A genome-wide approach reveals novel imprinted genes expressed in the human placenta

Epigenetics

Volumn 7, Issue 9, 2012, Pages 1079-1090

  Barbaux, Sandrine ^a,b,c   Gascoin Lachambre, Géraldine ^a,b,c,d   Buffat, Christophe ^e,f   Monnier, Paul ^a,b,c   Mondon, Françoise ^a,b,c   Tonanny, Marie Béatrice ^a,b,c   Pinard, Amélie ^a,b,c   Auer, Jana ^a,b,c   Bessières, Bettina ^g   Barlier, Anne ^f,h   Jacques, Sébastien ^a,b,c   Simeoni, Umberto ^f,h   Dandolo, Luisa ^a,b,c   Letourneur, Franck ^a,b,c   Jammes, Hélène ^i,j   Vaiman, Daniel ^a,b,c  

^a INSTITUT COCHIN   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d AP HP ^*  (France)

^e AIX MARSEILLE UNIVERSITÉ   (France)

^f HÔPITAL DE LA CONCEPTION   (France)

^g Institut de Puericulture   (France)

^h AIX MARSEILLE UNIVERSITY   (France)

ⁱ INRA Institut National de la Recherche Agronomique   (France)

^j ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

more..

Author keywords

Gene; Monoallelic expression; Parental imprinting; Placenta; Zinc finger

Indexed keywords

COMPLEMENTARY DNA; COMPLEMENTARY RNA; GENOMIC DNA; GLIS3 PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; INPP5F PROTEIN; IPW PROTEIN; LIN28B PROTEIN; MAGI2 PROTEIN; MESSENGER RNA; NTM PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZC3H12C PROTEIN; ZFAT AS1 PROTEIN; ZFAT PROTEIN; ZNF597 PROTEIN;

ALLELE; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA MICROARRAY; DOWN REGULATION; ENDOTHELIUM CELL; FILTRATION; GENE EXPRESSION; GENE LOCUS; GENOME IMPRINTING; GENOTYPE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; PLACENTA; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; SYNCYTIOTROPHOBLAST;

MUS;

EID: 84866098740     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.21495     Document Type: Article

References (71)

1. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001; 2:21-32; http://dx.doi.org/10.1038/35047554.
2. Varrault A, Gueydan C, Delalbre A, Bellmann A, Houssami S, Aknin C, et al. Zac1 regulates an imprint-ed gene network critically involved in the control of embryonic growth. Dev Cell 2006; 11:711-22; http://dx.doi.org/10.1016/j.dev-cel.2006.09.003.
3. Graves JA. Genomic imprinting, development and disease--is pre-eclampsia caused by a maternally imprinted gene? Reprod Fertil Dev 1998; 10:23-9; http://dx.doi.org/10.1071/R98014.
4. Fenstad MH, Johnson MP, Løset M, Mundal SB, Roten LT, Eide IP, et al. STOX2 but not STOX1 is differen-tially expressed in decidua from pre-eclamptic women: data from the Second Nord-Trondelag Health Study. Mol Hum Reprod 2010; 16:960-8; http://dx.doi.org/10.1093/molehr/gaq064.
5. 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; http://dx.doi.org/10.1093/molehr/8.12.1129.
6. Rigourd V, Chauvet C, Chelbi ST, Rebourcet R, Mondon F, Letourneur F, et al. STOX1 overexpres-sion in choriocarcinoma cells mimics transcriptional alterations observed in preeclamptic placentas. PLoS One 2008; 3:e3905; http://dx.doi.org/10.1371/journal.pone.0003905.
7. van Dijk M, Mulders J, Poutsma A, Könst AA, Lachmeijer AM, Dekker GA, et al. Maternal seg-regation of the Dutch preeclampsia locus at 10q22 with a new member of the winged helix gene family. Nat Genet 2005; 37:514-9; http://dx.doi.org/10.1038/ng1541.
8. van Dijk M, van Bezu J, Poutsma A, Veerhuis R, Rozemuller AJ, Scheper W, et al. The pre-eclampsia gene STOX1 controls a conserved pathway in placenta and brain upregulated in late-onset Alzheimer's disease. J Alzheimers Dis 2010; 19:673-9;
9. Brideau CM, Eilertson KE, Hagarman JA, Bustamante CD, Soloway PD. Successful computational prediction of novel imprinted genes from epigenomic features. Mol Cell Biol 2010; 30:3357-70; http://dx.doi.org/10.1128/MCB.01355-09.
10. Hutter B, Bieg M, Helms V, Paulsen M. Imprinted genes show unique patterns of sequence conservation. BMC Genomics 2010; 11:649; http://dx.doi.org/10.1186/1471-2164-11-649.
11. Luedi PP, Dietrich FS, Weidman JR, Bosko JM, Jirtle RL, Hartemink AJ. Computational and experimen-tal identification of novel human imprinted genes. Genome Res 2007; 17:1723-30; http://dx.doi.org/10.1101/gr.6584707.
12. Luedi PP, Hartemink AJ, Jirtle RL. Genome-wide prediction of imprinted murine genes. Genome Res 2005; 15:875-84; http://dx.doi.org/10.1101/gr.3303505.
13. Pollard KS, Serre D, Wang X, Tao H, Grundberg E, Hudson TJ, et al. A genome-wide approach to identifying novel-imprinted genes. Hum Genet 2008; 122:625-34; http://dx.doi.org/10.1007/s00439-007-0440-1.
14. Wang Z, Fan H, Yang HH, Hu Y, Buetow KH, Lee MP. Comparative sequence analysis of imprinted genes between human and mouse to reveal imprinting signa-tures. Genomics 2004; 83:395-401; http://dx.doi.org/10.1016/j.ygeno.2003.09.007.
15. Yang HH, Hu Y, Edmonson M, Buetow K, Lee MP. Computation method to identify differential allelic gene expression and novel imprinted genes. Bioinformatics 2003; 19:952-5; http://dx.doi.org/10.1093/bioinformatics/btg127.
16. Choufani S, Shapiro JS, Susiarjo M, Butcher DT, Grafodatskaya D, Lou Y, et al. A novel approach identifies new differentially methylated regions (DMRs) associated with imprinted genes. Genome Res 2011; 21:465-76; http://dx.doi.org/10.1101/gr.111922.110.
17. Ruf N, Dünzinger U, Brinckmann A, Haaf T, Nürnberg P, Zechner U. Expression profiling of uni-parental mouse embryos is inefficient in identify-ing novel imprinted genes. Genomics 2006; 87:509-19; http://dx.doi.org/10.1016/j.ygeno.2005.12.007.
18. Smith RJ, Dean W, Konfortova G, Kelsey G. Identification of novel imprinted genes in a genome-wide screen for maternal methylation. Genome Res 2003; 13:558-69; http://dx.doi.org/10.1101/gr.781503.
19. Sritanaudomchai H, Ma H, Clepper L, Gokhale S, Bogan R, Hennebold J, et al. Discovery of a novel imprinted gene by transcriptional analysis of parthenogenetic embryonic stem cells. Hum Reprod 2010; 25:1927-41; http://dx.doi.org/10.1093/humrep/deq144.
