Imprinted and X-linked non-coding RNAs as potential regulators of human placental function

Epigenetics

Volumn 9, Issue 1, 2014, Pages 81-89

  Buckberry, Sam ^a   Bianco Miotto, Tina ^a,b   Roberts, Claire T ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Epigenetics; microRNA; Non coding RNA; Placenta; Preeclampsia; Pregnancy

Indexed keywords

H19 LONG NON-CODING RNA; LONG UNTRANSLATED RNA; MICRORNA; MIRN675 MICRORNA, HUMAN; UNTRANSLATED RNA;

ANIMAL; FEMALE; GENE EXPRESSION; GENETIC EPIGENESIS; GENETICS; GENOME IMPRINTING; HUMAN; METABOLISM; PHYSIOLOGY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; X CHROMOSOME;

ANIMALS; CHROMOSOMES, HUMAN, X; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GENOMIC IMPRINTING; HUMANS; MICRORNAS; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; RNA, LONG NONCODING; RNA, UNTRANSLATED;

EID: 84891923097     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.26197     Document Type: Article

References (129)

1. Murray MJ, Lessey BA. Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis. Semin Reprod Endocrinol 1999; 17:275-90. PMID:10797946 http://dx.doi.org/10.1055/s-2007-1016235
2. Graham CH, Lala PK. Mechanisms of placental invasion of the uterus and their control. Biochem Cell Biol 1992; 70:867-74. PMID:1297352 http://dx.doi.org/10.1139/o92-135
3. Lyall F. The human placental bed revisited. Placenta 2002; 23:555-62. PMID:12361674 http://dx.doi.org/10.1053/plac.2002.0850
4. Roberts CT. IFPA Award in Placentology Lecture: Complicated interactions between genes and the environment in placentation, pregnancy outcome and long term health. Placenta 2010; 31(Suppl):S47-53. PMID:20096927 http://dx.doi.org/10.1016/j.placenta.2010.01.001
5. Khong TY, De Wolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93:1049-59. PMID:3790464 http://dx.doi.org/10.1111/j.1471-0528.1986.tb07830.x
6. Kim YM, Bujold E, Chaiworapongsa T, Gomez R, Yoon BH, Thaler HT, Rotmensch S, Romero R. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2003; 189:1063-9. PMID:14586356 http://dx.doi.org/10.1067/S0002-9378(03)00838-X
7. Kim YM, Chaiworapongsa T, Gomez R, Bujold E, Yoon BH, Rotmensch S, Thaler HT, Romero R. Failure of physiologic transformation of the spiral arteries in the placental bed in preterm premature rupture of membranes. Am J Obstet Gynecol 2002; 187:1137-42. PMID:12439491 http://dx.doi.org/10.1067/mob.2002.127720
8. Rinkenberger JL, Cross JC, Werb Z. Molecular genetics of implantation in the mouse. Dev Genet 1997; 21:6-20. PMID:9291576 urlhttp://dx.doi.org/10.1002/(SICI)1520-6408(1997)21:1 3.0.CO;2-B
9. Zhou Y, Genbacev O, Damsky CH, Fisher SJ. Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. J Reprod Immunol 1998; 39:197-213. PMID:9786462 http://dx.doi.org/10.1016/S0165-0378(98)00022-9
10. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet 2006; 15(Spec No 1):R17-29.PMID:16651366 http://dx.doi.org/10.1093/hmg/ddl046
11. Mercer TR, Dinger ME, Mattick JS. Long noncoding RNAs: insights into functions. Nat Rev Genet 2009; 10:155-9. PMID:19188922 http://dx.doi.org/10.1038/nrg2521
12. Kapranov P, St Laurent G, Raz T, Ozsolak F, Reynolds CP, Sorensen PH, Reaman G, Milos P, Arceci RJ, Thompson JF, et al. The majority of total nuclear-encoded non-ribosomal RNA in a human cell is 'dark matter' un-annotated RNA. BMC Biol 2010; 8:149. PMID:21176148 http://dx.doi.org/10.1186/1741-7007-8-149
13. Mattick JS. Challenging the dogma: the hidden layer of non-protein-coding RNAs in complex organisms. Bioessays 2003; 25:930-9. PMID:14505360 http://dx.doi.org/10.1002/bies.10332
14. Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res 2012; 40:6391-400. PMID:22492512 http://dx.doi.org/10.1093/nar/gks296
15. Frankish A, Mudge JM, Thomas M, Harrow J. The importance of identifying alternative splicing in vertebrate genome annotation. Database (Oxford) 2012; 2012:bas014. PMID:22434846 http://dx.doi.org/10.1093/database/bas014
16. Mercer TR, Gerhardt DJ, Dinger ME, Crawford J, Trapnell C, Jeddeloh JA, Mattick JS, Rinn JL. Targeted RNA sequencing reveals the deep complexity of the human transcriptome. Nat Biotechnol 2012; 30:99-104. PMID:22081020 http://dx.doi.org/10.1038/nbt.2024
17. Fowden AL, Coan PM, Angiolini E, Burton GJ, Constancia M. Imprinted genes and the epigenetic regulation of placental phenotype. Prog Biophys Mol Biol 2011; 106:281-8. PMID:21108957 http://dx.doi.org/10.1016/j.pbiomolbio.2010.11.005
18. Frost JM, Moore GE. The importance of imprinting in the human placenta. PLoS Genet 2010; 6:e1001015. PMID:20617174 http://dx.doi.org/10.1371/journal. pgen.1001015
19. Bressan FF, De Bem TH, Perecin F, Lopes FL, Ambrosio CE, Meirelles FV, Miglino MA. Unearthing the roles of imprinted genes in the placenta. Placenta 2009; 30:823-34. PMID:19679348 http://dx.doi.org/10.1016/j.placenta.2009.07.007
20. Ferguson-Smith AC, Surani MA. Imprinting and the epigenetic asymmetry between parental genomes. Science 2001; 293:1086-9. PMID:11498578 http://dx.doi.org/10.1126/science.1064020
21. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001; 2:21-32. PMID:11253064 http://dx.doi.org/10.1038/35047554
22. Koerner MV, Pauler FM, Huang R, Barlow DP. The function of non-coding RNAs in genomic imprinting. Development 2009; 136:1771-83. PMID:19429783 http://dx.doi.org/10.1242/dev.030403
23. Constância M, Pickard B, Kelsey G, Reik W. Imprinting mechanisms. Genome Res 1998; 8:881-900.PMID:9750189
24. Kacem S, Feil R. Chromatin mechanisms in genomic imprinting. Mamm Genome 2009; 20:544-56. PMID:19760321 http://dx.doi.org/10.1007/s00335-009-9223-4
25. Koerner MV, Barlow DP. Genomic imprinting-an epigenetic gene-regulatory model. Curr Opin Genet Dev 2010; 20:164-70. PMID:20153958 http://dx.doi.org/10.1016/j.gde.2010.01.009
26. Monk D, Arnaud P, Apostolidou S, Hills FA, Kelsey G, Stanier P, Feil R, Moore GE. Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci U S A 2006; 103:6623-8. PMID:16614068 http://dx.doi.org/10.1073/pnas.0511031103
27. Haig D. Altercation of generations: genetic conflicts of pregnancy. Am J Reprod Immunol 1996; 35:226-32. PMID:8962651 http://dx.doi.org/10.1111/j.1600-0897.1996.tb00035.x
28. Haig D. Genetic conflicts in human pregnancy. Q Rev Biol 1993; 68:495-532. PMID:8115596 http://dx.doi.org/10.1086/418300
29. Wagschal A, Feil R. Genomic imprinting in the placenta. Cytogenet Genome Res 2006; 113:90-8. PMID:16575167 http://dx.doi.org/10.1159/000090819
30. Buckberry S, Bianco-Miotto T, Hiendleder S, Roberts CT. Quantitative allele-specific expression and DNA methylation analysis of H19, IGF2 and IGF2R in the human placenta across gestation reveals H19 imprinting plasticity. PLoS One 2012; 7:e51210. PMID:23227253 http://dx.doi.org/10.1371/journal.pone.0051210
31. Kim J, Zhao K, Jiang P, Lu ZX, Wang J, Murray JC, Xing Y. Transcriptome landscape of the human placenta. BMC Genomics 2012; 13:115. PMID:22448651 http://dx.doi.org/10.1186/1471-2164-13-115
32. Gabory A, Ripoche MA, Yoshimizu T, Dandolo L. The H19 gene: regulation and function of a non-coding RNA. Cytogenet Genome Res 2006; 113:188-93. PMID:16575179 http://dx.doi.org/10.1159/000090831
