Display options
Cite
Dudek KA, Kaufmann FN, Lavoie O, et al. Central and peripheral stress-induced epigenetic mechanisms of resilience. Curr Opin Psychiatry. 2021;34(1):1-9doi: 10.1097/YCO.0000000000000664.
Dudek, K. A., Kaufmann, F. N., Lavoie, O., & Menard, C. (2021). Central and peripheral stress-induced epigenetic mechanisms of resilience. Current opinion in psychiatry, 34(1), 1-9. https://doi.org/10.1097/YCO.0000000000000664
Dudek, Katarzyna Anna, et al. "Central and peripheral stress-induced epigenetic mechanisms of resilience." Current opinion in psychiatry vol. 34,1 (2021): 1-9. doi: https://doi.org/10.1097/YCO.0000000000000664
Dudek KA, Kaufmann FN, Lavoie O, Menard C. Central and peripheral stress-induced epigenetic mechanisms of resilience. Curr Opin Psychiatry. 2021 Jan;34(1):1-9. doi: 10.1097/YCO.0000000000000664. PMID: 33141775.
Copy Download .nbib Format: NLM
Share it on

Curr Opin Psychiatry. 2021 Jan;34(1):1-9. doi: 10.1097/YCO.0000000000000664.

Central and peripheral stress-induced epigenetic mechanisms of resilience.

Current opinion in psychiatry

Katarzyna Anna Dudek, Fernanda Neutzling Kaufmann, Olivier Lavoie, Caroline Menard

Affiliations

  1. Department of Psychiatry and Neuroscience, Faculty of Medicine and CERVO Brain Research Center, Université Laval, Quebec City, Canada.

PMID: 33141775 DOI: 10.1097/YCO.0000000000000664

Abstract

PURPOSE OF REVIEW: Resilience is an adaptation process presented by an individual despite facing adversities. Epigenetic changes, such as histone acetylation/methylation and DNA methylation, have been demonstrated to mediate stress response. In this review, we summarize recent findings on epigenetic mechanisms contributing to stress resilience.

RECENT FINDINGS: Epigenetic modifications of genes involved in synaptic plasticity, endocrine, immune, and vascular systems are linked to resilience. For instance, increased DNA methylation of the nonneuronal growth factor Gdnf in specific brain regions promotes stress resilience. Additionally, high DNA methylation at the glucocorticoid receptor gene was associated with resilience in both rodents and humans. At the immune level, chronic stress induces increased DNA methylation at IL6 gene, a mediator of stress vulnerability. Moreover, epigenetic adaptations of the blood--brain barrier have been recently associated with stress resilience, which could lead to innovative therapeutic approaches to treat depression.

SUMMARY: Identification of both central and peripheral epigenetic changes promoting stress resilience represent promising novel targets in the development of preventive and personalized medicine. Nevertheless, more research is needed to establish sex specific differences and to identify novel epigenetic mechanisms, such as serotonylation and dopaminylation, that hold great promises for the field of psychiatry.

