5-Hydroxymethylcytosine-mediated alteration of transposon activity associated with the exposure to adverse in utero environments in human

Human Molecular Genetics

Volumn 25, Issue 11, 2016, Pages 2208-2219

  Sun, Miao ^a   Song, Mingxi M ^b   Wei, Bin ^a   Gao, Qinqin ^a   Li, Lingjun ^a   Yao, Bing ^b   Chen, Li ^b   Lin, Li ^b   Dai, Qing ^c   Zhou, Xiuwen ^a   Tao, Jianying ^a   Chen, Jie ^a   He, Chuan ^c   Jin, Peng ^b   Xu, Zhice ^a  

^a THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; ASCORBIC ACID; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE; DNA BINDING PROTEIN; ONCOPROTEIN; TET2 PROTEIN, HUMAN; TRANSPOSON;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE LOCUS; GENE ONTOLOGY; GENOMICS; HUMAN; HYPOXIA; NONHUMAN; PREECLAMPSIA; PREGNANCY DIABETES MELLITUS; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; TRANSPOSON; UMBILICAL VEIN; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PREGNANCY;

5-METHYLCYTOSINE; ADULT; ASCORBIC ACID; DIABETES, GESTATIONAL; DNA METHYLATION; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; PRE-ECLAMPSIA; PREGNANCY; PROTO-ONCOGENE PROTEINS;

EID: 84999008873     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw089     Document Type: Article

References (55)

