Recent progress towards understanding the role of DNA methylation in human placental development

Reproduction

Volumn 152, Issue 1, 2016, Pages R23-R30

  Bianco Miotto, Tina ^a,b   Mayne, Benjamin T ^a,b   Buckberry, Sam ^c   Breen, James ^a,b   Rodriguez Lopez, Carlos M ^a   Roberts, Claire T ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; HUMAN; PLACENTA; PLACENTA DEVELOPMENT; PLACENTA TISSUE; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; CYTOLOGY; FEMALE; GENETIC EPIGENESIS; METABOLISM;

BIOLOGICAL MARKER;

BIOMARKERS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HUMANS; PLACENTA; PREGNANCY;

EID: 84976883193     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-16-0014     Document Type: Review

References (63)

1. Andraweera PH, Dekker GA, Laurence JA & Roberts CT 2012 Placental expression of VEGF family mRNA in adverse pregnancy outcomes. Placenta 33 467-472. (doi:10.1016/j.placenta.2012.02.013)
2. Anton L, Brown AG, Bartolomei MS & Elovitz MA 2014 Differential methylation of genes associated with cell adhesion in preeclamptic placentas. PLoS ONE 9 e100148. (doi:10.1371/journal.pone.0100148)
3. Aryee MJ, Jaffe AE, Corrada-Bravo H, Ladd-Acosta C, Feinberg AP, Hansen KD & Irizarry RA 2014 Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics 30 1363-1369. (doi:10.1093/bioinformatics/btu049)
4. Banister CE, Koestler DC, Maccani MA, Padbury JF, Houseman EA & Marsit CJ 2011 Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas. Epigenetics 6 920-927. (doi:10.4161/epi.6.7.16079)
5. Becket E, Chopra S, Duymich CE, Lin JJ, You JS, Pandiyan K, Nichols PW, Siegmund KD, Charlet J, Weisenberger DJ et al. 2016 Identification of DNA methylation-independent epigenetic events underlying clear cell renal cell carcinoma. Cancer Research 76 1954-1964. (doi:10.1158/0008-5472.CAN-15-2622)
6. Bianco-Miotto T, Rodriguez Lopez C, Leemaqz S, Buckberry S, McCullough D, Zhuang Z, Dekker G, Wilkinson M & Roberts CT 2015 DNA methylation biomarkers for predicting pregnancy complications. Placenta 36 A38-A39. (doi:10.1016/j.placenta.2015.07.302)
7. Blair JD, Yuen RK, Lim BK, McFadden DE, von Dadelszen P & Robinson WP 2013 Widespread DNA hypomethylation at gene enhancer regions in placentas associated with early-onset pre-eclampsia. Molecular Human Reproduction 19 697-708. (doi:10.1093/molehr/gat044)
8. Chu T, Bunce K, Shaw P, Shridhar V, Althouse A, Hubel C & Peters D 2014 Comprehensive analysis of preeclampsia-associated DNA methylation in the placenta. PLoS ONE 9 e107318. (doi:10.1371/journal.pone.0107318)
9. Cotton AM, Avila L, Penaherrera MS, Affleck JG, Robinson WP & Brown CJ 2009 Inactive X chromosome-specific reduction in placental DNA methylation. Human Molecular Genetics 18 3544-3552. (doi:10.1093/hmg/ddp299)
10. Cotton AM, Lam L, Affleck JG, Wilson IM, Penaherrera MS, McFadden DE, Kobor MS, Lam WL, Robinson WP & Brown CJ 2011 Chromosome-wide DNA methylation analysis predicts human tissue-specific X inactivation. Human Genetics 130 187-201. (doi:10.1007/s00439-011-1007-8)
11. Das R, Lee YK, Strogantsev R, Jin S, Lim YC, Ng PY, Lin XM, Chng K, Yeo G, Ferguson-Smith AC et al. 2013 DNMT1 and AIM1 Imprinting in human placenta revealed through a genome-wide screen for allele-specific DNA methylation. BMC Genomics 14 685. (doi:10.1186/1471-2164-14-685)
12. Denis H, Ndlovu MN & Fuks F 2011 Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Reports 12 647-656. (doi:10.1038/embor.2011.110)
13. Dwi Putra SE, Neuber C, Reichetzeder C, Hocher B & Kleuser B 2014 Analysis of genomic DNA methylation levels in human placenta using liquid chromatography-electrospray ionization tandem mass spectrometry. Cellular Physiology and Biochemistry 33 945-952. (doi:10.1159/000358666)