20. Ruf N, Bähring S, Galetzka D, Pliushch G, Luft FC, Nürnberg P, et al. Sequence-based bioinformatic predic-tion and QUASEP identify genomic imprinting of the KCNK9 potassium channel gene in mouse and human. Hum Mol Genet 2007; 16:2591-9; http://dx.doi.org/10.1093/hmg/ddm216.
21. Pant PV, Tao H, Beilharz EJ, Ballinger DG, Cox DR, Frazer KA. Analysis of allelic differential expression in human white blood cells. Genome Res 2006; 16:331-9; http://dx.doi.org/10.1101/gr.4559106.
22. Yoshida Y, Tsunoda T, Takashima Y, Fujimoto T, Doi K, Sasazuki T, et al. ZFAT is essential for endothelial cell assembly and the branch point formation of capillary-like structures in an angiogenesis model. Cell Mol Biol Lett 2010; 15:541-50; http://dx.doi.org/10.2478/s11658-010-0028-y.
23. Shirasawa S, Harada H, Furugaki K, Akamizu T, Ishikawa N, Ito K, et al. SNPs in the promoter of a B cell-specific antisense transcript, SAS-ZFAT, deter-mine susceptibility to autoimmune thyroid disease. Hum Mol Genet 2004; 13:2221-31; http://dx.doi.org/10.1093/hmg/ddh245.
24. Cattanach BM, Kirk M. Differential activity of mater-nally and paternally derived chromosome regions in mice. Nature 1985; 315:496-8; http://dx.doi.org/10.1038/315496a0.
25. Kanber D, Berulava T, Ammerpohl O, Mitter D, Richter J, Siebert R, et al. The human retinoblastoma gene is imprinted. PLoS Genet 2009; 5:e1000790; http://dx.doi.org/10.1371/journal.pgen.1000790.
26. Daelemans C, Ritchie ME, Smits G, Abu-Amero S, Sudbery IM, Forrest MS, et al. High-throughput analysis of candidate imprinted genes and allele-specific gene expression in the human term placenta. BMC Genet 2010; 11:25; http://dx.doi.org/10.1186/1471-2156-11-25.
27. Gimelbrant A, Hutchinson JN, Thompson BR, Chess A. Widespread monoallelic expression on human auto-somes. Science 2007; 318:1136-40; http://dx.doi.org/10.1126/science.1148910.
28. Blagitko N, Mergenthaler S, Schulz U, Wollmann HA, Craigen W, Eggermann T, et al. Human GRB10 is imprinted and expressed from the paternal and mater-nal allele in a highly tissue- and isoform-specific fashion. Hum Mol Genet 2000; 9:1587-95; http://dx.doi.org/10.1093/hmg/9.11.1587.
29. Nakabayashi K, Trujillo AM, Tayama C, Camprubi C, Yoshida W, Lapunzina P, et al. Methylation screen-ing of reciprocal genome-wide UPDs identifies novel human-specific imprinted genes. Hum Mol Genet 2011; 20:3188-97; http://dx.doi.org/10.1093/hmg/ddr224.
30. Tanabe Y, Hirano A, Iwasato T, Itohara S, Araki K, Yamaguchi T, et al. Molecular characterization and gene disruption of a novel zinc-finger protein, HIT-4, expressed in rodent brain. J Neurochem 2010; 112:1035-44; http://dx.doi.org/10.1111/j.1471-4159.2009.06525.x.
31. Gil OD, Zanazzi G, Struyk AF, Salzer JL. Neurotrimin mediates bifunctional effects on neurite outgrowth via homophilic and heterophilic interactions. J Neurosci 1998; 18:9312-25;
32. Marshall CR, Young EJ, Pani AM, Freckmann ML, Lacassie Y, Howald C, et al. Infantile spasms is associ-ated with deletion of the MAGI2 gene on chromosome 7q11.23-q21.11. Am J Hum Genet 2008; 83:106-11; http://dx.doi.org/10.1016/j.ajhg.2008.06.001.
33. Doi K, Fujimoto T, Koyanagi M, Tsunoda T, Tanaka Y, Yoshida Y, et al. ZFAT is a critical molecule for cell survival in mouse embryonic fibroblasts. Cell Mol Biol Lett 2011; 16:89-100; http://dx.doi.org/10.2478/s11658-010-0041-1.
34. Fujimoto T, Doi K, Koyanagi M, Tsunoda T, Takashima Y, Yoshida Y, et al. ZFAT is an antiapoptotic molecule and critical for cell survival in MOLT-4 cells. FEBS Lett 2009; 583:568-72; http://dx.doi.org/10.1016/j.febslet.2008.12.063.
35. Kang HS, Kim YS, ZeRuth G, Beak JY, Gerrish K, Kilic G, et al. Transcription factor Glis3, a novel critical player in the regulation of pancreatic beta-cell devel-opment and insulin gene expression. Mol Cell Biol 2009; 29:6366-79; http://dx.doi.org/10.1128/MCB.01259-09.