References

  1. Radley JJ, Kabbaj M, Jacobson L, et al. Stress risk factors and stress-related pathology: neuroplasticity, epigenetics and endophenotypes. Stress 2011; 14:481–497. - PubMed
  2. APA. Building your resilience. 2013; USA: American Psychological Association, Available at https://www.apa.org/topics/resilience. (Accessed on 9 June 2020). - PubMed
  3. Cathomas F, Murrough JW, Nestler EJ, et al. Neurobiology of resilience: interface between mind and body. Biol Psychiatry 2019; 86:410–420. - PubMed
  4. Gottschalk MG, Domschke K, Schiele MA. Epigenetics underlying susceptibility and resilience relating to daily life stress, work stress, and socioeconomic status. Front Psychiatry 2020; 11:163. - PubMed
  5. Peña CJ, Nestler EJ. Progress in epigenetics of depression. Prog Mol Biol Transl Sci 2018; 157:41–66. - PubMed
  6. Vialou V, Feng J, Robison AJ, Nestler EJ. Epigenetic mechanisms of depression and antidepressant action. Annu Rev Pharmacol Toxicol 2013; 53:59–87. - PubMed
  7. Borrelli E, Nestler EJ, Allis CD, Sassone-Corsi P. Decoding the epigenetic language of neuronal plasticity. Neuron 2008; 60:961–974. - PubMed
  8. Jiang S, Postovit L, Cattaneo A, et al. Epigenetic modifications in stress response genes associated with childhood trauma. Front Psychiatry 2019; 10:808. - PubMed
  9. Liu W, Ge T, Leng Y, et al. The role of neural plasticity in depression: from hippocampus to prefrontal cortex. Neural Plast 2017; 2017:6871089. - PubMed
  10. Duman RS, Deyama S, Fogaça MV. Role of BDNF in the pathophysiology and treatment of depression: activity-dependent effects distinguish rapid-acting antidepressants. Eur J Neurosci 2019; [Epub ahead of print]. - PubMed
  11. Tsybko AS, Ilchibaeva TV, Popova NK. Role of glial cell line-derived neurotrophic factor in the pathogenesis and treatment of mood disorders. Rev Neurosci 2017; 28:219–233. - PubMed
  12. Vialou V, Maze I, Renthal W, et al. Serum response factor promotes resilience to chronic social stress through the induction of ΔFosB. J Neurosci 2010; 30:14585–14592. - PubMed
  13. Golden SA, Covington HE III, Berton O, Russo SJ. A standardized protocol for repeated social defeat stress in mice. Nat Protoc 2011; 6:1183–1191. - PubMed
  14. Uchida S, Yamagata H, Seki T, Watanabe Y. Epigenetic mechanisms of major depression: targeting neuronal plasticity. Psychiatry Clin Neurosci 2018; 72:212–227. - PubMed
  15. Uchida S, Hara K, Kobayashi A, et al. Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 2011; 69:359–372. - PubMed
  16. Ménard C, Hodes GE, Russo SJ. Pathogenesis of depression: insights from human and rodent studies. Neuroscience 2016; 321:138–162. - PubMed
  17. Hamilton PJ, Burek DJ, Lombroso SI, et al. Cell-type-specific epigenetic editing at the Fosb gene controls susceptibility to social defeat stress. Neuropsychopharmacology 2018; 43:272–284. - PubMed
  18. Peña CJ, Kronman HG, Walker DM, et al. Early life stress confers lifelong stress susceptibility in mice via ventral tegmental area OTX2. Science 2017; 356:1185–1188. - PubMed
  19. Kaufman J, Wymbs NF, Montalvo-Ortiz JL, et al. Methylation in OTX2 and related genes, maltreatment, and depression in children. Neuropsychopharmacology 2018; 43:2204–2211. - PubMed
  20. Juruena MF. Early-life stress and HPA axis trigger recurrent adulthood depression. Epilepsy Behav 2014; 38:148–159. - PubMed
  21. Champagne FA. Early environments, glucocorticoid receptors, and behavioral epigenetics. Behav Neurosci 2013; 127:628–636. - PubMed
  22. Palma-Gudiel H, Córdova-Palomera A, Eixarch E, et al. Maternal psychosocial stress during pregnancy alters the epigenetic signature of the glucocorticoid receptor gene promoter in their offspring: a meta-analysis. Epigenetics 2015; 10:893–902. - PubMed
  23. Folger AT, Ding L, Ji H, et al. Neonatal NR3C1 methylation and social-emotional development at 6 and 18 months of age. Front Behav Neurosci 2019; 13:14. - PubMed
  24. Pan-Vazquez A, Rye N, Ameri M, et al. Impact of voluntary exercise and housing conditions on hippocampal glucocorticoid receptor, miR-124 and anxiety. Mol Brain 2015; 8:1–12. - PubMed
