Sex Dependent Impact of Gestational Stress on Predisposition to Eating Disorders and Metabolic Disease

Overview

Journal Mol Metab

Specialty Cell Biology

Date 2018 Sep 4

PMID 30174229

Citations 6

Authors

Mariana Schroeder

Mira Jakovcevski

Tamar Polacheck

Yonat Drori

Shifra Ben-Dor

Simone Roh

Alon Chen

Affiliations

Soon will be listed here.

Abstract

Objective: Vulnerability to eating disorders (EDs) is broadly assumed to be associated with early life stress. However, a careful examination of the literature shows that susceptibility to EDs may depend on the type, severity and timing of the stressor and the sex of the individual. We aimed at exploring the link between chronic prenatal stress and predisposition to EDs and metabolic disease.

Methods: We used a chronic variable stress protocol during gestation to explore the metabolic response of male and female offspring to food restriction (FR), activity-based anorexia (ABA), binge eating (BE) and exposure to high fat (HF) diet.

Results: Contrary to controls, prenatally stressed (PNS) female offspring showed resistance to ABA and BE and displayed a lower metabolic rate leading to hyperadiposity and obesity on HF diet. Male PNS offspring showed healthy responses to FR and ABA, increased propensity to binge and improved coping with HF compared to controls. We found that long-lasting abnormal responses to metabolic challenge are linked to fetal programming and adult hypothalamic dysregulation in PNS females, resulting from sexually dimorphic adaptations in placental methylation and gene expression.

Conclusions: Our results show that maternal stress may have variable and even opposing effects on ED risk, depending on the ED and the sex of the offspring.

Citing Articles

Maternal preconception stress produces sex-specific effects at the maternal:fetal interface to impact offspring development and phenotypic outcomes†.

Cisse Y, Montgomery K, Zierden H, Hill E, Kane P, Huang W Biol Reprod. 2023; 110(2):339-354.

PMID: 37971364 PMC: 10873277. DOI: 10.1093/biolre/ioad156.

The Placenta-A New Source of Bile Acids during Healthy Pregnancy? First Results of a Gene Expression Study in Humans and Mice.

Ontsouka E, Schroeder M, Ok L, Vaillancourt C, Stroka D, Albrecht C Int J Mol Sci. 2023; 24(11).

PMID: 37298459 PMC: 10253767. DOI: 10.3390/ijms24119511.

The relation between prenatal stress, overweight and obesity in children diagnosed according to BMI and percentage fat tissue.

Bryl E, Hanc T, Szczesniewska P, Dutkiewicz A, Dmitrzak-Weglarz M, Slopien A Eat Weight Disord. 2022; 27(7):2759-2773.

PMID: 35691007 DOI: 10.1007/s40519-022-01416-4.

A Framework for Developing Translationally Relevant Animal Models of Stress-Induced Changes in Eating Behavior.

Francois M, Fernandez-Gayol O, Zeltser L Biol Psychiatry. 2021; 91(10):888-897.

PMID: 34433512 PMC: 8720907. DOI: 10.1016/j.biopsych.2021.06.020.

The role of TET proteins in stress-induced neuroepigenetic and behavioural adaptations.

Dick A, Chen A Neurobiol Stress. 2021; 15:100352.

PMID: 34189192 PMC: 8220100. DOI: 10.1016/j.ynstr.2021.100352.

References

Lager S, Powell T . Regulation of nutrient transport across the placenta. J Pregnancy. 2013; 2012:179827. PMC: 3523549. DOI: 10.1155/2012/179827. View

Rayworth B, Wise L, Harlow B . Childhood abuse and risk of eating disorders in women. Epidemiology. 2004; 15(3):271-8. DOI: 10.1097/01.ede.0000120047.07140.9d. View

Hall J, Smith K, SCHNITZER S, Hanford P . Elevation of activity level in the rat following transition from ad libitum to restricted feeding. J Comp Physiol Psychol. 1953; 46(6):429-33. DOI: 10.1037/h0062565. View

Holtkamp K, Hebebrand J, Herpertz-Dahlmann B . The contribution of anxiety and food restriction on physical activity levels in acute anorexia nervosa. Int J Eat Disord. 2004; 36(2):163-71. DOI: 10.1002/eat.20035. View

Moisiadis V, Matthews S . Glucocorticoids and fetal programming part 1: Outcomes. Nat Rev Endocrinol. 2014; 10(7):391-402. DOI: 10.1038/nrendo.2014.73. View