36. Yang Y, Chang BH, Yechoor V, Chen W, Li L, Tsai MJ, et al. The Krüppel-like zinc finger protein GLIS3 trans-activates neurogenin 3 for proper fetal pancreatic islet differentiation in mice. Diabetologia 2011; 54:2595-605; http://dx.doi.org/10.1007/s00125-011-2255-9.
37. Cetin I, Antonazzo P. The role of the placenta in intrauterine growth restriction (IUGR). Z Geburtshilfe Neonatol 2009; 213:84-8; http://dx.doi.org/10.1055/s-0029-1224143.
38. Jansson T, Myatt L, Powell TL. The role of trophoblast nutrient and ion transporters in the development of pregnancy complications and adult disease. Curr Vasc Pharmacol 2009; 7:521-33; http://dx.doi.org/10.2174/157016109789043982.
39. King CE, Wang L, Winograd R, Madison BB, Mongroo PS, Johnstone CN, et al. LIN28B fosters colon cancer migration, invasion and transformation through let-7-dependent and -independent mechanisms. Oncogene 2011; 30:4185-93; http://dx.doi.org/10.1038/onc.2011.131.
40. Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP, Einhorn WS, et al.; DIAGRAM Consortium; MAGIC Investigators. The Lin28/let-7 axis regulates glucose metabolism. Cell 2011; 147:81-94; http://dx.doi.org/10.1016/j.cell.2011.08.033.
41. Elks CE, Ong KK. Whole genome associated studies for age at menarche. Brief Funct Genomics 2011; 10:91-7; http://dx.doi.org/10.1093/bfgp/elq030.
42. Balzer E, Heine C, Jiang Q, Lee VM, Moss EG. LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development 2010; 137:891-900; http://dx.doi.org/10.1242/dev.042895.
43. Polesskaya A, Cuvellier S, Naguibneva I, Duquet A, Moss EG, Harel-Bellan A. Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes Dev 2007; 21:1125-38; http://dx.doi.org/10.1101/gad.415007.
44. Lu L, Katsaros D, Shaverdashvili K, Qian B, Wu Y, de la Longrais IA, et al. Pluripotent factor lin-28 and its homologue lin-28b in epithelial ovarian cancer and their associations with disease outcomes and expression of let-7a and IGF-II. Eur J Cancer 2009; 45:2212-8; http://dx.doi.org/10.1016/j.ejca.2009.05.003.
45. Liang J, Wang J, Azfer A, Song W, Tromp G, Kolattukudy PE, et al. A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J Biol Chem 2008; 283:6337-46; http://dx.doi.org/10.1074/jbc.M707861200.
46. Lockwood CJ, Huang SJ, Krikun G, Caze R, Rahman M, Buchwalder LF, et al. Decidual hemostasis, inflam-mation, and angiogenesis in pre-eclampsia. Semin Thromb Hemost 2011; 37:158-64; http://dx.doi.org/10.1055/s-0030-1270344.
47. Lockwood CJ, Krikun G, Caze R, Rahman M, Buchwalder LF, Schatz F. Decidual cell-expressed tis-sue factor in human pregnancy and its involvement in hemostasis and preeclampsia-related angiogenesis. Ann N Y Acad Sci 2008; 1127:67-72; http://dx.doi.org/10.1196/annals.1434.013.
48. Kim HN, Lee EJ, Jung SC, Lee JY, Chung HW, Kim HL. Genetic variants that affect length/height in infancy/early childhood in Vietnamese-Korean fami-lies. J Hum Genet 2010; 55:681-90; http://dx.doi.org/10.1038/jhg.2010.88.
49. Takeuchi F, Nabika T, Isono M, Katsuya T, Sugiyama T, Yamaguchi S, et al. Evaluation of genetic loci influ-encing adult height in the Japanese population. J Hum Genet 2009; 54:749-52; http://dx.doi.org/10.1038/jhg.2009.99.
50. Widén E, Ripatti S, Cousminer DL, Surakka I, Lappalainen T, Järvelin MR, et al. Distinct variants at LIN28B influence growth in height from birth to adulthood. Am J Hum Genet 2010; 86:773-82; http://dx.doi.org/10.1016/j.ajhg.2010.03.010.
51. 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; 103:6623-8; http://dx.doi.org/10.1073/pnas.0511031103.
52. Blahnik KR, Dou L, Echipare L, Iyengar S, O'Geen H, Sanchez E, et al. Characterization of the contradic-tory chromatin signatures at the 3' exons of zinc finger genes. PLoS One 2011; 6:e17121; http://dx.doi.org/10.1371/journal.pone.0017121.
53. Li J, Bench AJ, Vassiliou GS, Fourouclas N, Ferguson-Smith AC, Green AR. Imprinting of the human L3MBTL gene, a polycomb family member located in a region of chromosome 20 deleted in human myeloid malignancies. Proc Natl Acad Sci U S A 2004; 101:7341-6; http://dx.doi.org/10.1073/pnas.0308195101.
