Widespread DNA hypomethylation at gene enhancer regions in placentas associated with early-onset pre-eclampsia

Molecular Human Reproduction

Volumn 19, Issue 10, 2013, Pages 697-708

  Blair, John D ^a,b   Yuen, Ryan K C ^a,c   Lim, Brendan K ^b   McFadden, Deborah E ^a   von Dadelszen, Peter ^a,b   Robinson, Wendy P ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

450 K array; DNA methylation; Placenta; Pre eclampsia

Indexed keywords

TRANSCRIPTION FACTOR;

ADULT; ANGIOGENESIS; ARTICLE; CASE CONTROL STUDY; CELL POPULATION; CHORION VILLUS; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; CPG ISLAND; DISEASE ASSOCIATION; DNA METHYLATION; EARLY ONSET PREECLAMPSIA; ENHANCER REGION; FEMALE; FOLLOW UP; GENE; GENE EXPRESSION; GESTATIONAL AGE; HUMAN; HUMAN CELL; PLACENTA; PLACENTA FUNCTION; PREECLAMPSIA; PREMATURE LABOR; PRENATAL DIAGNOSIS; PRENATAL GROWTH; PRIORITY JOURNAL; PYROSEQUENCING; SCREENING;

450 K ARRAY; DNA METHYLATION; PLACENTA; PRE-ECLAMPSIA;

ADAM PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CPG ISLANDS; DNA METHYLATION; FEMALE; GLUCOSE TRANSPORTER TYPE 1; HOMEODOMAIN PROTEINS; HUMANS; INHIBIN-BETA SUBUNITS; MEMBRANE PROTEINS; PLACENTA; PRE-ECLAMPSIA; PREGNANCY;

EID: 84884935122     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat044     Document Type: Article

References (62)

