Partial loss of genomic imprinting reveals important roles for Kcnq1 and Peg10 imprinted domains in placental development

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Koppes, Erik ^a   Himes, Katherine P ^a   Chaillet, J Richard ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; POTASSIUM CHANNEL KCNQ1; PROLACTIN; PROLACTIN 1; PROLIFERIN; RNA H19; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; KCNQ1 PROTEIN, MOUSE; NUCLEAR PROTEIN; PEG10 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL EXPANSION; COMMD1 GENE; CONTROLLED STUDY; CPG ISLAND; DIFFERENTIALLY METHYLATED DOMAIN; DLK1 GENE; DNA METHYLATION; EMBRYO; FEMALE; FETAL WELL BEING; GENE; GENE FUNCTION; GENE STRUCTURE; GENETIC ASSOCIATION; GENOME IMPRINTING; GIANT CELL; H19 GENE; IGF2R GENE; IMPRINT CONTROL REGION; INNER EAR; KCNQ1 GENE; MALE; MEST GENE; MOUSE; NESPAS GENE; NNAT GENE; NONHUMAN; PEG10 GENE; PEG3 GENE; PHENOTYPE; PL2 GENE; PLACENTA DEVELOPMENT; PLACENTA DISORDER; PLACENTA WEIGHT; PLAGL1 GENE; PLF GENE; PROGENY; SEX DIFFERENCE; SNRPN GENE; SPONGIOTROPHOBLAST; TROPHOBLAST; 129 MOUSE; ABNORMALITIES; ANIMAL; DEFICIENCY; ETIOLOGY; FETUS DEATH; GENETICS; GESTATIONAL AGE; LITTER SIZE; METABOLISM; PHYSIOLOGY; PLACENTA; PREGNANCY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; FEMALE; FETAL DEATH; GENOMIC IMPRINTING; GESTATIONAL AGE; KCNQ1 POTASSIUM CHANNEL; LITTER SIZE; MICE; MICE, 129 STRAIN; NUCLEAR PROTEINS; PHENOTYPE; PLACENTA; PREGNANCY; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; TRIGLYCERIDES;

EID: 84941992000     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135202     Document Type: Article

References (45)

1. Reinhart B, Paolini-Giacobino A, Chaillet JR. Specific differentially methylated domain sequences direct the maintenance of methylation at imprinted genes. Mol Cell Biol. 2006; 26:8347-8356 PMID: 16954379
2. MacdonaldW, Mann M. Epigenetic regulation of genomic imprinting from germ line to preimplantation. Mol Reprod Dev. 2014; 81:126-140. doi: 10.1002/mrd.22220 PMID: 23893518
3. Cirio M, Ratnam S, Ding F, Reinhart B, Navara C, Chaillet JR. DNA methyltransferase 1o functions during preimplantation development to preclude a profound level of epigenetic variation. BMC Dev Biol. 2008; 8(1), 9
4. Howell C, Bestor T, Ding F, Latham K, Mertineit C, Trasler J, et al. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell. 2001; 104:829-838 PMID: 11290321
5. Cirio M, Martel J, Mann M, Toppings M, Bartolomei M, Trasler J, et al. DNA methyltransferase 1o functions during preimplantation development to preclude a profound level of epigenetic variation. Dev Biol. 2008; 324:139-150 doi: 10.1016/j.ydbio.2008.09.015 PMID: 18845137
6. Weksberg R, Shuman C, Smith A. Beckwith-Wiedmann Syndrome. Am J Med Genet C. 2005; 137C:12-23
7. Choufani S, Shuman C, Weksberg R. Beckwith-Wiedemann Syndrome. Am J Med Genet C. 2010; 153C:343-354
8. Smith A, Choufani S, Ferreira J, Weksberg R. Growth Regulation, Imprinted Genes, and Chromosome 11p15.5. Pediatr Res. 2007; 61:43R-47R PMID: 17413842
9. Abu-Amero S, Wakeling E., Preece M., Whittaker J., Stanie P, Moore G. Epigenetic Signatures of Silver-Russell Syndrome. 2010. J Med Genet. 47(3) 150-154 doi: 10.1136/jmg.2009.071316 PMID: 20305090
10. Abu-Amero S, Monk D, Frost J, Stanier P, Moore G. The Genetic Aetiology of Silver-Russel Syndrome. 2007; J Med Genet. 45:193-199 PMID: 18156438
