Association between placental global DNA methylation and blood pressure during human pregnancy.


Journal

Journal of hypertension
ISSN: 1473-5598
Titre abrégé: J Hypertens
Pays: Netherlands
ID NLM: 8306882

Informations de publication

Date de publication:
01 05 2022
Historique:
pubmed: 1 3 2022
medline: 6 5 2022
entrez: 28 2 2022
Statut: ppublish

Résumé

Gene-specific placental DNA methylation patterns differ between normal pregnancies and pregnancies complicated by hypertension. However, whether global placental DNA methylation is associated with maternal blood pressure remains controversial. Using multiple linear regression models, we analysed the association between maternal mean arterial pressure (MAP) at the third trimester of pregnancy and global DNA methylation in the placenta in 922 mothers using LC-ESI-MS/MS. To better characterize the contribution of genetic or epigenetic mechanisms, we performed isolated analyses in mothers with and without a family history of hypertension. Mean placental global DNA methylation was 3.00 ± 0.46%. A significant negative correlation between placental global DNA methylation and mean arterial blood pressure (MAP) in the third trimester could be observed (P = 0.023, r = -0.075). This association remained significant after adjusting for confounders. In placenta samples from mothers with a family history of hypertension, mean maternal MAP was higher (86.1 ± 8.1 vs. 84.6 ± 7.5, P < 0.01) and placental global DNA methylation was lower (2.94 ± 0.43 vs. 3.04 ± 0.47, P < 0.01) compared with samples without a family history of hypertension. Furthermore, the significant independent negative correlation between global placental DNA methylation and MAP was only found in mothers without a family history of hypertension. This study showed an independent negative correlation between placental global DNA methylation and maternal MAP in mothers without a family history of hypertension.

Identifiants

pubmed: 35221324
doi: 10.1097/HJH.0000000000003103
pii: 00004872-202205000-00021
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1002-1009

Informations de copyright

Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.