14. Ehrlich M, Gama-Sosa MA, Huang LH, Midgett RM, Kuo KC, McCune RA & Gehrke C 1982 Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Research 10 2709-2721. (doi:10.1093/nar/10.8.2709)
15. Finer S, Mathews C, Lowe R, Smart M, Hillman S, Foo L, Sinha A, Williams D, Rakyan VK & Hitman GA 2015 Maternal gestational diabetes is associated with genome-wide DNA methylation variation in placenta and cord blood of exposed offspring. Human Molecular Genetics 24 3021-3029. (doi:10.1093/hmg/ddv013)
16. Fogarty NM, Burton GJ & Ferguson-Smith AC 2015 Different epigenetic states define syncytiotrophoblast and cytotrophoblast nuclei in the trophoblast of the human placenta. Placenta 36 796-802. (doi:10.1016/j.placenta.2015.05.006)
17. Fuke C, Shimabukuro M, Petronis A, Sugimoto J, Oda T, Miura K, Miyazaki T, Ogura C, Okazaki Y & Jinno Y 2004 Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Annals of Human Genetics 68 196-204. (doi:10.1046/j.1529-8817.2004.00081.x)
18. Goll MG & Bestor TH 2005 Eukaryotic cytosine methyltransferases. Annual Review of Biochemistry 74 481-514. (doi:10.1146/annurev.biochem.74.010904.153721)
19. Gordon L, Joo JE, Powell JE, Ollikainen M, Novakovic B, Li X, Andronikos R, Cruickshank MN, Conneely KN, Smith AK, Alisch RS, Morley R, Visscher PM, Craig JM & Saffery R 2012 Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Research 22 1395-1406. (doi:10.1101/gr.136598.111)
20. Graham CH & Lala PK 1992 Mechanisms of placental invasion of the uterus and their control. Biochemistry and Cell Biology 70 867-874. (doi:10.1139/o92-135)
21. Grigoriu A, Ferreira JC, Choufani S, Baczyk D, Kingdom J & Weksberg R 2011 Cell specific patterns of methylation in the human placenta. Epigenetics 6 368-379. (doi:10.4161/epi.6.3.14196)
22. Gude NM, Roberts CT, Kalionis B & King RG 2004 Growth and function of the normal human placenta. Thrombosis Research 114 397-407. (doi:10.1016/j.thromres.2004.06.038)
23. Guo H, Zhu P, Yan L, Li R, Hu B, Lian Y, Yan J, Ren X, Lin S, Li J et al. 2014 The DNA methylation landscape of human early embryos. Nature 511 606-610. (doi:10.1038/nature13544)
24. Hall E, Volkov P, Dayeh T, Esguerra JL, Salo S, Eliasson L, Ronn T, Bacos K & Ling C 2014 Sex differences in the genome-wide DNA methylation pattern and impact on gene expression, microRNA levels and insulin secretion in human pancreatic islets. Genome Biology 15 522. (doi:10.1186%2Fs13059-014-0522-z)
25. Hernando-Herraez I, Garcia-Perez R, Sharp AJ & Marques-Bonet T 2015 DNA methylation: insights into human evolution. PLoS Genetics 11 e1005661. (doi:10.1371/journal.pgen.1005661)
26. Hillman SL, Finer S, Smart MC, Mathews C, Lowe R, Rakyan VK, Hitman GA & Williams DJ 2015 Novel DNA methylation profiles associated with key gene regulation and transcription pathways in blood and placenta of growth-restricted neonates. Epigenetics 10 50-61. (doi:10.4161/15592294.2014.989741)
27. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P, Lee H, Aryee MJ, Irizarry RA, Kim K et al. 2010 Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467 338-342. (doi:10.1038/nature09367)
28. Jia RZ, Zhang X, Hu P, Liu XM, Hua XD, Wang X & Ding HJ 2012 Screening for differential methylation status in human placenta in preeclampsia using a CpG island plus promoter microarray. International Journal of Molecular Medicine 30 133-141.
29. Joo JE, Novakovic B, Cruickshank M, Doyle LW, Craig JM & Saffery R 2014 Human active X-specific DNA methylation events showing stability across time and tissues. European Journal of Human Genetics 22 1376-1381. (doi:10.1038/ejhg.2014.34)
30. Kanellopoulos-Langevin C, Caucheteux SM, Verbeke P & Ojcius DM 2003 Tolerance of the fetus by the maternal immune system: role of inflammatory mediators at the feto-maternal interface. Reproductive Biology and Endocrinology 1 121. (doi:10.1186/1477-7827-1-121)
