Alterations to Placental Glucocorticoid Receptor Expression with Alcohol Consumption.


Journal

Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249

Informations de publication

Date de publication:
05 2021
Historique:
received: 31 07 2020
accepted: 23 11 2020
pubmed: 8 1 2021
medline: 28 1 2022
entrez: 7 1 2021
Statut: ppublish

Résumé

Maternal alcohol consumption during pregnancy results in elevated vulnerability to intrauterine growth restriction, preterm birth, miscarriage, and stillbirth. Many of the detrimental effects of fetal alcohol exposure may be mediated through placental dysfunction; however, the exact mechanisms remain unknown. Here, we aimed to determine the effect of maternal alcohol exposure prior to and during early pregnancy on placental glucocorticoid receptor (GR) isoforms, associated GR regulated genes, and infant outcomes. Participants carrying singleton fetuses (n = 113) were recruited during early pregnancy. Amount and type of alcohol consumed over the last 12 months were obtained at 18 weeks of gestation. The level of drinking was separated into none (0 g/day), low (< 10 g/day), moderate (10-100 g/day), and heavy (> 100 g/day). At delivery, placental weight, infant sex, birthweight, and head circumference were recorded. Placental GR isoforms and genes involved in downstream signalling pathways were quantified. The majority of women (70.8%) consumed alcohol. Of these, most consumed low (48.8%) or moderate (37.5%) amounts. Placental weight was unaffected by alcohol consumption, but infants born to heavy drinkers tended to be lighter at birth. In female, but not male, placentae, maternal alcohol consumption resulted in increased GRαC and decreased GRαD1 cytoplasmic expression. In both female and male placentae, a dampened inflammatory response was evident with maternal alcohol consumption, involving downregulated IL6R and upregulated POU2F2 gene expression, respectively. Maternal alcohol consumption in the months prior to, and/or during early, pregnancy alters placental GR isoform and expression of some inflammatory genes in a sex-specific manner.

Identifiants

pubmed: 33409870
doi: 10.1007/s43032-020-00413-1
pii: 10.1007/s43032-020-00413-1
doi:

Substances chimiques

Protein Isoforms 0
Receptors, Glucocorticoid 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1390-1402