Références

Hall ME, George EM, Granger JP. The heart during pregnancy. Rev Espariol Cardiol (English Edition) 2011; 64:1045–1050.
Grindheim G, Estensen M-E, Langesaeter E, Rosseland LA, Toska K. Changes in blood pressure during healthy pregnancy: a longitudinal cohort study. J Hypertens 2012; 30:342–350.
Pirani BBK, Campbell DM, MacGillivray I. Plasma volume in normal first pregnancy. J Obstet Gynaecol Br Commonw 1973; 80:884–887.
Clapp MJF III, Capeless E. Cardiovascular function before, during, and after the first and subsequent pregnancies. Am J Cardiol 1997; 80:1469–1473.
Chung E, Leinwand LA. Pregnancy as a cardiac stress model. Cardiovasc Res 2014; 101:561–570.
Valdes G, Kaufmann P, Corthorn J, Erices R, Brosnihan KB, Joyner-Grantham J. Vasodilator factors in the systemic and local adaptations to pregnancy. Reprod Biol Endocrinol 2009; 7:79.
Iliodromiti Z, Antonakopoulos N, Sifakis S, Tsikouras P, Daniilidis A, Dafopoulos K. Endocrine, paracrine, and autocrine placental mediators in labor. Hormones (Athens) 2012; 11:397–409.
Maccani MA, Marsit CJ. Epigenetics in the placenta. Am J Reprod Immunol 2009; 62:78–89.
Bell JT, Spector TD. A twin approach to unraveling epigenetics. Trends Genet 2011; 27:116–125.
Kulkarni A, Chavan-Gautam P, Mehendale S, Yadav H, Joshi S. Global DNA methylation patterns in placenta and its association with maternal hypertension in preeclampsia. DNA Cell Biol 2011; 30:79–84.
Nomura Y, Lambertini L, Rialdi A, Lee M, Mystal EY, Grabie Mua. Global methylation in the placenta and umbilical cord blood from pregnancies with maternal gestational diabetes, preeclampsia, and obesity. Reprod Sci 2014; 21:131–137.
Poon LCY, Kametas NA, Valencia C, Chelemen T, Nicolaides KH. Hypertensive disorders in pregnancy: screening by systolic diastolic and mean arterial pressure at 11-13 weeks. Hypertens Pregnancy 2011; 30:93–107.
Cnossen JS, Vollebregt KC, de Vrieze N, ter Riet G, Mol BWJ, Franx Aua. Accuracy of mean arterial pressure and blood pressure measurements in predicting preeclampsia: systematic review and meta-analysis. BMJ 2008; 336:1117–1120.
Hocher B, Slowinski T, Stolze T, Pleschka A, Neumayer HH, Halle H. Association of maternal G protein beta3 subunit 825T allele with low birthweight. Lancet 2000; 355:1241–1242.
Pfab T, Slowinski T, Godes M, Halle H, Priem F, Hocher B. Low birth weight, a risk factor for cardiovascular diseases in later life, is already associated with elevated fetal glycosylated hemoglobin at birth. Circulation 2006; 114:1687–1692.
Nair AV, Hocher B, Verkaart S, van Zeeland F, Pfab T, Slowinski Tua. Loss of insulin-induced activation of TRPM6 magnesium channels results in impaired glucose tolerance during pregnancy. Proc Natl Acad Sci U S A 2012; 109:11324–11329.
Zheng L, Sun Z, Li J, Zhang R, Zhang X, Liu S. Pulse pressure and mean arterial pressure in relation to ischemic stroke among patients with uncontrolled hypertension in rural areas of China. Stroke 2008; 39:1932–1937.
Dwi Putra SE, Neuber C, Reichetzeder C, Hocher B, Kleuser B. Analysis of genomic DNA methylation levels in human placenta using liquid chromatography-electrospray ionization tandem mass spectrometry. Cell Physiol Biochem 2014; 33:945–952.
Adkins RM, Thomas F, Tylavsky FA, Krushkal J. Parental ages and levels of DNA methylation in the newborn are correlated. BMC Med Genet 2011; 12:47.
Fuke C, Shimabukuro M, Petronis A, Sugimoto J, Oda T, Miura K. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann Hum Genet 2004; 68:196–204.
Zhang FF, Cardarelli R, Carroll J, Fulda KG, Kaur M, Gonzalez K. Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics 2011; 6:623–629.
Adkins RM, Krushkal J, Tylavsky FA, Thomas F. Racial differences in gene-specific DNA methylation levels are present at birth. Birth Defects Res Part A Clin Mol Teratol 2011; 91:728–736.
Magriples U, Boynton MH, Kershaw TS, Rising SS, Ickovics JR. Blood pressure changes during pregnancy: impact of race, body mass index, and weight gain. Am J Perinatol 2013; 30:415–424.
Papachatzi E, Dimitriou G, Dimitropoulos K, Vantarakis A. Prepregnancy obesity: maternal, neonatal and childhood outcomes. J Neonatal Perinatal Med 2013; 6:203–216.
Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS One 2011; 6:e25254.
McEniery CM, Yasmin, Wallace S, Maki-Petaja K, McDonnell B, Sharman JE. Increased stroke volume and aortic stiffness contribute to isolated systolic hypertension in young adults. Hypertension 2005; 46:221–226.
Lampinen R, Vehviläinen-Julkunen K, Kankkunen P. A review of pregnancy in women over 35 years of age. Open Nurs J 2009; 3:33–38.
Tin LL, Beevers DG, Lip GYH. Systolic vs diastolic blood pressure and the burden of hypertension. J Hum Hypertens 2002; 16:147–150.
Workalemahu T, Ouidir M, Shrestha D, Wu J, Grantz KL, Tekola-Ayele F. Differential DNA methylation in placenta associated with maternal blood pressure during pregnancy. Hypertens Am Heart Assoc 2020; 75:1117–1124.
Vaiman D. Placental methylome under pressure. Hypertens Am Heart Assoc 2020; 75:938–940.
Smolarek I, Wyszko E, Barciszewska AM, Nowak S, Gawronska I, Jablecka Aua. Global DNA methylation changes in blood of patients with essential hypertension. Med Sci Monit 2010; 16:CR149–CR155.
Turcot V, Tchernof A, Deshaies Y, Pérusse L, Bélisle A, Marceau S. LINE-1 methylation in visceral adipose tissue of severely obese individuals is associated with metabolic syndrome status and related phenotypes. Clin Epigenetics 2012; 4:10.
Alexeeff SE, Baccarelli AA, Halonen J, Coull BA, Wright RO, Tarantini L. Association between blood pressure and DNA methylation of retrotransposons and pro-inflammatory genes. Int J Epidemiol 2013; 42:270–280.
Lisanti S, Omar WAW, Tomaszewski B, De Prins S, Jacobs G, Koppen G. Comparison of methods for quantification of global DNA methylation in human cells and tissues. PLoS One 2013; 8:e79044.
Simar D, Versteyhe S, Donkin I, Liu J, Hesson L, Nylander Vua. DNA methylation is altered in B and NK lymphocytes in obese and type 2 diabetic human. Metab Clin Exp 2014; 63:1188–1197.
Zhao J, Goldberg J, Bremner JD, Vaccarino V. Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 2012; 61:542–546.
Paravicini TM, Touyz RM. Redox signaling in hypertension. Cardiovasc Res 2006; 71:247–258.
Wu Q, Ni X. ROS-mediated DNA methylation pattern alterations in carcinogenesis. Curr Drug Targets 2015; 16:13–19.
Tunc O, Tremellen K. Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 2009; 26:537–544.
Vlahos A, Mansell T, Saffery R, Novakovic B. Human placental methylome in the interplay of adverse placental health, environmental exposure, and pregnancy outcome. PLoS Genet 2019; 15:e1008236.
Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21:5400–5413.
Ehrlich M, Gama-Sosa MA, Huang L-H, Midgett RM, Kuo KC, McCune RA. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues or cells. Nucleic Acids Res 1982; 10:2709–2721.
Chatterjee A, Macaulay EC, Rodger EJ, Stockwell PA, Parry MF, Roberts HE. Placental hypomethylation is more pronounced in genomic loci devoid of retroelements. G3 (Bethesda) 2016; 6:1911–1921.
Wilhelm-Benartzi CS, Houseman EA, Maccani MA, Poage GM, Koestler DC, Langevin SM. In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta. Environ Health Perspect 2012; 120:296–302.
Serman L, Vlahović M, Sijan M, Bulić-Jakus F, Serman A, Sincić N. The impact of 5-azacytidine on placental weight, glycoprotein pattern and proliferating cell nuclear antigen expression in rat placenta. Placenta 2007; 28:803–811.
Ziller MJ, Gu H, Müller F, Donaghey J, Tsai LT-Y, Kohlbacher O. Charting a dynamic DNA methylation landscape ofthe human genome. Nature 2013; 500:477–481.
Novak P, Stampfer MR, Munoz-Rodriguez JL, Garbe JC, Ehrich M, Futscher BW. Cell-type specific DNA methylation patterns define human breast cellular identity. PLoS One 2012; 7:e52299.
Futscher BW, Oshiro MM, Wozniak RJ, Holtan N, Hanigan CL, Duan H. Role for DNA methylation in the control of cell type specific maspin expression. Nat Genet 2002; 31:175–179.
Oshiro MM, Futscher BW, Lisberg A, Wozniak RJ, Klimecki WT, Domann FE. Epigenetic regulation of the cell type-specific gene 14-3–3sigma. Neoplasia 2005; 7:799–808.
Avila L, Yuen RK, Diego-Alvarez D, Peñaherrera MS, Jiang R, Robinson WP. Evaluating DNA methylation and gene expression variability in the human term placenta. Placenta 2010; 31:1070–1077.
Non AL, Binder AM, Barault L, Rancourt RC, Kubzansky LD, Michels KB. DNA methylation of stress-related genes and LINE-1 repetitive elements across the healthy human placenta. Placenta 2012; 33:183–187.
Vilahur N, Baccarelli AA, Bustamante M, Agramunt S, Byun H-M, Fernandez MFua. Storage conditions and stability of global DNA methylation in placental tissue. Epigenomics 2013; 5:341–348.
Liu J. Liquid chromatography tandem mass spectrometry for the measurement of global DNA methylation and hydroxymethylation. J Proteom Bioinform 2013; 1:
Janssen BG, Godderis L, Pieters N, Poels K, Kiciński M, Cuypers Aua. Placental DNA hypomethylation in association with particulate air pollution in early life. Particle Fibre Toxicol 2013; 10:22.