Waddell B, Wharfe M, Crew R, Mark P . A rhythmic placenta? Circadian variation, clock genes and placental function. Placenta. 2012; 33(7):533-9. DOI: 10.1016/j.placenta.2012.03.008. View

Darnaudery M, Maccari S . Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev. 2008; 57(2):571-85. DOI: 10.1016/j.brainresrev.2007.11.004. View

Entringer S, Wust S, Kumsta R, Layes I, Nelson E, Hellhammer D . Prenatal psychosocial stress exposure is associated with insulin resistance in young adults. Am J Obstet Gynecol. 2008; 199(5):498.e1-7. PMC: 3587039. DOI: 10.1016/j.ajog.2008.03.006. View

Pjetri E, de Haas R, de Jong S, Gelegen C, Oppelaar H, Verhagen L . Identifying predictors of activity based anorexia susceptibility in diverse genetic rodent populations. PLoS One. 2012; 7(11):e50453. PMC: 3511580. DOI: 10.1371/journal.pone.0050453. View

10.

Bianco-Miotto T, Mayne B, Buckberry S, Breen J, Rodriguez Lopez C, Roberts C . Recent progress towards understanding the role of DNA methylation in human placental development. Reproduction. 2016; 152(1):R23-30. PMC: 5064761. DOI: 10.1530/REP-16-0014. View

11.

Corwin R, Buda-Levin A . Behavioral models of binge-type eating. Physiol Behav. 2004; 82(1):123-30. DOI: 10.1016/j.physbeh.2004.04.036. View

12.

Schroeder M, Jakovcevski M, Polacheck T, Lebow M, Drori Y, Engel M . A Methyl-Balanced Diet Prevents CRF-Induced Prenatal Stress-Triggered Predisposition to Binge Eating-like Phenotype. Cell Metab. 2017; 25(6):1269-1281.e6. DOI: 10.1016/j.cmet.2017.05.001. View

13.

Boersma G, Liang N, Lee R, Albertz J, Kastelein A, Moody L . Failure to upregulate Agrp and Orexin in response to activity based anorexia in weight loss vulnerable rats characterized by passive stress coping and prenatal stress experience. Psychoneuroendocrinology. 2016; 67:171-81. PMC: 4808341. DOI: 10.1016/j.psyneuen.2016.02.002. View

14.

Steiger H, Thaler L . Eating disorders, gene-environment interactions and the epigenome: Roles of stress exposures and nutritional status. Physiol Behav. 2016; 162:181-5. DOI: 10.1016/j.physbeh.2016.01.041. View

15.

Bulbul M, Sinen O, Gemici B, Izgut-Uysal V . Opposite effects of central oxytocin and arginine vasopressin on changes in gastric motor function induced by chronic stress. Peptides. 2016; 87:1-11. DOI: 10.1016/j.peptides.2016.11.001. View

16.

Keski-Rahkonen A, Mustelin L . Epidemiology of eating disorders in Europe: prevalence, incidence, comorbidity, course, consequences, and risk factors. Curr Opin Psychiatry. 2016; 29(6):340-5. DOI: 10.1097/YCO.0000000000000278. View

17.

Entringer S, Wadhwa P . Developmental programming of obesity and metabolic dysfunction: role of prenatal stress and stress biology. Nestle Nutr Inst Workshop Ser. 2013; 74:107-20. PMC: 4159714. DOI: 10.1159/000348454. View

18.

Raum W, Swerdloff R . The role of hypothalamic adrenergic receptors in preventing testosterone-induced androgenization in the female rat brain. Endocrinology. 1981; 109(1):273-8. DOI: 10.1210/endo-109-1-273. View

19.

Wu Z, Xu Y, Zhu Y, Sutton A, Zhao R, Lowell B . An obligate role of oxytocin neurons in diet induced energy expenditure. PLoS One. 2012; 7(9):e45167. PMC: 3445456. DOI: 10.1371/journal.pone.0045167. View

20.

Brondani L, Duarte G, Canani L, Crispim D . The presence of at least three alleles of the ADRB3 Trp64Arg (C/T) and UCP1 -3826A/G polymorphisms is associated with protection to overweight/obesity and with higher high-density lipoprotein cholesterol levels in Caucasian-Brazilian patients with.... Metab Syndr Relat Disord. 2013; 12(1):16-24. DOI: 10.1089/met.2013.0077. View