regulation of imprinting cluster in Kip2/Lit1 subdomain on mouse chromosome 7 F4/F5: large-scale DNA methylation analysis reveals that DMR-Lit1 is a putative imprinting control region. Genome Res 2002: 12: 1860-1870.
71. Lewis A, Mitsuya K, Umlauf D et al. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat Genet 2004: 36: 1291-1295.
72. John RM, Lefebvre L. Developmental regulation of somatic imprints. Differentiation 2011: 81: 270-280.
73. Caspary T, Cleary MA, Baker CC, Guan XJ, Tilghman SM. Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Mol Cell Biol 1998: 18: 3466-3474.
74. Fan T, Hagan JP, Kozlov SV, Stewart CL, Muegge K. Lsh controls silencing of the imprinted Cdkn1c gene. Development 2005: 132: 635-644.
75. Yuen RK, Jiang R, Peñaherrera MS, Mcfadden DE, Robinson WP. Genome-wide mapping of imprinted differentially methylated regions by DNA methylation profiling of human placentas from triploidies. Epigenetics Chromatin 2011: 4: 10.
76. Frank D, Mendelsohn CL, Ciccone E, Svensson K, Ohlsson R, Tycko B. A novel pleckstrin homology-related gene family defined by Ipl/Tssc3, TDAG51, and Tih1: tissue-specific expression, chromosomal location, and parental imprinting. Mamm Genome 1999: 10: 1150-1159.
77. Qian N, Frank D, O'Keefe D et al. The IPL gene on chromosome 11p15.5 is imprinted in humans and mice and is similar to TDAG51, implicated in Fas expression and apoptosis. Hum Mol Genet 1997: 6: 2021-2029.
78. Frank D, Fortino W, Clark L et al. Placental overgrowth in mice lacking the imprinted gene Ipl. Proc Natl Acad Sci USA 2002: 99: 7490-7495.
79. Salas M, John R, Saxena A et al. Placental growth retardation due to loss of imprinting of Phlda2. Mech Dev 2004: 121: 1199-1210.
80. Grandjean V, Smith J, Schofield PN, Ferguson-Smith AC. Increased IGF-II protein affects p57kip2 expression in vivo and in vitro: implications for Beckwith-Wiedemann syndrome. Proc Natl Acad Sci USA 2000: 97: 5279-5284.
81. Veronese A, Lupini L, Consiglio J et al. Oncogenic role of miR-483-3p at the IGF2/483 locus. Cancer Res 2010: 70: 3140-3149.
82. Cerrato F, Sparago A, Di Matteo I et al. The two-domain hypothesis in Beckwith-Wiedemann syndrome: autonomous imprinting of the telomeric domain of the distal chromosome 7 cluster. Hum Mol Genet 2005: 14: 503-511.
83. Onyango P, Feinberg AP. A nucleolar protein, H19 opposite tumor suppressor (HOTS), is a tumor growth inhibitor encoded by a human imprinted H19 antisense transcript. Proc Natl Acad Sci USA 2011: 108: 16759-16764.
84. Kannenberg K, Weber K, Binder C, Urban C, Kirschner H-J, Binder G. IGF2/H19 hypomethylation is tissue, cell, and CpG site dependent and not correlated with body asymmetry in adolescents with Silver-Russell syndrome. Clin Epigenetics 2012: 4: 15.
85. Binder G, Seidel A-K, Weber K et al. IGF-II serum levels are normal in children with Silver-Russell syndrome who frequently carry epimutations at the IGF2 locus. J Clin Endocrinol Metab 2006: 91: 4709-4712.
86. Searle AG, Beechey CV. Genome imprinting phenomena on mouse chromosome 7. Genet Res 1990: 56: 237-244.
87. Mclaughlin KJ, Szabó P, Haegel H, Mann JR. Mouse embryos with paternal duplication of an imprinted chromosome 7 region die at midgestation and lack placental spongiotrophoblast. Development 1996: 122: 265-270.
88. Rentsendorj A, Mohan S, Szabó P, Mann JR. A genomic imprinting defect in mice traced to a single gene. Genetics 2010: 186: 917-927.
89. Bliek J, Verde G, Callaway J et al. Hypomethylation at multiple maternally methylated imprinted regions including PLAGL1 and GNAS loci in Beckwith-Wiedemann syndrome. Eur J Hum Genet 2009: 17: 611-619.
90. Hanel ML, Wevrick R. The role of genomic imprinting in human developmental disorders: lessons from Prader-Willi syndrome. Clin Genet 2001: 59: 156-164.