Auteurs

Sulistyo E Dwi Putra (SED)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology/Pneumology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
University of Surabaya, Surabaya, Indonesia.

Christoph Reichetzeder (C)

Institute of Nutritional Science, Department of Nutritional Toxicology, University of Potsdam, Nuthetal.

Karoline von Websky (K)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology/Pneumology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Institute of Nutritional Science, Department of Nutritional Toxicology, University of Potsdam, Nuthetal.

Corinna Neuber (C)

Institute of Nutritional Science, Department of Nutritional Toxicology, University of Potsdam, Nuthetal.

Horst Halle (H)

Department of Obstetrics and Gynecology, Charite University Hospital, Campus Mitte.

Burkard Kleuser (B)

Institute of Pharmacy, Department of Pharmacology, Freie Universität Berlin, Berlin.

Bernhard K Krämer (BK)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology/Pneumology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
European Center for Angioscience ECAS, Medical Faculty Mannheim of the University of Heidelberg, Mannheim, Germany.

Berthold Hocher (B)

Fifth Department of Medicine (Nephrology/Endocrinology/Rheumatology/Pneumology), University Medical Centre Mannheim, University of Heidelberg, Heidelberg, Germany.
Key Laboratory of Study and Discovery of Small Targeted Molecules of Hunan Province, School of Medicine, Hunan Normal University.
eproductive and Genetic Hospital of CITIC-Xiangya, Changsha, China.
Institute of Medical Diagnostics (IMD), Berlin, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH