The Role of Epigenetic Mechanisms in the Long-term Effects of Early-life Adversity and Mother-infant Relationship on Physiology and Behavior of Offspring in Laboratory Rats and Mice

Overview

Journal Dev Psychobiol

Specialties Pediatrics
Psychiatry
Psychology

Date 2024 Mar 12

PMID 38470450

Authors

Olga V Burenkova

Elena L Grigorenko

Affiliations

Soon will be listed here.

Abstract

Maternal care during the early postnatal period of altricial mammals is a key factor in the survival and adaptation of offspring to environmental conditions. Natural variations in maternal care and experimental manipulations with maternal-child relationships modeling early-life adversity (ELA) in laboratory rats and mice have a strong long-term influence on the physiology and behavior of offspring in rats and mice. This literature review is devoted to the latest research on the role of epigenetic mechanisms in these effects of ELA and mother-infant relationship, with a focus on the regulation of hypothalamic-pituitary-adrenal axis and brain-derived neurotrophic factor. An important part of this review is dedicated to pharmacological interventions and epigenetic editing as tools for studying the causal role of epigenetic mechanisms in the development of physiological and behavioral profiles. A special section of the manuscript will discuss the translational potential of the discussed research.

Citing Articles

Brain Evolution in the Times of the Pandemic and Multimedia.

Castelon Konkiewitz E, Ziff E Eur Neurol. 2024; 87(5-6):261-272.

PMID: 39265548 PMC: 11651333. DOI: 10.1159/000541361.

References

Lindeyer C, Meaney M, Reader S . Early maternal care predicts reliance on social learning about food in adult rats. Dev Psychobiol. 2012; 55(2):168-75. DOI: 10.1002/dev.21009. View

Wondrak G, Jacobson E, Jacobson M . Histone carbonylation in vivo and in vitro. Biochem J. 2000; 351 Pt 3:769-77. PMC: 1221418. View

Hertzman C . Putting the concept of biological embedding in historical perspective. Proc Natl Acad Sci U S A. 2012; 109 Suppl 2:17160-7. PMC: 3477385. DOI: 10.1073/pnas.1202203109. View

Walker C, Perrin M, Vale W, Rivier C . Ontogeny of the stress response in the rat: role of the pituitary and the hypothalamus. Endocrinology. 1986; 118(4):1445-51. DOI: 10.1210/endo-118-4-1445. View

Yoshii A, Constantine-Paton M . Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev Neurobiol. 2010; 70(5):304-22. PMC: 2923204. DOI: 10.1002/dneu.20765. View

Wei L, David A, Duman R, Anisman H, Kaffman A . Early life stress increases anxiety-like behavior in Balb c mice despite a compensatory increase in levels of postnatal maternal care. Horm Behav. 2010; 57(4-5):396-404. PMC: 2849915. DOI: 10.1016/j.yhbeh.2010.01.007. View

Boyes J, Bird A . Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein. EMBO J. 1992; 11(1):327-33. PMC: 556453. DOI: 10.1002/j.1460-2075.1992.tb05055.x. View

Zhu Y, Wang Y, Yao R, Hao T, Cao J, Huang H . Enhanced neuroinflammation mediated by DNA methylation of the glucocorticoid receptor triggers cognitive dysfunction after sevoflurane anesthesia in adult rats subjected to maternal separation during the neonatal period. J Neuroinflammation. 2017; 14(1):6. PMC: 5234142. DOI: 10.1186/s12974-016-0782-5. View

Gugliucci A . Advanced glycation of rat liver histone octamers: an in vitro study. Biochem Biophys Res Commun. 1994; 203(1):588-93. DOI: 10.1006/bbrc.1994.2223. View

10.

Vitolo J, Thiriet C, HAYES J . The H3-H4 N-terminal tail domains are the primary mediators of transcription factor IIIA access to 5S DNA within a nucleosome. Mol Cell Biol. 2000; 20(6):2167-75. PMC: 110833. DOI: 10.1128/MCB.20.6.2167-2175.2000. View

11.

Sun Z, Allis C . Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature. 2002; 418(6893):104-8. DOI: 10.1038/nature00883. View

12.

Ladd C, Huot R, Thrivikraman K, Nemeroff C, Plotsky P . Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol Psychiatry. 2004; 55(4):367-75. DOI: 10.1016/j.biopsych.2003.10.007. View

13.

Lee D, HAYES J, Pruss D, Wolffe A . A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993; 72(1):73-84. DOI: 10.1016/0092-8674(93)90051-q. View

14.

Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky P, Meaney M . Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A. 1998; 95(9):5335-40. PMC: 20261. DOI: 10.1073/pnas.95.9.5335. View

15.

Heijmans B, Tobi E, Stein A, Putter H, Blauw G, Susser E . Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008; 105(44):17046-9. PMC: 2579375. DOI: 10.1073/pnas.0806560105. View

16.

Smotherman W, Brown C, Levine S . Maternal responsiveness following differential pup treatment and mother-pup interactions. Horm Behav. 1977; 8(2):242-53. DOI: 10.1016/0018-506x(77)90041-1. View

17.

Stanley J, Griffin J, Zempleni J . Biotinylation of histones in human cells. Effects of cell proliferation. Eur J Biochem. 2001; 268(20):5424-9. DOI: 10.1046/j.0014-2956.2001.02481.x. View

18.

Li E . Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet. 2002; 3(9):662-73. DOI: 10.1038/nrg887. View

19.

Roth T, Lubin F, Funk A, Sweatt J . Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry. 2009; 65(9):760-9. PMC: 3056389. DOI: 10.1016/j.biopsych.2008.11.028. View

20.

McKay M, Kilmartin L, Meagher A, Cannon M, Healy C, Clarke M . A revised and extended systematic review and meta-analysis of the relationship between childhood adversity and adult psychiatric disorder. J Psychiatr Res. 2022; 156:268-283. DOI: 10.1016/j.jpsychires.2022.10.015. View