54. Iida J, Ishizaki H, Okamoto-Tanaka M, Kawata A, Sumita K, Ohgake S, et al. Synaptic scaffolding mole-cule alpha is a scaffold to mediate N-methyl-D-aspartate receptor-dependent RhoA activation in dendrites. Mol Cell Biol 2007; 27:4388-405; http://dx.doi.org/10.1128/MCB.01901-06.
55. Kim J, Bergmann A, Lucas S, Stone R, Stubbs L. Lineage-specific imprinting and evolution of the zinc-finger gene ZIM2. Genomics 2004; 84:47-58; http://dx.doi.org/10.1016/j.ygeno.2004.02.007.
56. Zhang Y, Guan DG, Yang JH, Shao P, Zhou H, Qu LH. ncRNAimprint: a comprehensive database of mammalian imprinted noncoding RNAs. RNA 2010; 16:1889-901; http://dx.doi.org/10.1261/rna.2226910.
57. Koyanagi M, Nakabayashi K, Fujimoto T, Gu N, Baba I, Takashima Y, et al. ZFAT expression in B and T lym-phocytes and identification of ZFAT-regulated genes. Genomics 2008; 91:451-7; http://dx.doi.org/10.1016/j.ygeno.2008.01.009.
58. Coan PM, Burton GJ, Ferguson-Smith AC. Imprinted genes in the placenta--a review. Placenta 2005; 26(Suppl A):S10-20; http://dx.doi.org/10.1016/j.placenta.2004.12.009.
59. Pham NV, Nguyen MT, Hu JF, Vu TH, Hoffman AR. Dissociation of IGF2 and H19 imprinting in human brain. Brain Res 1998; 810:1-8; http://dx.doi.org/10.1016/S0006-8993(98)00783-5.
60. Tsunoda T, Takashima Y, Tanaka Y, Fujimoto T, Doi K, Hirose Y, et al. Immune-related zinc finger gene ZFAT is an essential transcriptional regulator for hematopoi-etic differentiation in blood islands. Proc Natl Acad Sci U S A 2010; 107:14199-204; http://dx.doi.org/10.1073/pnas.1002494107.
61. Winn VD, Haimov-Kochman R, Paquet AC, Yang YJ, Madhusudhan MS, Gormley M, et al. Gene expression profiling of the human maternal-fetal interface reveals dramatic changes between midgestation and term. Endocrinology 2007; 148:1059-79; http://dx.doi.org/10.1210/en.2006-0683.
62. Slavin TP, Feng T, Schnell A, Zhu X, Elston RC. Two-marker association tests yield new disease associations for coronary artery disease and hypertension. Hum Genet 2011; 130:725-33; http://dx.doi.org/10.1007/s00439-011-1009-6.
63. Okae H, Hiura H, Nishida Y, Funayama R, Tanaka S, Chiba H, et al. Re-investigation and RNA sequencing-based identification of genes with placenta-specific imprinted expression. Hum Mol Genet 2012; 21:548-58; http://dx.doi.org/10.1093/hmg/ddr488.
64. Proudhon C, Bourc'his D. Identification and resolu-tion of artifacts in the interpretation of imprinted gene expression. Brief Funct Genomics 2010; 9:374-84; http://dx.doi.org/10.1093/bfgp/elq020.
65. Wang X, Sun Q, McGrath SD, Mardis ER, Soloway PD, Clark AG. Transcriptome-wide identification of novel imprinted genes in neonatal mouse brain. PLoS One 2008; 3:e3839; http://dx.doi.org/10.1371/journal.pone.0003839.
66. Gascoin-Lachambre G, Buffat C, Rebourcet R, Chelbi ST, Rigourd V, Mondon F, et al. Cullins in human intra-uterine growth restriction: expressional and epigenetic alterations. Placenta 2010; 31:151-7; http://dx.doi.org/10.1016/j.placen-ta.2009.11.008.
67. Mondon F, Mignot TM, Rebourcet R, Jammes H, Danan JL, Ferré F, et al. Profiling of oxygen-modulated gene expression in early human placenta by system-atic sequencing of suppressive subtractive hybridiza-tion products. Physiol Genomics 2005; 22:99-107; http://dx.doi.org/10.1152/physiol-genomics.00276.2004.
68. Borghese B, Mondon F, Noël 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; http://dx.doi.org/10.1210/me.2008-0322.
69. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-9; http://dx.doi.org/10.1016/0003-2697(87)90021-2.
70. Meller M, Vadachkoria S, Luthy DA, Williams MA. Evaluation of housekeeping genes in placental com-parative expression studies. Placenta 2005; 26:601-7; http://dx.doi.org/10.1016/j.placen-ta.2004.09.009.
71. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:e45; http://dx.doi.org/10.1093/nar/29.9.e45.