1. Barker, D.J. (1990) The fetal and infant origins of adult disease. Br. Med. J., 301, 1111
2. Barker, D.J., Osmond, C., Golding, J., Kuh, D. and Wadsworth, M.E. (1989) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Br. Med. J., 298, 564-567.
3. Barker, D.J., Winter, P.D., Osmond, C., Margetts, B. and Simmonds, S.J. (1989) Weight in infancy and death from ischaemic heart disease. Lancet, 2, 577-580.
4. Calkins, K. and Devaskar, S.U. (2011) Fetal origins of adult disease. Curr. Probl. Pediatr. Adolesc. Health Care, 41, 158-176.
5. Page, K.A., Romero, A., Buchanan, T.A. and Xiang, A.H. (2014) Gestational diabetes mellitus, maternal obesity, and adiposity in offspring. J. Pediatr, 164, 807-810.
6. Holder, T., Giannini, C., Santoro, N., Pierpont, B., Shaw, M., Duran, E., Caprio, S. and Weiss, R. (2014) A low disposition index in adolescent offspring of mothers with gestational diabetes: a risk marker for the development of impaired glucose tolerance in youth. Diabetologia, 57, 2413-2420.
7. Kajantie, E., Eriksson, J.G., Osmond, C., Thornburg, K. and Barker, D.J. (2009) Pre-eclampsia is associated with increased risk of stroke in the adult offspring: the Helsinki birth cohort study. Stroke, 40, 1176-1180.
8. Palmsten, K., Buka, S.L. and Michels, K.B. (2010) Maternal pregnancy-related hypertension and risk for hypertension in offspring later in life. Obstet. Gynecol., 116, 858-864.
9. Daskalakis, G., Marinopoulos, S., Krielesi, V., Papapanagiotou, A., Papantoniou, N., Mesogitis, S. and Antsaklis, A. (2008) Placental pathology in women with gestational diabetes. Acta Obstet. Gynecol. Scand., 87, 403-407.
10. Koech, A., Ndungu, B. and Gichangi, P. (2008) Structural changes in umbilical vessels in pregnancy induced hypertension. Placenta, 29, 210-214.
11. Cetin, A., Kukner, A. and Ozturk, F. (2002) Ultrastructure of human umbilical vessels in pre-eclampsia. J. Matern. Fetal. Neonatal. Med., 12, 178-184.
12. Inan, S., Sanci, M., Can, D., Vatansever, S., Oztekin, O. and Tinar, S. (2002) Comparative morphological differences between umbilical cords from chronic hypertensive and preeclamptic pregnancies. Acta Med. Okayama, 56, 177-186.
13. Gao, Q., Tang, J., Chen, J., Jiang, L., Zhu, X. and Xu, Z. (2014) Epigenetic code and potential epigenetic-based therapies against chronic diseases in developmental origins. Drug Discov. Today, 19, 1744-1750.
14. Cutfield, W.S., Hofman, P.L., Mitchell, M. and Morison, I.M. (2007) Could epigenetics play a role in the developmental origins of health and disease? Pediatr. Res., 61, 68r-75r.
15. Raychaudhuri, N., Raychaudhuri, S., Thamotharan, M. and Devaskar, S.U. (2008) Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J. Biol. Chem., 283, 13611-13626.
16. Simmons, R.A. (2007) Developmental origins of beta-cell failure in type 2 diabetes: the role of epigenetic mechanisms. Pediatr. Res., 61, 64r-67r.
17. Heijmans, B.T., Tobi, E.W., Stein, A.D., Putter, H., Blauw, G.J., Susser, E.S., Slagboom, P.E. and Lumey, L.H. (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. U. S. A., 105, 17046-17049.
18. Rehan, V.K., Liu, J., Naeem, E., Tian, J., Sakurai, R., Kwong, K., Akbari, O. and Torday, J.S. (2012) Perinatal nicotine exposure induces asthma in second generation offspring. BMC Med., 10, 129.
19. Leslie, F.M. (2013) Multigenerational epigenetic effects of nicotine on lung function. BMC Med., 11, 27.
20. Kanaka-Gantenbein, C. (2010) Fetal origins of adult diabetes. Ann. N. Y. Acad. Sci., 1205, 99-105.
21. Gluckman, P.D., Hanson, M.A., Spencer, H.G. and Bateson, P. (2005) Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc. Biol. Sci., 272, 671-677.
22. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L. et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 324, 930-935.
23. Ito, S., Shen, L., Dai, Q., Wu, S.C., Collins, L.B., Swenberg, J.A., He, C. and Zhang, Y. (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science, 333, 1300-1303.
24. Pastor, W.A., Aravind, L. and Rao, A. (2013) TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol., 14, 341-356.
25. Ficz, G., Branco, M.R., Seisenberger, S., Santos, F., Krueger, F., Hore, T.A., Marques, C.J., Andrews, S. and Reik, W. (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature, 473, 398-402.
26. Kraus, T.F., Guibourt, V. and Kretzschmar, H.A. (2015) 5-Hydroxymethylcytosine, the "Sixth Base", during brain development and ageing. J. Neural Transm., 122, 1035-1043.
27. Kriaucionis, S. and Heintz, N. (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science, 324, 929-930.
28. Szulwach, K.E., Li, X., Li, Y., Song, C.X., Wu, H., Dai, Q., Irier, H., Upadhyay, A.K., Gearing, M., Levey, A.I. et al. (2011) 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci., 14, 1607-1616.
29. Irier, H., Street, R.C., Dave, R., Lin, L., Cai, C., Davis, T.H., Yao, B., Cheng, Y. and Jin, P. (2014) Environmental enrichment modulates 5-hydroxymethylcytosine dynamics in hippocampus. Genomics, 104, 376-382.
30. Nomura, Y., Lambertini, L., Rialdi, A., Lee, M., Mystal, E.Y., Grabie, M., Manaster, I., Huynh, N., Finik, J., Davey, M. et al. (2014) Global methylation in the placenta and umbilical cord blood from pregnancies with maternal gestational diabetes, preeclampsia, and obesity. Reprod. Sci., 21, 131-137.