1. Alsat E, Wyplosz P, Malassine A, Guibourdenche J, Porquet D, Nessmann C, Evain-Brion D. Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro. J Cell Physiol 1996;168:346-353.
2. Bahado-Singh RO, Akolekar R, Mandal R, Dong E, Xia J, Kruger M, Wishart DS, Nicolaides K. First-trimester metabolomic detection of late-onset preeclampsia. Am J Obstet Gynecol 2012;25:1840-1847.
3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, LiWW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009;37:W202-W208.
4. Baumann MU, Zamudio S, Illsley NP. Hypoxic upregulation of glucose transporters in BeWo choriocarcinoma cells is mediated by hypoxia-inducible factor-1.AmJ Physiol Cell Physiol 2007;293:C477-C485.
5. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, Delano D, Zhang L, Schroth GP, Gunderson KL et al. High density DNA methylation array with single CpG site resolution. Genomics 2011;98:288-295.
6. Chakrabarti J, TurleyH, Campo L, Han C, Harris AL, Gatter KC, Fox SB. The transcription factorDEC1(stra13, SHARP2) is associated with the hypoxic response and high tumour grade in human breast cancers. Br J Cancer 2004; 91:954-958.
7. Chen Y, Huang Y, Jiang R, Teng Y. Syncytiotrophoblast-derived microparticle shedding in early-onset and late-onset severe pre-eclampsia. Int J Gynaecol Obstet 2012;119:234-238.
8. Cote AM, Firoz T, Mattman A, Lam EM, von Dadelszen P, Magee LA. The 24-hour urine collection: gold standard or historical practice? Am J Obstet Gynecol 2008;199:625.e1-625.e6.
9. Cox B, Sharma P, Evangelou AI, Whiteley K, Ignatchenko V, Ignatchenko A, Baczyk D, Czikk M, Kingdom J, Rossant J et al.. Translational analysis of mouse and human placental protein and mRNA reveals distinct molecular pathologies in human preeclampsia. Mol Cell Proteomics 2011; 10:M111.012526.
10. Cross JC. The genetics of pre-eclampsia: a feto-placental or maternal problem? Clin Genet 2003;64:96-103.
11. Davis S,Du P, Bilke S. methylumi: Handle Illumina Methylation Data. R package version 2.0.13 2011. http://www.bioconductor.org/.
12. DuP, Zhang X, HuangCC, JafariN, KibbeWA,HouL, Lin SM. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 2010;11:587.
13. 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.e1-566.e11.
14. Escudero C, Bertoglia P, Hernadez M, Celis C, Gonzalez M, Aguayo C, Acurio J. Impaired A(2A) adenosine receptor/nitric oxide/VEGF signaling pathway in fetal endothelium during late- and early-onset preeclampsia. Purinergic Signal 2013;9:215-226.
15. Ezashi T, Telugu BP, Roberts RM. Model systems for studying trophoblast differentiation from human pluripotent stem cells. Cell Tissue Res 2012; 349:809-824.
16. Gauster M, Moser G, Orendi K, Huppertz B. Factors involved in regulating trophoblast fusion: potential role in the development of preeclampsia. Placenta 2009;30(Suppl A):S49-S54.
17. Ghulmiyyah L, Sibai B. Maternal mortality from preeclampsia/eclampsia. Semin Perinatol 2012;36:56-59.
18. Hoegh AM, Borup R, Nielsen FC, Sorensen S, Hviid TV. Gene expression profiling of placentas affected by pre-eclampsia. J Biomed Biotechnol 2010;2010:787545.
19. Hogg K, Blair JD, McFadden DE, von Dadelszen P, RobinsonWP. Early onset pre-eclampsia is associated with altered DNA methylation of cortisol-signalling and steroidogenic genes in the placenta. PloS One 2013a;8:e62969.
20. Hogg K, Blair JD, von Dadelszen P, Robinson WP. Hypomethylation of the LEP gene in placenta and elevated maternal leptin concentration in early onset pre-eclampsia. Mol Cell Endocrinol 2013b;367:64-73.
21. Horiuchi A, Hayashi T, Kikuchi N, Hayashi A, FuseyaC, Shiozawa T, Konishi I. Hypoxia upregulates ovarian cancer invasiveness via the binding of HIF-1alpha to a hypoxia-induced, methylation-free hypoxia response element of S100A4 gene. Int J Cancer 2012;131:1755-1767.
22. Huang daW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57.
23. Hung TH, Skepper JN, Charnock-Jones DS, Burton GJ. Hypoxiareoxygenation: a potent inducer of apoptotic changes in the human placenta and possible etiological factor in preeclampsia. Circ Res 2002; 90:1274-1281.
24. Huppertz B. Placental pathology in pregnancy complications. Thromb Res 2011;127(Suppl 3):S96-S99.
25. Irizarry RA, Ladd-Acosta C,Wen B,Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 2009;41:178-186.
26. 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;23:351-355.
27. Jia RZ, Zhang X, Hu P, Liu XM, Hua XD, Wang X, Ding HJ. Screening for differential methylation status in human placenta in preeclampsia using a CpG island plus promoter microarray. Int J Mol Med 2012; 30:133-141.
28. Kleinrouweler CE, Wiegerinck MM, Ris-Stalpers C, Bossuyt PM, van der Post JA, von Dadelszen P, Mol BW, Pajkrt E. EBM CONNECT Collaboration. Accuracy of circulating placental growth factor, vascular endothelial growth factor, soluble fms-like tyrosine kinase 1 and soluble endoglin in the prediction of pre-eclampsia: a systematic review and meta-analysis. BJOG 2012;119:778-787.
29. Kuc S, Wortelboer EJ, van Rijn BB, Franx A, Visser GH, Schielen PC. Evaluation of 7 serum biomarkers and uterine artery Doppler ultrasound for first-trimester prediction of preeclampsia: a systematic review. Obstet Gynecol Surv 2011;66:225-239.
30. Louwen F, Muschol-Steinmetz C, Reinhard J, Reitter A, Yuan J. A lesson for cancer research: placental microarray gene analysis in preeclampsia. Oncotarget 2012;3:759-773.
31. Magee LA,Helewa M,Moutquin JM, vonDadelszen P.HypertensionGuideline Committee and Strategic Training Initiative in Research in the Reproductive Health Sciences (STIRRHS) Scholars. Diagnosis, evaluation, and management of the hypertensive disorders of pregnancy. J Obstet Gynaecol Can 2008;30:S1-48.