Références

Substance Abuse and Mental Health Services Administration (SAMHSA). Alcohol use in lifetime, past year, and past month among persons aged 12 or older, by detailed age category: percentages, 2016 and 2017. 2017 National Survey on Drug Use and Health (NSDUH) 2017; Available from: https://www.samhsa.gov/data/sites/default/files/cbhsq-reports/NSDUHDetailedTabs2017/NSDUHDetailedTabs2017.htm#tab2-19B . Accessed 26 Apr 2020.
Mazza D, Harrison C, Taft A, Brijnath B, Britt H, Hobbs M, et al. Current contraceptive management in Australian general practice: an analysis of BEACH data. Med J Aust. 2012;197(2):110–4.
pubmed: 22794058
(AIHW), A.I.o.H.a.W., National Drug Strategy Household Survey detailed report 2013. 2014, Australian Institute of Health and Welfare: Canberra.
Australian Government., Australian guidelines to reduce health risks from drinking alcohol, N.H.a.M.R. Council., Editor. 2009, NHMRC: Canberra.
Spohr, H.-L., J. Willms, and H.-C.J.T.L. Steinhausen, Prenatal alcohol exposure and long-term developmental consequences 1993. 341(8850): p. 907–910.
Kalisch-Smith JI, et al. Periconceptional alcohol exposure causes female-specific perturbations to trophoblast differentiation and placental formation in the rat. Development. 2019;146(11):dev172205.
pubmed: 31182432
Gårdebjer EM, Cuffe JSM, Pantaleon M, Wlodek ME, Moritz KM. Periconceptional alcohol consumption causes fetal growth restriction and increases glycogen accumulation in the late gestation rat placenta. Placenta. 2014;35(1):50–7.
pubmed: 24239160
Gardebjer EM, et al. Maternal alcohol intake around the time of conception causes glucose intolerance and insulin insensitivity in rat offspring, which is exacerbated by a postnatal high-fat diet. FASEB J. 2015;29(7):2690–701.
pubmed: 25733565
Gluckman PD, Cutfield W, Hofman P, Hanson MA. The fetal, neonatal, and infant environments-the long-term consequences for disease risk. Early Hum Dev. 2005;81(1):51–9.
pubmed: 15707715
Barker D, et al. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993;341(8850):938–41.
pubmed: 8096277
Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;303(6809):1019–22.
pubmed: 1954451 pmcid: 1671766
Barker D. The developmental origins of chronic adult disease. Acta Paediatr. 2004;93(s446):26–33.
Clifton VL et al. Alterations of Placental Vascular Function in Asthmatic Pregnancies 2001. 164(4): p. 546–553.
Bale TL. The placenta and neurodevelopment: sex differences in prenatal vulnerability. Dialogues Clin Neurosci. 2016;18(4):459–64.
pubmed: 28179817 pmcid: 5286731
Burd L, Blair J, Dropps K. Prenatal alcohol exposure, blood alcohol concentrations and alcohol elimination rates for the mother, fetus and newborn. J Perinatol. 2012;32(9):652–9.
pubmed: 22595965
Carter RC et al. Alcohol-related alterations in placental imprinted gene expression in humans mediate effects of prenatal alcohol exposure on postnatal growth 2018. 42(8): p. 1431–1443.
Bocking AD, et al. Increased uteroplacental production of prostaglandin E2 during ethanol infusion. Am J Phys. 1993;265(3 Pt 2):R640–5.
Gabriel K, Hofmann C, Glavas M, Weinberg J. The hormonal effects of alcohol use on the mother and fetus. Alcohol Health Res World. 1998;22(3):170–7.
pubmed: 15706792 pmcid: 6761898
Chapman K, Holmes M, Seckl J. 11β-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol Rev. 2013;93(3):1139–206.
pubmed: 23899562 pmcid: 3962546
Yu L, Zhou J, Zhang G, Huang W, Pei L, Lv F, et al. cAMP/PKA/EGR1 signaling mediates the molecular mechanism of ethanol-induced inhibition of placental 11β-HSD2 expression. Toxicol Appl Pharmacol. 2018;352:77–86.
pubmed: 29802914
Liang, G., et al., Ethanol-induced inhibition of fetal hypothalamic–pituitary–adrenal axis due to prenatal overexposure to maternal glucocorticoid in mice. 2011. 63(7–8): p. 607–611.
Murphy VE, et al. Reduced 11β-hydroxysteroid dehydrogenase type 2 activity is associated with decreased birth weight centile in pregnancies complicated by asthma. J Clin Endocrinol Metab. 2002;87(4):1660–8.
pubmed: 11932298
Hodyl NA, et al. Sex-specific associations between cortisol and birth weight in pregnancies complicated by asthma are not due to differential glucocorticoid receptor expression.(Clinical report). Thorax. 2010;65(8):677.
pubmed: 20627904
