Investigating the influence of maternal cortisol and emotional state during pregnancy on the DNA methylation status of the glucocorticoid receptor gene (NR3C1) promoter region in cord blood

Journal of Psychiatric Research

Volumn 47, Issue 7, 2013, Pages 880-891

  Hompes, Titia ^a   Izzi, Benedetta ^b   Gellens, Edith ^a   Morreels, Maarten ^a   Fieuws, Steffen ^c,d   Pexsters, Anne ^a   Schops, Ganel ^a   Dom, Myriam ^a   Van Bree, Rieta ^a   Freson, Kathleen ^b   Verhaeghe, Johan ^a   Spitz, Bernard ^a   Demyttenaere, Koen ^a   Glover, Vivette ^e   Van den Bergh, Bea ^f,g   Allegaert, Karel ^a   Claes, Stephan ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c KU LEUVEN   (Belgium)

^d HASSELT UNIVERSITY   (Belgium)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f TILBURG UNIVERSITY   (Netherlands)

^g UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Maternal anxiety; Maternal HPA axis; Methylation state NR3C1; Prenatal maternal emotional wellbeing

Indexed keywords

GENOMIC DNA; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOID RECEPTOR NR3C1; HYDROCORTISONE; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR INDUCIBLE PROTEIN A; UNCLASSIFIED DRUG;

ADULT; ANXIETY; ARTICLE; BINDING SITE; CIRCADIAN RHYTHM; CPG ISLAND; DELIVERY; DEPRESSION; DNA METHYLATION; EMOTION; EXON; FEAR; FEMALE; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; HUMAN; MAJOR CLINICAL STUDY; MATERNAL STRESS; MONONUCLEAR CELL; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PSYCHOLOGICAL ASPECT; PSYCHOLOGICAL WELL BEING; UMBILICAL CORD BLOOD;

EID: 84877119617     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2013.03.009     Document Type: Article

References (42)