33. Lau MM, Stewart CE, Liu Z, Bhatt H, Rotwein P, Stewart CL. Loss of the imprinted IGF2/cationindependent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 1994; 8:2953-63. PMID:8001817 http://dx.doi.org/10.1101/gad.8.24.2953
34. Constância M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, Stewart F, Kelsey G, Fowden A, Sibley C, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002; 417:945-8. PMID:12087403 http://dx.doi.org/10.1038/nature00819
35. Hirasawa R, Feil R. Genomic imprinting and human disease. Essays Biochem 2010; 48:187-200. PMID:20822494 http://dx.doi.org/10.1042/bse0480187
36. Yu L, Chen M, Zhao D, Yi P, Lu L, Han J, Zheng X, Zhou Y, Li L. The H19 gene imprinting in normal pregnancy and pre-eclampsia. Placenta 2009; 30:443-7. PMID:19342096 http://dx.doi.org/10.1016/j.placenta.2009.02.011
37. Gao WL, Li D, Xiao ZX, Liao QP, Yang HX, Li YX, Ji L, Wang YL. Detection of global DNA methylation and paternally imprinted H19 gene methylation in preeclamptic placentas. Hypertens Res 2011; 34:655-61. PMID:21326306 http://dx.doi.org/10.1038/hr.2011.9
38. Pozharny Y, Lambertini L, Ma Y, Ferrara L, Litton CG, Diplas A, Jacobs AR, Chen J, Stone JL, Wetmur J, et al. Genomic loss of imprinting in first-trimester human placenta. Am J Obstet Gynecol 2010; 202:e1-8. PMID:20350649 http://dx.doi.org/10.1016/j. ajog.2010.01.039
39. Jinno Y, Ikeda Y, Yun K, Maw M, Masuzaki H, Fukuda H, Inuzuka K, Fujishita A, Ohtani Y, Okimoto T, et al. Establishment of functional imprinting of the H19 gene in human developing placentae. Nat Genet 1995; 10:318-24. PMID:7670470 http://dx.doi.org/10.1038/ng0795-318
40. Gabory A, Jammes H, Dandolo L. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 2010; 32:473-80. PMID:20486133 http://dx.doi.org/10.1002/bies.200900170
41. Cai X, Cullen BR. The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 2007; 13:313-6. PMID:17237358 http://dx.doi.org/10.1261/rna.351707
42. Steck E, Boeuf S, Gabler J, Werth N, Schnatzer P, Diederichs S, Richter W. Regulation of H19 and its encoded microRNA-675 in osteoarthritis and under anabolic and catabolic in vitro conditions. J Mol Med (Berl) 2012; 90:1185-95. PMID:22527881 http://dx.doi.org/10.1007/s00109-012-0895-y
43. Keniry A, Oxley D, Monnier P, Kyba M, Dandolo L, Smits G, Reik W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat Cell Biol 2012; 14:659-65. PMID:22684254 http://dx.doi.org/10.1038/ncb2521
44. Sitras V, Fenton C, Paulssen R, Vårtun A, Acharya G. Differences in gene expression between first and third trimester human placenta: a microarray study. PLoS One 2012; 7:e33294. PMID:22442682 http://dx.doi.org/10.1371/journal.pone.0033294
45. Noguer-Dance M, Abu-Amero S, Al-Khtib M, Lefèvre A, Coullin P, Moore GE, Cavaillé J. The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. Hum Mol Genet 2010; 19:3566-82. PMID:20610438 http://dx.doi.org/10.1093/hmg/ddq272
46. Flor I, Neumann A, Freter C, Helmke BM, Langenbuch M, Rippe V, Bullerdiek J. Abundant expression and hemimethylation of C19MC in cell cultures from placenta-derived stromal cells. Biochem Biophys Res Commun 2012; 422:411-6. PMID:22575509 http://dx.doi.org/10.1016/j.bbrc.2012.05.004
47. Bortolin-Cavaillé ML, Dance M, Weber M, Cavaillé J. C19MC microRNAs are processed from introns of large Pol-II, non-protein-coding transcripts. Nucleic Acids Res 2009; 37:3464-73. PMID:19339516 http://dx.doi.org/10.1093/nar/gkp205
48. Saito Y, Suzuki H, Tsugawa H, Nakagawa I, Matsuzaki J, Kanai Y, Hibi T. Chromatin remodeling at Alu repeats by epigenetic treatment activates silenced microRNA-512-5p with downregulation of Mcl-1 in human gastric cancer cells. Oncogene 2009; 28:2738-44. PMID:19503096 http://dx.doi.org/10.1038/onc.2009.140