31. He, J., Zhang, A., Fang, M., Fang, R., Ge, J., Jiang, Y., Zhang, H., Han, C., Ye, X., Yu, D. et al. (2013) Methylation levels at IGF2 and GNAS DMRs in infants born to preeclamptic pregnancies. BMC Genom., 14, 472.
32. Chen, D., Zhang, A., Fang, M., Fang, R., Ge, J., Jiang, Y., Zhang, H., Han, C., Ye, X., Huang, H. et al. (2014) Increased methylation at differentially methylated region of GNAS in infants born to gestational diabetes. BMC Med. Genet., 15, 108.
33. Xiang, Y., Zhang, X., Li, Q., Xu, J., Zhou, X., Wang, T., Xing, Q., Liu, Y., Wang, L., He, L. et al. (2013) Promoter hypomethylation of TIMP3 is associated with pre-eclampsia in a Chinese population. Mol. Hum. Reprod., 19, 153-159.
34. Lal, A.K., Gao, W. and Hibbard, J.U. (2013) Eclampsia: Maternal and neonatal outcomes. Pregnancy Hypertens., 3, 186-190.
35. Yao, B., Lin, L., Street, R.C., Zalewski, Z.A., Galloway, J.N., Wu, H., Nelson, D.L. and Jin, P. (2014) Genome-wide alteration of 5-hydroxymethylcytosine in a mouse model of fragile X-associated tremor/ataxia syndrome. Hum. Mol. Genet., 23, 1095-1107.
36. Huang, Y., Chavez, L., Chang, X., Wang, X., Pastor, W.A., Kang, J., Zepeda-Martinez, J.A., Pape, U.J., Jacobsen, S.E., Peters, B. et al. (2014) Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells. Proc. Natl Acad. Sci. U. S. A, 111, 1361-1366.
37. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
38. Gellhaus, A., Schmidt, M., Dunk, C., Lye, S.J. and Winterhager, E. (2007) The circulating proangiogenic factors CYR61 (CCN1) and NOV (CCN3) are significantly decreased in placentae and sera of preeclamptic patients. Reprod. Sci., 14, 46-52.
39. Tsankov, A.M., Gu, H., Akopian, V., Ziller, M.J., Donaghey, J., Amit, I., Gnirke, A. and Meissner, A. (2015) Transcription factor binding dynamics during human ES cell differentiation. Nature, 518, 344-349.
40. Wang, G.L., Jiang, B.H., Rue, E.A. and Semenza, G.L. (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl Acad. Sci. U. S. A., 92, 5510-5514.
41. Pal, A., Srivastava, T., Sharma, M.K., Mehndiratta, M., Das, P., Sinha, S. and Chattopadhyay, P. (2010) Aberrant methylation and associated transcriptional mobilization of Alu elements contributes to genomic instability in hypoxia. J. Cell Mol. Med., 14, 2646-2654.
42. Krause, B.J., Costello, P.M., Munoz-Urrutia, E., Lillycrop, K.A., Hanson, M.A. and Casanello, P. (2013) Role of DNA methyltransferase 1 on the altered eNOS expression in human umbilical endothelium from intrauterine growth restricted fetuses. Epigenetics, 8, 944-952.
43. Blaschke, K., Ebata, K.T., Karimi, M.M., Zepeda-Martinez, J.A., Goyal, P., Mahapatra, S., Tam, A., Laird, D.J., Hirst, M., Rao, A. et al. (2013) Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature, 500, 222-226.
44. Barker, D.J. (1998) In utero programming of chronic disease. Clin. Sci., 95, 115-128.
45. Brenseke, B., Prater, M.R., Bahamonde, J. and Gutierrez, J.C. (2013) Current thoughts on maternal nutrition and fetal programming of themetabolic syndrome. J. Pregnancy, 2013, 368461.
46. Mimura, I., Nangaku, M., Kanki, Y., Tsutsumi, S., Inoue, T., Kohro, T., Yamamoto, S., Fujita, T., Shimamura, T., Suehiro, J. et al. (2012) Dynamic change of chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of hypoxia-inducible factor 1 and KDM3A. Mol. Cell Biol., 32, 3018-3032.
47. Kazazian, H.H. Jr. (2004) Mobile elements: drivers of genome evolution. Science, 303, 1626-1632.
48. Wilson, A.S., Power, B.E. and Molloy, P.L. (2007) DNA hypomethylation and human diseases. Biochim. Biophys. Acta, 1775, 138-162.
49. Leung, D., Du, T., Wagner, U., Xie, W., Lee, A.Y., Goyal, P., Li, Y., Szulwach, K.E., Jin, P., Lorincz, M.C. et al. (2014) Regulation of DNA methylation turnover at LTR retrotransposons and imprinted loci by the histone methyltransferase Setdb1. Proc. Natl Acad. Sci. U. S. A., 111, 6690-6695.
50. Olcina, M.M., Leszczynska, K.B., Senra, J.M., Isa, N.F., Harada, H. and Hammond, E.M. (2016) H3K9me3 facilitates hypoxiainduced p53-dependent apoptosis through repression of APAK. Oncogene, 35, 793-799.
51. Conde-Agudelo, A., Romero, R., Kusanovic, J.P. and Hassan, S.S. (2011) Supplementation with vitamins C and E during pregnancy for the prevention of preeclampsia and other adverse maternal and perinatal outcomes: a systematic review andmetaanalysis. Am. J. Obstet. Gynecol., 204, 503. e1-e12.
52. Poston, L., Briley, A.L., Seed, P.T., Kelly, F.J. and Shennan, A.H. (2006) Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial. Lancet, 367, 1145-1154.
53. Abramovici, a., Gandley, R., Clifton, R., Leveno, K., Myatt, L., Wapner, R., Thorp, J., Jr., Mercer, B., Peaceman, A., Samuels, P. et al. (2015) Prenatal vitamin C and E supplementation in smokers is associated with reduced placental abruption and preterm birth: a secondary analysis. Bjog, 122, 1740-1747.
54. Debnath, M., Venkatasubramanian, G. and Berk, M. (2015) Fetal programming of schizophrenia: select mechanisms. Neurosci. Biobehav. Rev., 49, 90-104.
55. Shen, L., Shao, N., Liu, X. and Nestler, E. (2014) ngs. plot: quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics, 15, 284.