1. Bird A. Molecular biology. Methylation talk between histones and DNA. Science 2001, 294:2113-2115.
2. van den Boom D., Ehrich M. Mass spectrometric analysis of cytosine methylation by base-specific cleavage and primer extension methods. Methods in Molecular Biology 2009, 507:207-227.
3. Cao-Lei L., Leija S.C., Kumsta R., Wust S., Meyer J., Turner J.D., et al. Transcriptional control of the human glucocorticoid receptor: identification and analysis of alternative promoter regions. Human Genetics 2011, 129:533-543.
4. Clarke A.S., Wittwer D.J., Abbott D.H., Schneider M.L. Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Developmental Psychobiology 1994, 27:257-269.
5. Coolen M.W., Statham A.L., Gardiner-Garden M., Clark S.J. Genomic profiling of CpG methylation and allelic specificity using quantitative high-throughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Research 2007, 35:e119.
6. Cox J.L., Holden J.M., Sagovsky R. Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. British Journal of Psychiatry 1987, 150:782-786.
7. Cranley M.S. Development of a tool for the measurement of maternal attachment during pregnancy. Nursing Research 1981, 30:281-284.
8. de W.C., Buitelaar J.K. Cortisol awakening response in pregnant women. Psychoneuroendocrinology 2005, 30:902-907.
9. Freson K., Izzi B., Jaeken J., Van H.M., Thys C., Wittevrongel C., et al. Compound heterozygous mutations in the GNAS gene of a boy with morbid obesity, thyroid-stimulating hormone resistance, pseudohypoparathyroidism, and a prothrombotic state. Journal of Clinical Endocrinology & Metabolism 2008, 93:4844-4849.
10. Gaynes B.N., Gavin N., Meltzer-Brody S., Lohr K.N., Swinson T., Gartlehner G., et al. Perinatal depression: prevalence, screening accuracy, and screening outcomes. Evidence Report/Technology Assessment (Summary) 2005, 1-8.
11. Giardinelli L., Innocenti A., Benni L., Stefanini M.C., Lino G., Lunardi C., et al. Depression and anxiety in perinatal period: prevalence and risk factors in an Italian sample. Archives of Women's Mental Health 2012, 15:21-30.
12. Glover V., O'Connor T.G., O'Donnell K. Prenatal stress and the programming of the HPA axis. Neuroscience & Biobehavioral Reviews 2010, 35:17-22.
13. Gluckman P.D., Hanson M.A. Living with the past: evolution, development, and patterns of disease. Science 2004, 305:1733-1736.
14. Gluckman P.D., Hanson M.A., Cooper C., Thornburg K.L. Effect of in utero and early-life conditions on adult health and disease. New England Journal of Medicine 2008, 359:61-73.
15. Grant K.A., McMahon C., Austin M.P. Maternal anxiety during the transition to parenthood: a prospective study. Journal of Affective Disorders 2008, 108:101-111.
16. Green J.M., Murray D. The use of the Edinburgh postnatal depression scale in research to explore the relationship between antenatal and postnatal dysphoria. Perinatal psychiatry: the use and misuse of the Edinburgh postnatal depression scale 1994, 180-215. Gaskell, London. J.L. Cox, J.M. Holden (Eds.).
17. Hompes T., Vrieze E., Fieuws S., Simons A., Jaspers L., Van B.J., et al. The influence of maternal cortisol and emotional state during pregnancy on fetal intrauterine growth. Pediatric Research 2012, 72(3):305-315.
18. Huizink A.C., Mulder E.J., Robles de Medina P.G., Visser G.H., Buitelaar J.K. Is pregnancy anxiety a distinctive syndrome?. Early Human Development 2004, 79:81-91.
19. Izzi B., Decallonne B., Devriendt K., Bouillon R., Vanderschueren D., Levtchenko E., et al. Anew approach to imprinting mutation detection in GNAS by Sequenom EpiTYPER system. Clinica Chimica Acta 2010, 411:2033-2039.
20. Izzi B., Francois I., Labarque V., Thys C., Wittevrongel C., Devriendt K., et al. Methylation defect in imprinted genes detected in patients with an Albright's hereditary osteodystrophy like phenotype and platelet Gs hypofunction. PLoS One 2012, 7:e38579.
21. Lam L.L., Emberly E., Fraser H.B., Neumann S.M., Chen E., Miller G.E., et al. Factors underlying variable DNA methylation in a human community cohort. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(Suppl. 2):17253-17260.
22. Levine A., Zagoory-Sharon O., Feldman R., Lewis J.G., Weller A. Measuring cortisol in human psychobiological studies. Physiology & Behavior 2007, 90:43-53.
23. McCormick J.A., Lyons V., Jacobson M.D., Noble J., Diorio J., Nyirenda M., et al. 5'-heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Molecular Endocrinology 2000, 14:506-517.
24. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience 2009, 12:342-348.
25. Meaney M.J., Ferguson-Smith A.C. Epigenetic regulation of the neural transcriptome: the meaning of the marks. Nature Neuroscience 2010, 13:1313-1318.
26. Meaney M.J., Szyf M., Seckl J.R. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in Molecular Medicine 2007, 13:269-277.
27. Mulligan C.J., D'Errico N.C., Stees J., Hughes D.A. Methylation changes at NR3C1 in newborns associate with maternal prenatal stress exposure and newborn birth weight. Epigenetics 2012, 7:853-857.
28. Obel C., Hedegaard M., Henriksen T.B., Secher N.J., Olsen J., Levine S. Stress and salivary cortisol during pregnancy. Psychoneuroendocrinology 2005, 30:647-656.
29. Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
30. Radtke K.M., Ruf M., Gunter H.M., Dohrmann K., Schauer M., Meyer A., et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Translational Psychiatry 2011, 1:e21.
31. Sarkar P., Bergman K., Fisk N.M., Glover V. Maternal anxiety at amniocentesis and plasma cortisol. Prenatal Diagnosis 2006, 26:505-509.
32. Schneider M.L., Roughton E.C., Koehler A.J., Lubach G.R. Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability. Child Development 1999, 70:263-274.
33. Schulte H.M., Weisner D., Allolio B. The corticotrophin releasing hormone test in late pregnancy: lack of adrenocorticotrophin and cortisol response. Clinical Endocrinology (Oxford) 1990, 33:99-106.
34. Schweder T., Spjotvoll E. Plots of p-values to evaluate many tests simultaneously. Biometrika 1982, 69:493-502.
35. Spielberger C.D. Manual for state-trait anxiety inventory 1983, Consulting Psychologist Press, Palo Alto, CA.
36. Turner J.D., Muller C.P. Structure of the glucocorticoid receptor (NR3C1) gene 5' untranslated region: identification, and tissue distribution of multiple new human exon 1. Journal of Molecular Endocrinology 2005, 35:283-292.
37. Tyrka A.R., Price L.H., Marsit C., Walters O.C., Carpenter L.L. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One 2012, 7:e30148.
38. Van den Bergh B.R. Developmental programming of early brain and behaviour development and mental health: a conceptual framework. Developmental Medicine & Child Neurology 2011, 53(Suppl. 4):19-23.
39. Van den Bergh B.R., Mulder E.J., Mennes M., Glover V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neuroscience & Biobehavioral Reviews 2005, 29:237-258.
40. Weaver I.C., Diorio J., Seckl J.R., Szyf M., Meaney M.J. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Annals of the New York Academy of Sciences 2004, 1024:182-212.
41. Weinstock M., Poltyrev T., Schorer-Apelbaum D., Men D., McCarty R. Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats. Physiology & Behavior 1998, 64:439-444.
42. Zhang T.Y., Hellstrom I.C., Bagot R.C., Wen X., Diorio J., Meaney M.J. Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. Journal of Neuroscience 2010, 30:13130-13137.