49. Tsai KW, Kao HW, Chen HC, Chen SJ, Lin WC. Epigenetic control of the expression of a primatespecific microRNA cluster in human cancer cells. Epigenetics 2009; 4:587-92. PMID:19923923 http://dx.doi.org/10.4161/epi.4.8.10230
50. Donker RB, Mouillet JF, Chu T, Hubel CA, Stolz DB, Morelli AE, Sadovsky Y. The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes. Mol Hum Reprod 2012; 18:417-24. PMID:22383544 http://dx.doi.org/10.1093/molehr/gas013
51. Enquobahrie DA, Abetew DF, Sorensen TK, Willoughby D, Chidambaram K, Williams MA. Placental microRNA expression in pregnancies complicated by preeclampsia. Am J Obstet Gynecol 2011; 204:e12-21. PMID:21093846 http://dx.doi.org/10.1016/j.ajog.2010.09.004
52. Zhu XM, Han T, Sargent IL, Yin GW, Yao YQ. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol 2009; 200:e1-7. PMID:19285651 http://dx.doi.org/10.1016/j.ajog.2008.12.045
53. Ishibashi O, Ohkuchi A, Ali MM, Kurashina R, Luo SS, Ishikawa T, Takizawa T, Hirashima C, Takahashi K, Migita M, et al. Hydroxysteroid (17-β) dehydrogenase 1 is dysregulated by miR- 210 and miR-518c that are aberrantly expressed in preeclamptic placentas: a novel marker for predicting preeclampsia. Hypertension 2012; 59:265-73. PMID:22203747 http://dx.doi.org/10.1161/HYPERTENSIONAHA.111.180232
54. Hu Y, Li P, Hao S, Liu L, Zhao J, Hou Y. Differential expression of microRNAs in the placentae of Chinese patients with severe pre-eclampsia. Clin Chem Lab Med 2009; 47:923-9. PMID:19642860 http://dx.doi.org/10.1515/CCLM.2009.228
55. Ye W, Lv Q, Wong CK, Hu S, Fu C, Hua Z, Cai G, Li G, Yang BB, Zhang Y. The effect of central loops in miRNA:MRE duplexes on the efficiency of miRNAmediated gene regulation. PLoS One 2008; 3:e1719. PMID:18320040 http://dx.doi.org/10.1371/journal.pone.0001719
56. Enquobahrie DA, Meller M, Rice K, Psaty BM, Siscovick DS, Williams MA. Differential placental gene expression in preeclampsia. Am J Obstet Gynecol 2008; 199:566.e1-11
57. McCarthy C, Cotter FE, McElwaine S, Twomey A, Mooney EE, Ryan F, Vaughan J. Altered gene expression patterns in intrauterine growth restriction: potential role of hypoxia. Am J Obstet Gynecol 2007; 196:e1-6. PMID:17240240 http://dx.doi.org/10.1016/j.ajog.2006.08.027
58. Nishizawa H, Pryor-Koishi K, Kato T, Kowa H, Kurahashi H, Udagawa Y. Microarray analysis of differentially expressed fetal genes in placental tissue derived from early and late onset severe pre-eclampsia. Placenta 2007; 28:487-97. PMID:16860862 http://dx.doi.org/10.1016/j.placenta.2006.05.010
59. Winn VD, Gormley M, Paquet AC, Kjaer-Sorensen K, Kramer A, Rumer KK, Haimov-Kochman R, Yeh RF, Overgaard MT, Varki A, et al. Severe preeclampsia-related changes in gene expression at the maternal-fetal interface include sialic acid-binding immunoglobulin-like lectin-6 and pappalysin-2. Endocrinology 2009; 150:452-62. PMID:18818296 http://dx.doi.org/10.1210/en.2008-0990
60. Jarvenpaa J, Vuoristo JT, Savolainen ER, Ukkola O, Vaskivuo T, Ryynanen M. Altered expression of angiogenesis-related placental genes in pre-eclampsia associated with intrauterine growth restriction. Gynecol Endocrinol 2007; 23:351-5. PMID:17616861 http://dx.doi.org/10.1080/09513590701350291
61. Sitras V, Paulssen RH, Grønaas H, Leirvik J, Hanssen TA, Vårtun A, Acharya G. Differential placental gene expression in severe preeclampsia. Placenta 2009; 30:424-33. PMID:19249095 http://dx.doi.org/10.1016/j.placenta.2009.01.012
