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Glucocorticoids and fetal programming part 2: mechanisms

Key Points

  • Transporter proteins and enzymes in the placenta and fetus protect the fetus from exposure to high levels of glucocorticoid; however, expression of these factors changes as a function of gestational age

  • Differences exist in the mechanisms by which synthetic glucocorticoids and endogenous glucocorticoids (that is, cortisol) affect fetal brain development, due to differences in receptor activation

  • Prenatal stress and glucocorticoids can influence the developing epigenome in a number of ways, including modified DNA methylation, histone acetylation and microRNA expression

  • Glucocorticoids probably act via a number of direct and indirect routes to influence the developing epigenome

  • Programmed changes in hypothalamic–pituitary–adrenal function and other endocrine systems following antenatal glucocorticoid exposure probably continue interacting with the epigenome throughout life

  • The latest evidence indicates that transgenerational epigenetic transmission might be partly responsible for the multigenerational effects of synthetic glucocorticoid exposure and maternal stress in pregnancy

Abstract

The lifelong health of an individual is shaped during critical periods of development. The fetus is particularly susceptible to internal and external stimuli, many of which can alter developmental trajectories and subsequent susceptibility to disease. Glucocorticoids are critical in normal development of the fetus, as they are involved in the growth and maturation of many organ systems. The surge in fetal glucocorticoid levels that occurs in most mammalian species over the last few days of pregnancy is an important developmental switch leading to fundamental changes in gene regulation in many organs, including the brain. These changes are important for the transition to postnatal life. Exposure of the fetus to increased levels of glucocorticoids, resulting from maternal stress or treatment with synthetic glucocorticoids, can lead to long-term 'programming' of hypothalamic–pituitary–adrenal function and behaviours. Glucocorticoids act at multiple levels within the fetal brain. Growing evidence indicates that they can exert powerful effects on the epigenome, including on DNA methylation, histone acetylation and microRNA, to influence gene expression. Such influences probably represent a critical component of the 'programming' process, and might be partly responsible for the transgenerational effects of antenatal glucocorticoid exposure on neurologic, cardiovascular and metabolic function.

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Figure 1: The routes by which glucocorticoids can program the HPA axis.
Figure 2: Enzymatic and transport barriers in the placenta and fetal brain.
Figure 3: Potential routes by which glucocorticoids influence the fetal epigenome.

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Acknowledgements

The authors thank Dr Majid Iqbal for the image used in Figure 2b. The authors would like to acknowledge the support of grants from the Canadian Institutes of Health Research (126166) and the Natural Sciences and Engineering Research Council of Canada.

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Moisiadis, V., Matthews, S. Glucocorticoids and fetal programming part 2: mechanisms. Nat Rev Endocrinol 10, 403–411 (2014). https://doi.org/10.1038/nrendo.2014.74

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