31. Ke XS, Qu Y, Cheng Y, Li WC, Rotter V, Oyan AM & Kalland KH 2010 Global profiling of histone and DNA methylation reveals epigenetic-based regulation of gene expression during epithelial to mesenchymal transition in prostate cells. BMC Genomics 11 669. (doi:10.1186/1471-2164-11-669)
32. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LI et al. 2010 Epigenetic memory in induced pluripotent stem cells. Nature 467 285-290. (doi:10.1038/nature09342)
33. Lambertini L, Lee TL, Chan WY, Lee MJ, Diplas A, Wetmur J & Chen J 2011 Differential methylation of imprinted genes in growth-restricted placentas. Reproductive Sciences 18 1111-1117. (doi:10.1177/1933719111404611)
34. Leek JT, Johnson WE, Parker HS, Jaffe AE & Storey JD 2012 The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics 28 882-883. (doi:10.1093/bioinformatics/bts034)
35. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G, Antosiewicz-Bourget J, O'Malley R, Castanon R, Klugman S et al. 2011 Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471 68-73. (doi:10.1038/nature09798)
36. Liu L, Zhang X, Rong C, Rui C, Ji H, Qian YJ, Jia R & Sun L 2014 Distinct DNA methylomes of human placentas between pre-eclampsia and gestational diabetes mellitus. Cellular Physiology and Biochemistry 34 1877-1889. (doi:10.1159/000366386)
37. Lyall F 2002 The human placental bed revisited. Placenta 23 555-562. (doi:10.1053/plac.2002.0850)
38. Mayhew TM, Wijesekara J, Baker PN & Ong SS 2004 Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by preeclampsia. Placenta 25 829-833. (doi:10.1016/j.placenta.2004.04.011)
39. Moarii M, Boeva V, Vert JP & Reyal F 2015 Changes in correlation between promoter methylation and gene expression in cancer. BMC Genomics 16 873. (doi:10.1186/s12864-015-1994-2)
40. Morris TJ, Butcher LM, Feber A, Teschendorff AE, Chakravarthy AR, Wojdacz TK & Beck S 2014 ChAMP: 450k Chip Analysis Methylation Pipeline. Bioinformatics 30 428-430. (doi:10.1093/bioinformatics/btt682)
41. Murray MJ & Lessey BA 1999 Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis. Seminars in Reproductive Endocrinology 17 275-290.
42. Novakovic B, Rakyan V, Ng HK, Manuelpillai U, Dewi C, Wong NC, Morley R, Down T, Beck S, Craig JM et al. 2008 Specific tumour-associated methylation in normal human term placenta and first-trimester cytotrophoblasts. Molecular Human Reproduction 14 547-554. (doi:10.1093/molehr/gan046)
43. Novakovic B, Wong NC, Sibson M, Ng HK, Morley R, Manuelpillai U, Down T, Rakyan VK, Beck S, Hiendleder S et al. 2010 DNA methylation-mediated down-regulation of DNA methyltransferase-1 (DNMT1) is coincident with, but not essential for, global hypomethylation in human placenta. Journal of Biological Chemistry 285 9583-9593. (doi:10.1074/jbc.M109.064956)
44. Novakovic B, Gordon L, Wong NC, Moffett A, Manuelpillai U, Craig JM, Sharkey A & Saffery R 2011a Wide-ranging DNA methylation differences of primary trophoblast cell populations and derived cell lines: implications and opportunities for understanding trophoblast function. Molecular Human Reproduction 17 344-353. (doi:10.1093/molehr/gar005)
45. Novakovic B, Yuen RK, Gordon L, Penaherrera MS, Sharkey A, Moffett A, Craig JM, Robinson WP & Saffery R 2011b Evidence for widespread changes in promoter methylation profile in human placenta in response to increasing gestational age and environmental/stochastic factors. BMC Genomics 12 529. (doi:10.1186/1471-2164-12-529)
46. Ou X, Wang H, Qu D, Chen Y, Gao J & Sun H 2014 Epigenome-wide DNA methylation assay reveals placental epigenetic markers for noninvasive fetal single-nucleotide polymorphism genotyping in maternal plasma. Transfusion 54 2523-2533. (doi:10.1111/trf.12659)