62. Meng T, Chen H, Sun M, Wang H, Zhao G, Wang X. Identification of differential gene expression profiles in placentas from preeclamptic pregnancies versus normal pregnancies by DNA microarrays. OMICS 2012; 16:301-11. PMID:22702245 http://dx.doi.org/10.1089/omi.2011.0066
63. Levy R. The role of apoptosis in preeclampsia. Isr Med Assoc J 2005; 7:178-81. PMID:15792265
64. Novakovic B, Saffery R. The ever growing complexity of placental epigenetics - role in adverse pregnancy outcomes and fetal programming. Placenta 2012; 33:959-70. PMID:23102655 http://dx.doi.org/10.1016/j.placenta.2012.10.003
65. Mayor-Lynn K, Toloubeydokhti T, Cruz AC, Chegini N. Expression profile of microRNAs and mRNAs in human placentas from pregnancies complicated by preeclampsia and preterm labor. Reprod Sci 2011; 18:46-56. PMID:21079238 http://dx.doi.org/10.1177/1933719110374115
66. Crawford MA, Doyle W, Meadows N. Gender differences at birth and differences in fetal growth. Hum Reprod 1987; 2:517-20. PMID:3667908
67. Bertino E, Coscia A, Boni L, Rossi C, Martano C, Giuliani F, Fabris C, Spada E, Zolin A, Milani S. Weight growth velocity of very low birth weight infants: role of gender, gestational age and major morbidities. Early Hum Dev 2009; 85:339-47. PMID:19189877 http://dx.doi.org/10.1016/j.earlhumdev.2008.12.014
68. de Onis M, Siyam A, Borghi E, Onyango AW, Piwoz E, Garza C. Comparison of the World Health Organization growth velocity standards with existing US reference data. Pediatrics 2011; 128:e18-26.PMID:21708799 http://dx.doi.org/10.1542/peds.2010-2630
69. Brettell R, Yeh PS, Impey LW. Examination of the association between male gender and preterm delivery. Eur J Obstet Gynecol Reprod Biol 2008; 141:123-6. PMID:18783867 http://dx.doi.org/10.1016/j.ejogrb.2008.07.030
70. Ingemarsson I. Gender aspects of preterm birth. BJOG 2003; 110(Suppl 20):34-8. PMID:12763109
71. Elsmén E, Källén K, Marsál K, Hellström-Westas L. Fetal gender and gestational-age-related incidence of pre-eclampsia. Acta Obstet Gynecol Scand 2006; 85:1285-91. PMID:17091404 http://dx.doi.org/10.1080/00016340600578274
72. Murji A, Proctor LK, Paterson AD, Chitayat D, Weksberg R, Kingdom J. Male sex bias in placental dysfunction. Am J Med Genet A 2012; 158A:779-83. PMID:22407866 http://dx.doi.org/10.1002/ajmg.a.35250
73. Vatten LJ, Skjaerven R. Offspring sex and pregnancy outcome by length of gestation. Early Hum Dev 2004; 76:47-54. PMID:14729162 http://dx.doi.org/10.1016/j.earlhumdev.2003.10.006
74. Clifton VL. Review: Sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 2010; 31(Suppl):S33-9. PMID:20004469 http://dx.doi.org/10.1016/j.placenta.2009.11.010
75. Hodyl NA, Wyper H, Osei-Kumah A, Scott N, Murphy VE, Gibson P, Smith R, Clifton VL. Sexspecific associations between cortisol and birth weight in pregnancies complicated by asthma are not due to differential glucocorticoid receptor expression. Thorax 2010; 65:677-83. PMID:20627904 http://dx.doi.org/10.1136/thx.2009.123091
76. Di Renzo GC, Rosati A, Sarti RD, Cruciani L, Cutuli AM. Does fetal sex affect pregnancy outcome? Gend Med 2007; 4:19-30. PMID:17584623 http://dx.doi.org/10.1016/S1550-8579(07)80004-0
77. Edwards A, Megens A, Peek M, Wallace EM. Sexual origins of placental dysfunction. Lancet 2000; 355:203-4. PMID:10675126 http://dx.doi.org/10.1016/S0140-6736(99)05061-8
78. Ghidini A, Salafia CM. Gender differences of placental dysfunction in severe prematurity. BJOG 2005; 112:140-4. PMID:15663576 http://dx.doi.org/10.1111/j.1471-0528.2004.00308.x