  25. Serpeloni F, Radtke KM, Hecker T, et al. Does prenatal stress shape postnatal resilience?–an epigenome-wide study on violence and mental health in humans. Front Genet 2019; 10:269. - PubMed
  26. Matosin N, Halldorsdottir T, Binder EB. Understanding the molecular mechanisms underpinning gene by environment interactions in psychiatric disorders: the FKBP5 model. Biol Psychiatry 2018; 83:821–830. - PubMed
  27. Hartmann J, Wagner KV, Liebl C, et al. The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology 2012; 62:332–339. - PubMed
  28. Sabbagh JJ, O’Leary JC 3rd, Blair LJ, et al. Age-associated epigenetic upregulation of the FKBP5 gene selectively impairs stress resiliency. PLoS One 2014; 9:e107241. - PubMed
  29. StatPearls Publishing, Sekhon S, Patel J, Sapra A. Late onset depression. StatPearls [Internet] 2019. - PubMed
  30. Dudek KA, Dion-Albert L, Kaufmann FN, et al. Neurobiology of resilience in depression: immune and vascular insights from human and animal studies. Eur J Neurosci 2019; [Epub ahead of print]. - PubMed
  31. Menard C, Pfau ML, Hodes GE, et al. Social stress induces neurovascular pathology promoting depression. Nat Neurosci 2017; 20:1752–1760. - PubMed
  32. Hodes GE, Pfau ML, Leboeuf M, et al. Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc Natl Acad Sci U S A 2014; 111:16136–16141. - PubMed
  33. Wang J, Hodes GE, Zhang H, et al. Epigenetic modulation of inflammation and synaptic plasticity promotes resilience against stress in mice. Nat Commun 2018; 9:477. - PubMed
  34. Hodes GE, Kana V, Menard C, et al. Neuroimmune mechanisms of depression. Nat Neurosci 2015; 18:1386–1393. - PubMed
  35. Dudek KA, Dion-Albert L, Lebel M, et al. Molecular adaptations of the blood–brain barrier promote stress resilience vs. depression. Proc Natl Acad Sci U S A 2020; 117:3326–3336. - PubMed
  36. Mena F, Benoit L. Molecular programs underlying differences in the expression of mood disorders in males and females. Brain Res 2019; 1719:89–103. - PubMed
  37. Heller EA, Cates HM, Peña CJ, et al. Locus-specific epigenetic remodeling controls addiction- and depression-related behaviors. Nature Neurosci 2014; 17:1720–1727. - PubMed
  38. Yin YY, Teague CD, Nestler EJ. In vivo locus-specific editing of the neuroepigenome. Nat Rev Neurosci 2020; [Epub ahead of print]. - PubMed
  39. Farrelly LA, Thompson RE, Zhao S, et al. Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me3. Nature 2019; 567:535–539. - PubMed
  40. Lepack AE, Werner CT, Stewart AF, et al. Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking. Science 2020; 368:197–201. - PubMed
  41. Messaoudi M, Violle N, Bisson JF, et al. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes 2011; 2:256–261. - PubMed
  42. Zhang K, Fujita Y, Chang L, et al. Abnormal composition of gut microbiota is associated with resilience versus susceptibility to inescapable electric stress. Transl Psychiatry 2019; 9:231. - PubMed
  43. Markowiak-Kopeć P, Śliżewska K. The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients 2020; 12:1107. - PubMed
  44. Sampson TR, Mazmanian SK. Control of brain development, function, and behavior by the microbiome. Cell Host Microbe 2015; 17:565–576. - PubMed
  45. Farzi A, Fröhlich EE, Holzer P. Gut microbiota and the neuroendocrine system. Neurotherapeutics 2018; 15:5–22. - PubMed
  46. Valles-Colomer M, Falony G, Darzi Y, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol 2019; 4:623–632. - PubMed
  47. Jiang H, Ling Z, Zhang Y, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun 2015; 48:186–194. - PubMed
  48. Schroeder FA, Lin CL, Crusio WE, Akbarian S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 2007; 62:55–64. - PubMed
  49. Sun J, Wang F, Hong G, et al. Antidepressant-like effects of sodium butyrate and its possible mechanisms of action in mice exposed to chronic unpredictable mild stress. Neurosci Lett 2016; 618:159–166. - PubMed

MeSH terms

Publication Types