32. Maksimovic J, Gordon L, Oshlack A. SWAN: Subset-quantile Within Array Normalization for Illumina Infinium HumanMethylation450 BeadChips. Genome Biol 2012;13:R44.
33. Masoura S, Kalogiannidis IA, Gitas G, Goutsioulis A, Koiou E, Athanasiadis A, Vavatsi N. Biomarkers in pre-eclampsia: a novel approach to early detection of the disease. J Obstet Gynaecol 2012;32:609-616.
34. Meinhardt G, Husslein P, Knofler M. Tissue-specific and ubiquitous basic helix-loop-helix transcription factors in human placental trophoblasts. Placenta 2005;26:527-539.
35. Mousa AA, Archer KJ, Cappello R, Estrada-Gutierrez G, Isaacs CR, Strauss JF 3rd,Walsh SW. DNA methylation is altered in maternal blood vessels of women with preeclampsia. Reprod Sci 2012;19:1332-1342.
36. 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;28:487-497.
37. Nishizawa H, Ota S, Suzuki M, Kato T, Sekiya T, Kurahashi H, Udagawa Y. Comparative gene expression profiling of placentas from patients with severe pre-eclampsia and unexplained fetal growth restriction. Reprod Biol Endocrinol 2011;9:107.
38. Novakovic B, Yuen RK, Gordon L, Penaherrera MS, Sharkey A, Moffett A, Craig JM, Robinson WP, Saffery R. Evidence for widespread changes in promoter methylation profile in human placenta in response to increasing gestational age and environmental/stochastic factors. BMC Genomics 2011;12:529.
39. Ogoshi K, Hashimoto S, Nakatani Y, Qu W, Oshima K, Tokunaga K, Sugano S, Hattori M, Morishita S, Matsushima K. Genome-wide profiling of DNA methylation in human cancer cells. Genomics 2011;98:280-287.
40. Price EM, Cotton AM, Lam LL, Farre P, Emberly E, Brown CJ, RobinsonWP, Kobor MS. Additional annotation enhances potential for biologicallyrelevant analysis of the Illumina Infinium HumanMethylation450 Bead Chip array. Epigenetics Chromatin 2013;6:4.
41. R Development Core Team. R: A Language and Environment for Statistical Computing 2011. http://www.bioconductor.org/.
42. Rajakumar A, Whitelock KA, Weissfeld LA, Daftary AR, Markovic N, Conrad KP. Selective overexpression of the hypoxia-inducible transcription factor, HIF-2alpha, in placentas from women with preeclampsia. Biol Reprod 2001;64:499-506.
43. Redline RW, Patterson P. Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Hum Pathol 1995; 26:594-600.
44. RedmanCW, Sargent IL. Immunology of pre-eclampsia. AmJ Reprod Immunol 2010;63:534-543.
45. Rolfo A, Many A, Racano A, Tal R, Tagliaferro A, Ietta F, Wang J, Post M, Caniggia I. Abnormalities in oxygen sensing define early and late onset preeclampsia as distinct pathologies. PLoS One 2010;5:e13288.
46. Sanyal A, Lajoie BR, Jain G, Dekker J. The long-range interaction landscape of gene promoters. Nature 2012;489:109-113.
47. Schodel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 2011;117:e207-e217.
48. Schwender H. Siggenes: Multiple Testing using SAM and Efron's Empirical Bayes Approaches. R package version 1.28.0. 2011. http://www.bioconductor.org/.
49. Shahrzad S, Bertrand K, Minhas K, Coomber BL. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2007;2:119-125.
50. Sitras V, Paulssen RH, Gronaas H, Leirvik J, Hanssen TA, Vartun A, Acharya G. Differential placental gene expression in severe preeclampsia. Placenta 2009;30:424-433.
51. Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg R. Pre-eclampsia. Lancet 2010;376:631-644.
52. Tal R. The Role of Hypoxia and Hypoxia-Inducible Factor 1 Alpha in Preeclampsia Pathogenesis. Biol Reprod 2012;87:134.
53. Tsai S, Hardison NE, James AH, Motsinger-Reif AA, Bischoff SR, Thames BH, Piedrahita JA. Transcriptional profiling of human placentas from pregnancies complicated by preeclampsia reveals disregulation of sialic acid acetylesterase and immune signalling pathways. Placenta 2011; 32:175-182.
54. Varkonyi T, Nagy B, Fule T, Tarca AL, Karaszi K, Schonleber J, Hupuczi P, Mihalik N, Kovalszky I, Rigo J Jr et al. Microarray profiling reveals that placental transcriptomes of early-onset HELLP syndrome and preeclampsia are similar. Placenta 2011;32(Suppl):S21-S29.
55. von Dadelszen P, Magee LA, Roberts JM. Subclassification of preeclampsia. Hypertens Pregnancy 2003;22:143-148.
56. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, Schubeler D. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007; 39:457-466.
57. Xiang Y, Zhang X, Li Q, Xu J, Zhou X,Wang T, Xing Q, Liu Y,Wang L, He L et al. Promoter hypomethylation of TIMP3 is associated with pre-eclampsia in a Chinese population. Mol Hum Reprod 2012; 19:153-159.
58. Yuen RK, Avila L, Penaherrera MS, von Dadelszen P, Lefebvre L, Kobor MS, Robinson WP. Human placental-specific epipolymorphism and its association with adverse pregnancy outcomes. PLoS One 2009;4: e7389.
59. Yuen RK, Penaherrera MS, von Dadelszen P, McFadden DE, Robinson WP. DNA methylation profiling of human placentas reveals promoter hypomethylation of multiple genes in early-onset preeclampsia. Eur J Hum Genet 2010;18:1006-1012.
60. Yuen RK, Manokhina I, Robinson WP. Are we ready for DNA methylation-based prenatal testing? Epigenomics 2011;3:387-390.
61. Yuen RK, Chen B, Blair JD, Robinson WP, Nelson DM. Hypoxia alters the epigenetic profile in cultured human placental trophoblasts. Epigenetics 2013;8:192-202.
62. Zeybek YG, Gunel T, Benian A, Aydinli K, Kaleli S. Clinical evaluations of cell-free fetal DNA quantities in pre-eclamptic pregnancies. J Obstet Gynaecol Res 2012;39:632-640.