Caldwell KK, Goggin SL, Tyler CR, Allan AM. Prenatal alcohol exposure is associated with altered subcellular distribution of glucocorticoid and mineralocorticoid receptors in the adolescent mouse hippocampal formation. Alcohol Clin Exp Res. 2014;38(2):392–400.
pubmed: 23992407
Lu N, Cidlowski J. The origin and functions of multiple human glucocorticoid receptor isoforms. Ann N Y Acad Sci. 2004;1024(1):102–23.
pubmed: 15265776
Duma D, et al. Sexually dimorphic actions of glucocorticoids provide a link to inflammatory diseases with gender differences in prevalence. Sci Signal. 2010;3(143):ra74–4.
Clifton V, et al. Review: the role of multiple placental glucocorticoid receptor isoforms in adapting to the maternal environment and regulating fetal growth. Placenta. 2017;54:24–9.
pubmed: 28017357
Patra J, Bakker R, Irving H, Jaddoe VWV, Malini S, Rehm J. Dose-response relationship between alcohol consumption before and during pregnancy and the risks of low birthweight, preterm birth and small for gestational age (SGA)-a systematic review and meta-analyses. Bjog. 2011;118(12):1411–21.
pubmed: 21729235 pmcid: 3394156
May PA, Tabachnick B, Hasken JM, Marais AS, de Vries MM, Barnard R, et al. Who is most affected by prenatal alcohol exposure: boys or girls? Drug Alcohol Depend. 2017;177:258–67.
pubmed: 28624747
Saif Z, Hodyl NA, Hobbs E, Tuck AR, Butler MS, Osei-Kumah A, et al. The human placenta expresses multiple glucocorticoid receptor isoforms that are altered by fetal sex, growth restriction and maternal asthma. Placenta. 2014;35(4):260–8.
pubmed: 24559727
Hodge A, Patterson AJ, Brown WJ, Ireland P, Giles G. The Anti Cancer Council of Victoria FFQ: relative validity of nutrient intakes compared with weighed food records in young to middle-aged women in a study of iron supplementation. Aust N Z J Public Health. 2000;24(6):576–83.
pubmed: 11215004
Bagnardi V, Blangiardo M, Vecchia CL, Corrao G. A meta-analysis of alcohol drinking and cancer risk. Br J Cancer. 2001;85(11):1700–5.
pubmed: 11742491 pmcid: 2363992
Taylor, B., et al. Alcohol and hypertension: gender differences in dose–response relationships determined through systematic review and meta-analysis 2009. 104(12): p. 1981–1990.
Wysocka J, Reilly PT, and Herr W. Loss of HCF-1–chromatin association precedes temperature-induced growth arrest of tsBN67 Cells. 2001. 21(11): p. 3820–3829.
Saif Z, Hodyl NA, Stark MJ, Fuller PJ, Cole T, Lu N, et al. Expression of eight glucocorticoid receptor isoforms in the human preterm placenta vary with fetal sex and birthweight. Placenta. 2015;36(7):723–30.
pubmed: 25990415 pmcid: 4830346
Meakin AS, Saif Z, Tuck AR, Clifton VL. Human placental androgen receptor variants: potential regulators of male fetal growth. Placenta. 2019;80:18–26.
pubmed: 31103062
Ray JG, Urquia ML. Risk of stillbirth at extremes of birth weight between 20 to 41 weeks gestation. J Perinatol. 2012;32(11):829–36.
pubmed: 22595964
Weinberg J, Sliwowska JH, Lan N, Hellemans KGC. Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J Neuroendocrinol. 2008;20(4):470–88.
pubmed: 18266938
Cameron CM, et al. Changes in alcohol consumption in pregnant Australian women between 2007 and 2011. 2013. 199(5): p. 355–357.
May PA, et al. Alcohol consumption and other maternal risk factors for fetal alcohol syndrome among three distinct samples of women before, during, and after pregnancy: the risk is relative. Am J Med Genet C: Semin Med Genet. 2004;127c(1):10–20.
Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010;31(Suppl):S33–9.
pubmed: 20004469
Lu N, Cidlowski J. Glucocorticoid receptor isoforms generate transcription specificity. Trends Cell Biol. 2006;16(6):301–7.
pubmed: 16697199
Clifton V. The regulation of placental inflammation by glucocorticoid receptor isoforms. Placenta. 2019;83:e9.
Goedhart G, Vrijkotte TGM, Roseboom TJ, van der Wal MF, Cuijpers P, Bonsel GJ. Maternal cortisol and offspring birthweight: results from a large prospective cohort study. Psychoneuroendocrinology. 2010;35(5):644–52.
pubmed: 19889503
Samarasinghe RA, di Maio R, Volonte D, Galbiati F, Lewis M, Romero G, et al. Nongenomic glucocorticoid receptor action regulates gap junction intercellular communication and neural progenitor cell proliferation. Proc Natl Acad Sci U S A. 2011;108(40):16657–62.
pubmed: 21930911 pmcid: 3189065