47. Petropoulos S, Guillemin C, Ergaz Z, Dimov S, Suderman M, Weinstein-Fudim L, Ornoy A & Szyf M 2014 Gestational diabetes alters offspring DNA methylation profiles in human and rat: identification of key pathways involved in endocrine system disorders, insulin signaling, diabetes signaling, and ILK signaling. Endocrinology 156 2222-2238. (doi:10.1210/en.2014-1643)
48. Plongthongkum N, Diep DH & Zhang K 2014 Advances in the profiling of DNA modifications: cytosine methylation and beyond. Nature Reviews Genetics 15 647-661. (doi:10.1038/nrg3772)
49. Portela A & Esteller M 2010 Epigenetic modifications and human disease. Nature Biotechnology 28 1057-1068. (doi:10.1038/nbt.1685)
50. Price EM, Cotton AM, Penaherrera MS, McFadden DE, Kobor MS & Robinson W 2012 Different measures of "genome-wide" DNA methylation exhibit unique properties in placental and somatic tissues. Epigenetics 7 652-663. (doi:10.4161/epi.20221)
51. Rakyan VK, Down TA, Thorne NP, Flicek P, Kulesha E, Graf S, Tomazou EM, Backdahl L, Johnson N, Herberth M, Howe KL, Jackson DK, Miretti MM, Fiegler H, Marioni JC, Birney E, Hubbard TJ, Carter NP, Tavare S & Beck S 2008 An integrated resource for genome-wide identification and analysis of human tissue-specific differentially methylated regions (tDMRs). Genome Research 18 1518-1529. (doi:10.1101/gr.077479.108)
52. Roberts CT 2010 IFPA Award in placentology lecture: complicated interactions between genes and the environment in placentation, pregnancy outcome and long term health. Placenta 31 (Supplement) S47-S53. (doi:10.1016/j.placenta.2009.12.019)
53. Robinson WP & Price EM 2015 The human placental methylome. Cold Spring Harbor Perspectives in Medicine 5 a023044.
54. Ruchat SM, Houde AA, Voisin G, St-Pierre J, Perron P, Baillargeon JP, Gaudet D, Hivert MF, Brisson D & Bouchard L 2013 Gestational diabetes mellitus epigenetically affects genes predominantly involved in metabolic diseases. Epigenetics 8 935-943. (doi:10.4161/epi.25578)
55. Schroeder DI & LaSalle JM 2013 How has the study of the human placenta aided our understanding of partially methylated genes? Epigenomics 5 645-654. (doi:10.2217/epi.13.62)
56. Schroeder DI, Blair JD, Lott P, Yu HO, Hong D, Crary F, Ashwood P, Walker C, Korf I, Robinson WP et al. 2013 The human placenta methylome. PNAS 110 6037-6042. (doi:10.1073/pnas.1215145110)
57. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A & Meissner A 2012 A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484 339-344. (doi:10.1038/nature10960)
58. Tan L & Shi YG 2012 Tet family proteins and 5-hydroxymethylcytosine in development and disease. Development 139 1895-1902. (doi:10.1242/dev.070771)
59. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D & Beck S 2013 A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics 29 189-196. (doi:10.1093/bioinformatics/bts680)
60. Turan N, Ghalwash MF, Katari S, Coutifaris C, Obradovic Z & Sapienza C 2012 DNA methylation differences at growth related genes correlate with birth weight: a molecular signature linked to developmental origins of adult disease? BMC Medical Genomics 5 10. (doi:10.1186/1755-8794-5-10)
61. Yasukochi Y, Maruyama O, Mahajan MC, Padden C, Euskirchen GM, Schulz V, Hirakawa H, Kuhara S, Pan XH, Newburger PE et al. 2010 X chromosome-wide analyses of genomic DNA methylation states and gene expression in male and female neutrophils. PNAS 107 3704-3709. (doi:10.1073/pnas.0914812107)
62. Xiang Y, Zhang J, Li Q, Zhou X, Wang T, Xu M, Xia S, Xing Q, Wang L, He L & Zhao X 2014 DNA methylome profiling of maternal peripheral blood and placentas reveal potential fetal DNA markers for noninvasive prenatal testing. Molecular Human Reproduction 20 875-884. (doi:10.1093/molehr/gau048)
63. Yu N, Yan W, Yin T, Wang Y, Guo Y, Zhou D, Xu M, Ding J & Yang J 2015 HCG-Activated Human Peripheral Blood Mononuclear Cells (PBMC) Promote Trophoblast Cell Invasion. PLoS ONE 10 e0125589. (doi:10.1371/journal.pone.0125589)