11. Coan P, Burton G, Ferguson-Smith A. Imprinted Genes in the Placenta - A Review. Placenta. 2005; 26:S10-S20 PMID: 15837057
12. Frost J, Moore G. The Importance of Imprinting in the Human Placenta. PLoS Genet. 2010; 6(7), e1001015 doi: 10.1371/journal.pgen.1001015 PMID: 20617174
13. Jacobs K, RobinsonWand Lefebvre L. Beckwith-Wiedemann and Silver-Russell syndromes: opposite developmental imbalances in imprinted regulators of placental function and embryonic growth. Clin Genet. 2013; 84:326-334 doi: 10.1111/cge.12143 PMID: 23495910
14. Guillemot F, Nagy A, Auerbach A, Rossant J, Joyner A. Essential Role of Mash-2 in Extraembryonic Development. Nature. 1994; 371:333-336 PMID: 8090202
15. Frank D, Fortino W, Clark L, Musalo R. Wang W, Saxena A, et al. Placental overgrowth in mice lacking the imprinted gene IPL. Proc Natl Acad Sci. 2002; 99:7490-7495 PMID: 12032310
16. Tunster S, Van de Pette M, John R. Fetal overgrowth in the Cdkn1c mouse model of Beckwith-Wiedmann Syndrome. Dis Model Mech. 2011; 4:814-821 doi: 10.1242/dmm.007328 PMID: 21729874
17. Salas M, John R, Axena A, Barton S, Frank D, Fitzpatrick G, et al. Placental growth retardation due to loss of imprinting of phlda2. Mech Dev. 2004; 121:119-1210
18. Tunster S, Tycko B, and John R. The Imprinted Phlda2 Gene Regulates Extraembryonic Energy Stores. Mol Cell Biol. 2010; 30(1):295-306 doi: 10.1128/MCB.00662-09 PMID: 19884348
19. Andrews S, Wood M, Tunster S, Barton S, Surani A, John R. Cdkn1c (p57kip2) is the Major Regulator of Embryonic Growth Within its Imprinted Domain on Mouse Distal Chromosome 7. BMC Dev Biol. 2007; 7:53 PMID: 17517131
20. Constancia M, Hemberger M, Hughes J, Wendy D, 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 PMID: 12087403
21. Coan PM, Fowden AL, Constancia M, Ferguson-Smith AC, Burton GJ, Sibley CP. Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J Physiol. 2008; 586:5023-5032 doi: 10.1113/jphysiol.2008.157313 PMID: 18755750
22. Sun F-L, Dean W, Kelsey G, Allen N, and Reik W. Transactivation of Igf2 in a mouse model of Beckwith-Wiedemann syndrome. Nature. 1997; 389: 809-815 PMID: 9349812
23. Charalambous M, Cowley M, Geoghegan F, Smith F, Radford E, Marlow B, et al. Maternally-inhertied Grb10 reduces placental size and efficiency. Dev Biol. 2010; 337: 1-8 doi: 10.1016/j.ydbio.2009.10. 011 PMID: 19833122
24. Wylie AA, Pulford DJ, McVie-Wylie AJ, Waterland RA, Evans HK, Chen YT et al. Tissue-specific Inactivation of murine M6P/Igf2r. Am J Pathol. 2003; 162:321-328 PMID: 12507915
25. Sekita Y, Wagatsuma H, Nakamura K, Ono R, Kagami M, Wakisaka N, et al. Role of retrotransposonderived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet. 2008; 40:243-248 doi: 10.1038/ng.2007.51 PMID: 18176565
26. Lefebvre L, Viville S, Barton S, Ishino F, Keverne E, Surani A. Abnormal maternal behavior and growth retardation associated with loss of the imprinted gene Mest. Nat Genet. 1998; 20:163-169 PMID: 9771709
27. Ono R, Nakamura K, Inoue K, Naruse M, Usami T, Wakisaka-Saito N, et al. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat Genet. 2006; 38:101-106 PMID: 16341224
28. Li E, Bestor T, and Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 1992; 69:915-926 PMID: 1606615
29. Lei H, Oh S, Okano M, Juttermann R, Gross K et al. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development. 1996; 122:3195-3205 PMID: 8898232
30. Toppings M, Castro C, Mills P, Reinhart B, and Schatten G, Ahrens E, et al. Profound phenotypic variation among mice deficient in the maintenance of genomic imprints. Hum Reprod. 2008; 23:807-818 doi: 10.1093/humrep/den009 PMID: 18276606
31. Himes KP, Koppes E, Chaillet JR. Generalized disruption of inherited genomic imprints leads to wideranging placental defects and dysregulated fetal growth. Dev Biol. 2013; 373: 72-82 doi: 10.1016/j. ydbio.2012.10.010 PMID: 23085235
32. McGraw S, Oakes C, Martel J, Cirio M, de Zeeuw P, Mark W, et al. Loss of DNMT1o disrupts imprinted X chromosome inactivation and accentuates placental defects in females. PLoS Genet. 2013; 9(11): e1003873 doi: 10.1371/journal.pgen.1003873 PMID: 24278026
33. Calvello M, Tabano S, Colapietro P, Maitz S, Pansa A, Augello C, et al. Quantitative DNA methylation analysis improves epigenotype-phenotype correlations in Beckwith-Wiedemann syndrome. Epigenetics. 2013; 8:1053-1060 doi: 10.4161/epi.25812 PMID: 23917791
34. Fuke T, Mizuno S, Nagai T, Hasegawa T, Horikawa R, Miyoshi Y, et al. Molecular and clinical studies in 138 Japanese patients with Silver-Russel Syndrome. PLoS One. 2013; 8(3):e60105 doi: 10.1371/journal.pone.0060105 PMID: 23533668
35. Himes KP, Young A, Koppes E, Stolz D, Barak Y, Sadovsky Y, et al. Loss of inherited genomic imprints in mice leads to severe disruption in placental lipid metabolism. Placenta. 2015; 36:389-396 doi: 10. 1016/j.placenta.2015.01.012 PMID: 25662615
36. Oh-McGinnis R, Bogutz A, Lebebvre L. Partial loss of Ascl2 function affects all three layers of the mouse placenta and causes intrauterine growth restriction. Dev Biol. 2011; 351:277-286 doi: 10.1016/j.ydbio.2011.01.008 PMID: 21238448
37. Green K, Lewis A, Dawson C, Dean W, Reinhart B, et al. A developmental window of opportunity for imprinted gene silencing mediated by DNA methylation and the Kcnq1ot1 noncoding RNA. Mamm Genome. 2007; 18:32-42 PMID: 17245608
38. Arima T, Hata K, Tanaka S, Kusumi M, Li E, Kato K, et al. Loss of the maternal imprint in the Dnmt3Lmat-/-mice leads to a differentiation defect in the extraembryonic tissue. Dev Biol. 2006; 297:361-373 PMID: 16920095
39. Schulz R, Proudhon C, Bestor T, Woodfine K, Lin CS, Lin SP, et al. The parental non-equivalence of imprinting control regions during mammalian development and evolution. PLoS Genet. 2010; 6:(11) e1001214 doi: 10.1371/journal.pgen.1001214 PMID: 21124941
40. Scott IC, Anson-Cartwright L, Riley P, Reda D, Cross JC. The Hand1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol Cell Biol. 2000; 30:530-541
41. Simmons D, Cross JC. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol. 2005; 284:12-24 PMID: 15963972
42. Hu D, Cross JC. Development and function of trophoblast giant cells in the rodent placenta. Int J Dev Biol. 2010; 54:341-354 doi: 10.1387/ijdb.082768dh PMID: 19876834
43. Fitzpatrick G, Soloway P, Higgins M. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMD1. Nat Genet. 2002; 32:426-431 PMID: 12410230
44. Choufani S, Shapiro J, Suisarjo M, Butcher D, Grafodatskaya D, Lou Y, et al. A novel approach identifies new differentially methylated regions (DMRs) associated with imprinted genes. Genome Res. 2011; 21:465-476 doi: 10.1101/gr.111922.110 PMID: 21324877
45. 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 intracacies of human imprinting and suggests a germline methylation-independent mechanism of establishment. Genome Res. 2014; 24:554-569 doi: 10.1101/gr.164913.113 PMID: 24402520