Morgan DJ, Poolman TM, Williamson AJK, Wang Z, Clark NR, Ma’ayan A, et al. Glucocorticoid receptor isoforms direct distinct mitochondrial programs to regulate ATP production. Sci Rep. 2016;6:26419.
pubmed: 27226058 pmcid: 4881047
Kadmiel M, Cidlowski JA. Glucocorticoid receptor signaling in health and disease. Trends Pharmacol Sci. 2013;34(9):518–30.
pubmed: 23953592 pmcid: 3951203
Tanaka T, Narazaki M, Kishimoto T. Therapeutic targeting of the interleukin-6 receptor. Ann Rev Pharmacol Toxicol Lett. 2012;52:199–219.
Zhao S, Gu Y, Dong Q, Fan R, Wang Y. Altered Interleukin-6 receptor, IL-6R and gp130, production and expression and decreased SOCS-3 expression in placentas from women with pre-eclampsia. Placenta. 2008;29(12):1024–8.
pubmed: 18986700 pmcid: 3272491
Jaskolka D, Retnakaran R, Zinman B, Kramer CK. Fetal sex and maternal risk of pre-eclampsia/eclampsia: a systematic review and meta-analysis. BJOG. 2017;124(4):553–60.
pubmed: 27315789
Wang JM, Préfontaine GG, Lemieux ME, Pope L, Akimenko MÁ, Haché RJG. Developmental effects of ectopic expression of the glucocorticoid receptor DNA binding domain are alleviated by an amino acid substitution that interferes with homeodomain binding. Mol Cell Biol. 1999;19(10):7106–22.
pubmed: 10490647 pmcid: 84705
O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44(D1):D733–45.
pubmed: 26553804
Edgar R, Domrachev M, and Lash A. Gene expression omnibus: NCBI gene expression and hybridization array data repository. 2002: Nucleic Acids Res.
Pierce DR, West JR. Blood alcohol concentration: a critical factor for producing fetal alcohol effects. Alcohol. 1986;3(4):269–72.
pubmed: 3638973
Jacobson JL, Jacobson SW, Sokol RJ, Ager JW. Relation of maternal age and pattern of pregnancy drinking to functionally significant cognitive deficit in infancy. Alcohol Clin Exp Res. 1998;22(2):345–51.
pubmed: 9581639
Jacobson SW. Specificity of neurobehavioral outcomes associated with prenatal alcohol exposure. Alcohol Clin Exp Res. 1998;22(2):313–20.
pubmed: 9581634
Muggli E, O’Leary C, Forster D, Anderson P, Lewis S, Nagle C, et al. Study protocol: asking questions about alcohol in pregnancy (AQUA): a longitudinal cohort study of fetal effects of low to moderate alcohol exposure. BMC Pregnancy Childbirth. 2014;14:302–2.
Muggli E et al. Alcohol in pregnancy: what questions should we be asking? , D.o. Health, Editor. 2010, Australian Government.
Muggli E, Cook B, O'Leary C, Forster D, Halliday J. Increasing accurate self-report in surveys of pregnancy alcohol use. Midwifery. 2015;31(3):e23–8.
pubmed: 25467595
Virji SK. The relationship between alcohol consumption during pregnancy and infant birthweight. An epidemiologic study. Acta Obstet Gynecol Scand. 1991;70(4–5):303–8.
pubmed: 1746254
Martinson ML, Reichman NE. Socioeconomic inequalities in low birth weight in the United States, the United Kingdom, Canada, and Australia. Am J Public Health. 2016;106(4):748–54.
pubmed: 26794171 pmcid: 26794171

Auteurs

S L Young (SL)

School of Biomedical Sciences, The University of Queensland, St Lucia, Australia.
Child Health Research Centre, The University of Queensland, South Brisbane, Australia.

Z Saif (Z)

Mater Research Institute-University of Queensland, Translational Research Institute, Woolloongabba, Queensland, Australia.

A S Meakin (AS)

Mater Research Institute-University of Queensland, Translational Research Institute, Woolloongabba, Queensland, Australia.

E S McMaster (ES)

School of Chemical and Molecular Biosciences, The University of Queensland, St Lucia, Australia.

N Hayes (N)

Child Health Research Centre, The University of Queensland, South Brisbane, Australia.

L A Gallo (LA)

School of Biomedical Sciences, The University of Queensland, St Lucia, Australia.

N Reid (N)

Child Health Research Centre, The University of Queensland, South Brisbane, Australia.

K M Moritz (KM)

School of Biomedical Sciences, The University of Queensland, St Lucia, Australia. k.moritz@uq.edu.au.
Child Health Research Centre, The University of Queensland, South Brisbane, Australia. k.moritz@uq.edu.au.

V L Clifton (VL)

Mater Research Institute-University of Queensland, Translational Research Institute, Woolloongabba, Queensland, Australia.

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