79. Wijchers PJ, Festenstein RJ. Epigenetic regulation of autosomal gene expression by sex chromosomes. Trends Genet 2011; 27:132-40. PMID:21334089 http://dx.doi.org/10.1016/j.tig.2011.01.004
80. Carrel L, Willard HF. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005; 434:400-4. PMID:15772666 http://dx.doi.org/10.1038/nature03479
81. Ober C, Loisel DA, Gilad Y. Sex-specific genetic architecture of human disease. Nat Rev Genet 2008; 9:911-22. PMID:19002143 http://dx.doi.org/10.1038/nrg2415
82. Graves JA. Review: Sex chromosome evolution and the expression of sex-specific genes in the placenta. Placenta 2010; 31(Suppl):S27-32. PMID:20163856 http://dx.doi.org/10.1016/j.placenta.2009.12.029
83. Arnold AP, Lusis AJ. Understanding the sexome: measuring and reporting sex differences in gene systems. Endocrinology 2012; 153:2551-5. PMID:22434084 http://dx.doi.org/10.1210/en.2011-2134
84. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39(Database issue):D152-7. PMID:21037258 http://dx.doi.org/10.1093/nar/gkq1027
85. Pinheiro I, Dejager L, Libert C. X-chromosomelocated microRNAs in immunity: might they explain male/female differences? The X chromosomegenomic context may affect X-located miRNAs and downstream signaling, thereby contributing to the enhanced immune response of females. Bioessays 2011; 33:791-802. PMID:21953569 http://dx.doi.org/10.1002/bies.201100047
86. Ropers HH, Wolff G, Hitzeroth HW. Preferential X inactivation in human placenta membranes: is the paternal X inactive in early embryonic development of female mammals? Hum Genet 1978; 43:265-73. PMID:700701 http://dx.doi.org/10.1007/BF00278833
87. Migeon BR, Do TT. In search of non-random X inactivation: studies of fetal membranes heterozygous for glucose-6-phosphate dehydrogenase. Am J Hum Genet 1979; 31:581-5. PMID:507052
88. Harrison KB, Warburton D. Preferential X-chromosome activity in human female placental tissues. Cytogenet Cell Genet 1986; 41:163-8. PMID:3956266 http://dx.doi.org/10.1159/000132221
89. Harrison KB. X-chromosome inactivation in the human cytotrophoblast. Cytogenet Cell Genet 1989; 52:37-41. PMID:2612213 http://dx.doi.org/10.1159/000132835
90. Mohandas TK, Passage MB, Williams JW 3rd, Sparkes RS, Yen PH, Shapiro LJ. X-chromosome inactivation in cultured cells from human chorionic villi. Somat Cell Mol Genet 1989; 15:131-6. PMID:2928838 http://dx.doi.org/10.1007/BF01535073
91. Goto T, Wright E, Monk M. Paternal X-chromosome inactivation in human trophoblastic cells. Mol Hum Reprod 1997; 3:77-80. PMID:9239711 http://dx.doi.org/10.1093/molehr/3.1.77
92. Looijenga LH, Gillis AJ, Verkerk AJ, van Putten WL, Oosterhuis JW. Heterogeneous X inactivation in trophoblastic cells of human full-term female placentas. Am J Hum Genet 1999; 64:1445-52. PMID:10205278 http://dx.doi.org/10.1086/302382
93. Zeng SM, Yankowitz J. X-inactivation patterns in human embryonic and extra-embryonic tissues. Placenta 2003; 24:270-5. PMID:12566254 http://dx.doi.org/10.1053/plac.2002.0889
94. Willemsen R, Bontekoe CJ, Severijnen LA, Oostra BA. Timing of the absence of FMR1 expression in full mutation chorionic villi. Hum Genet 2002; 110:601-5. PMID:12107447 http://dx.doi.org/10.1007/s00439-002-0723-5
95. Dhara SK, Benvenisty N. Gene trap as a tool for genome annotation and analysis of X chromosome inactivation in human embryonic stem cells. Nucleic Acids Res 2004; 32:3995-4002. PMID:15284332 http://dx.doi.org/10.1093/nar/gkh746
96. Uehara S, Tamura M, Nata M, Ji G, Yaegashi N, Okamura K, Yajima A. X-chromosome inactivation in the human trophoblast of early pregnancy. J Hum Genet 2000; 45:119-26. PMID:10807535 http://dx.doi.org/10.1007/s100380050197
97. Lee JT. Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat Rev Mol Cell Biol 2011; 12:815-26. PMID:22108600 http://dx.doi.org/10.1038/nrm3231
98. Moreira de Mello JC, de Araújo ES, Stabellini R, Fraga AM, de Souza JE, Sumita DR, Camargo AA, Pereira LV. Random X inactivation and extensive mosaicism in human placenta revealed by analysis of allelespecific gene expression along the X chromosome. PLoS One 2010; 5:e10947. PMID:20532033 http://dx.doi.org/10.1371/journal.pone.0010947
99. Ge B, Gurd S, Gaudin T, Dore C, Lepage P, Harmsen E, Hudson TJ, Pastinen T. Survey of allelic expression using EST mining. Genome Res 2005; 15:1584-91.PMID:16251468 http://dx.doi.org/10.1101/gr.4023805
100. Wang H, Elbein SC. Detection of allelic imbalance in gene expression using pyrosequencing. Methods Mol Biol 2007; 373:157-76. PMID:17185765
101. Knight JC. Allele-specific gene expression uncovered. Trends Genet 2004; 20:113-6. PMID:15049300 http://dx.doi.org/10.1016/j.tig.2004.01.001
102. Wang W, Feng L, Zhang H, Hachy S, Satohisa S, Laurent LC, Parast M, Zheng J, Chen DB. Preeclampsia up-regulates angiogenesis-associated microRNA (i.e., miR-17, -20a, and -20b) that target ephrin-B2 and EPHB4 in human placenta. J Clin Endocrinol Metab 2012; 97:E1051-9. PMID:22438230 http://dx.doi.org/10.1210/jc.2011-3131
103. PengFei L. YaLi H, Sha H, Liu L, JunLi Z, YaYi H. The expression of microRNA in placenca from severe preeclampsia patients. Chinese Journal of Practical Gynecology and Obstetrics 2009; 25:911-4
104. Andraweera PH, Dekker GA, Roberts CT. The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum Reprod Update 2012; 18:436-57. PMID:22495259 http://dx.doi.org/10.1093/humupd/dms011
105. Borzychowski AM, Sargent IL, Redman CW. Inflammation and pre-eclampsia. Semin Fetal Neonatal Med 2006; 11:309-16. PMID:16828580 http://dx.doi.org/10.1016/j.siny.2006.04.001
106. Ghosh G, Subramanian IV, Adhikari N, Zhang X, Joshi HP, Basi D, Chandrashekhar YS, Hall JL, Roy S, Zeng Y, et al. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-α isoforms and promotes angiogenesis. J Clin Invest 2010; 120:4141-54. PMID:20972335 http://dx.doi.org/10.1172/JCI42980
107. Cook KB, Kazan H, Zuberi K, Morris Q, Hughes TR. RBPDB: a database of RNA-binding specificities. Nucleic Acids Res 2011; 39(Database issue):D301-8. PMID:21036867 http://dx.doi.org/10.1093/nar/gkq1069
108. Lázár L, Nagy B, Molvarec A, Szarka A, Rigó J Jr. Role of hsa-miR-325 in the etiopathology of preeclampsia. Mol Med Rep 2012; 6:597-600. PMID:22710575
109. Papadopoulos GL, Reczko M, Simossis VA, Sethupathy P, Hatzigeorgiou AG. The database of experimentally supported targets: a functional update of TarBase. Nucleic Acids Res 2009; 37(Database issue):D155-8. PMID:18957447 http://dx.doi.org/10.1093/nar/gkn809
110. Hsu SD, Lin FM, Wu WY, Liang C, Huang WC, Chan WL, Tsai WT, Chen GZ, Lee CJ, Chiu CM, et al. miRTarBase: a database curates experimentally validated microRNA-target interactions. Nucleic Acids Res 2011; 39(Database issue):D163-9. PMID:21071411 http://dx.doi.org/10.1093/nar/gkq1107
111. Glienke J, Sturz A, Menrad A, Thierauch KH. CRIM1 is involved in endothelial cell capillary formation in vitro and is expressed in blood vessels in vivo. Mech Dev 2002; 119:165-75. PMID:12464430 http://dx.doi.org/10.1016/S09254773(02)00355-6
112. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003; 9:677-84. PMID:12778166 http://dx.doi.org/10.1038/nm0603-677
113. Pringle KG, Kind KL, Sferruzzi-Perri AN, Thompson JG, Roberts CT. Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy. Hum Reprod Update 2010; 16:415-31. PMID:19926662 http://dx.doi.org/10.1093/humupd/dmp046
114. Cazzalini O, Scovassi AI, Savio M, Stivala LA, Prosperi E. Multiple roles of the cell cycle inhibitor p21(CDKN1A) in the DNA damage response. Mutat Res 2010; 704:12-20. PMID:20096807 http://dx.doi.org/10.1016/j.mrrev.2010.01.009
115. Curtin JF, Cotter TG. Live and let die: regulatory mechanisms in Fas-mediated apoptosis. Cell Signal 2003; 15:983-92. PMID:14499341 http://dx.doi.org/10.1016/S0898-6568(03)00093-7
116. Poehlmann TG, Fitzgerald JS, Meissner A, Wengenmayer T, Schleussner E, Friedrich K, Markert UR. Trophoblast invasion: tuning through LIF, signalling via Stat3. Placenta 2005; 26(Suppl A):S37-41. PMID:15837065 http://dx.doi.org/10.1016/j.placenta.2005.01.007
117. Thomadaki H, Scorilas A. BCL2 family of apoptosis-related genes: functions and clinical implications in cancer. Crit Rev Clin Lab Sci 2006; 43:1-67. PMID:16531274 http://dx.doi.org/10.1080/10408360500295626
118. Chan KT, Creed SJ, Bear JE. Unraveling the enigma: progress towards understanding the coronin family of actin regulators. Trends Cell Biol 2011; 21:481-8.PMID:21632254 http://dx.doi.org/10.1016/j.tcb.2011.04.004
119. Preston GA, Lyon TT, Yin Y, Lang JE, Solomon G, Annab L, Srinivasan DG, Alcorta DA, Barrett JC. Induction of apoptosis by c-Fos protein. Mol Cell Biol 1996; 16:211-8. PMID:8524298
120. Urbich C, Knau A, Fichtlscherer S, Walter DH, Brühl T, Potente M, Hofmann WK, de Vos S, Zeiher AM, Dimmeler S. FOXO-dependent expression of the proapoptotic protein Bim: pivotal role for apoptosis signaling in endothelial progenitor cells. FASEB J 2005; 19:974-6. PMID:15824087
121. Gonzalvez F, Ashkenazi A. New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 2010; 29:4752-65. PMID:20531300 http://dx.doi.org/10.1038/onc.2010.221
122. Halperin R, Peller S, Sandbank J, Bukovsky I, Schneider D. Expression of the p53 gene and apoptosis in gestational trophoblastic disease. Placenta 2000; 21:58-62. PMID:10692252 http://dx.doi.org/10.1053/plac.1999.0442
123. Dye JF, Jablenska R, Donnelly JL, Lawrence L, Leach L, Clark P, Firth JA. Phenotype of the endothelium in the human term placenta. Placenta 2001; 22:32-43. PMID:11162350 http://dx.doi.org/10.1053/plac.2000.0579
124. Ullah Z, Kohn MJ, Yagi R, Vassilev LT, DePamphilis ML. Differentiation of trophoblast stem cells into giant cells is triggered by p57/Kip2 inhibition of CDK1 activity. Genes Dev 2008; 22:3024-36. PMID:18981479 http://dx.doi.org/10.1101/gad.1718108
125. Prendergast GC. Actin' up: RhoB in cancer and apoptosis. Nat Rev Cancer 2001; 1:162-8. PMID:11905808 http://dx.doi.org/10.1038/35101096
126. Akira S, Hirano T, Taga T, Kishimoto T. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J 1990; 4:2860-7. PMID:2199284
127. Yoshitomi T, Kawakami K, Enokida H, Chiyomaru T, Kagara I, Tatarano S, Yoshino H, Arimura H, Nishiyama K, Seki N, et al. Restoration of miR-517a expression induces cell apoptosis in bladder cancer cell lines. Oncol Rep 2011; 25:1661-8. PMID:21479368
128. Montenegro D, Romero R, Kim SS, Tarca AL, Draghici S, Kusanovic JP, Kim JS, Lee DC, Erez O, Gotsch F, et al. Expression patterns of microRNAs in the chorioamniotic membranes: a role for microRNAs in human pregnancy and parturition. J Pathol 2009; 217:113-21. PMID:18991333 http://dx.doi.org/10.1002/path.2463
129. Kolwankar D, Glover DD, Ware JA, Tracy TS. Expression and function of ABCB1 and ABCG2 in human placental tissue. Drug Metab Dispos 2005; 33:524-9. PMID:15640379 http://dx.doi.org/10.1124/dmd.104.002261