Bidirectional rescue of extreme genetic predispositions to anxiety: impact of CRH receptor 1 as epigenetic plasticity gene in the amygdala
Open accessAbstract
The continuum of physiological anxiety up to psychopathology is not merely dependent on genes, but is orchestrated by the interplay of genetic predisposition, gene x environment and epigenetic interactions. Accordingly, inborn anxiety is considered a polygenic, multifactorial trait, likely to be shaped by environmentally driven plasticity at the genomic level. We here took advantage of the extreme genetic predisposition of the selectively bred high (HAB) and low anxiety (LAB) mouse model exhibiting high vs low anxiety-related behavior and tested whether and how beneficial (enriched environment) vs detrimental (chronic mild stress) environmental manipulations are capable of rescuing phenotypes from both ends of the anxiety continuum. We provide evidence that (i) even inborn and seemingly rigid behavioral and neuroendocrine phenotypes can bidirectionally be rescued by appropriate environmental stimuli, (ii) corticotropin-releasing hormone receptor 1 (Crhr1), critically involved in trait anxiety, shows bidirectional alterations in its expression in the basolateral amygdala (BLA) upon environmental stimulation, (iii) these alterations are linked to an increased methylation status of its promoter and, finally, (iv) binding of the transcription factor Yin Yang 1 (YY1) to the Crhr1 promoter contributes to its gene expression in a methylation-sensitive manner. Thus, Crhr1 in the BLA is critically involved as plasticity gene in the bidirectional epigenetic rescue of extremes in trait anxiety.
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Exposure of LAB mice to chronic mild stress shifted CRHR1 expression levels to that of anxious HAB mice.
“Additionally, the exposure of LAB mice to chronic mild stress (CMS) shifted CRHR1 expression levels to that of anxious HAB mice (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
The Results section, “Crhr1 in the amygdala modulates anxiety-related behavior” (page unavailable), reports that chronic mild stress significantly increased Crhr1 mRNA levels in LAB mice and that untreated HAB mice had higher levels than untreated LAB mice. It does not establish that stress raised LAB expression to the same level as in HAB mice. (LLM, conf=0.84)
Experimental — accuracy not yet measuredExternal stimuli such as EE and CMS are able to alter gene methylation states and subsequently induce changes in anxiety-like behaviors via chromatin remodeling protein recruitment.
“Identification of this pattern of differential methylation of the Crhr1 gene highlights brain plasticity, such that external stimuli, such as EE and CMS, are able to alter gene methylation states and subsequently induce changes in anxiety-like behaviors via chromatin remodeling protein recruitment (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
The Results sections on trait anxiety and CpG1 methylation report that EE and CMS changed anxiety-like behavior and increased Crhr1 promoter methylation in different mouse lines (page numbers unavailable). The YY1 Results and Discussion describe methylation-sensitive binding of a transcription factor, not recruitment of chromatin-remodeling proteins as the mechanism causing the behavioral changes. (LLM, conf=0.88)
Experimental — accuracy not yet measuredYY1 was found to bind near CpG1 of the promoter of Crhr1 in response to the methylation of CpG1.
“YY1 was found to bind near CpG1 of the promoter of Crhr1 in response to the methylation of CpG1.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
The Results section, ‘Transcription factor YY1 regulates Crhr1 expression in a methylation-dependent manner,’ confirms that YY1 binds adjacent to the Crhr1 promoter’s differentially methylated region. But its EMSA results show that methylation of CpG1 decreased YY1 binding, rather than prompting it to bind. (LLM, conf=0.88)
Experimental — accuracy not yet measuredHypermethylation of CpG1 in the Crhr promoter can increase or decrease anxiety-like behaviors.
“In the study by Sotnikov et al. (2014), hypermethylation of CpG1 in the Crhr promoter can increase, or decrease, anxiety-like behaviors, emphasizing that gene expression regulation is incredibly complex as other epigenetic modifications may cooperate to regulate gene expression, which we will see below.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
The Results report that both environmental enrichment in high-anxiety mice and chronic mild stress in low-anxiety mice increased Crhr1 CpG1 methylation, while the two treatments changed anxiety-like behavior in opposite directions. The Discussion proposes methylation-dependent regulation involving YY1, but the paper does not establish that CpG1 hypermethylation itself caused either behavioral change. (LLM, conf=0.82)
Experimental — accuracy not yet measuredEE in HAB mice and CMS in LAB mice both caused an increase in methylation at CpG1 upstream of the Crhr1 promoter in the amygdala.
“Interestingly, EE in HAB mice and CMS in LAB mice both caused an increase in methylation at CpG1 upstream of the Crhr1 promoter in the amygdala.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
YY1 was reported to be bidirectionally expressed between HAB-EE and LAB-CMS mice.
“the researchers honed in on a transcription factor Ying-Yang1 (YY1), which was reported to be bidirectionally expressed between HAB-EE and LAB-CMS mice (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
Exposure of HAB mice to an enriched environment reverses CRHR1 overexpression.
“exposure of HAB mice to an enriched environment (EE) positively stimulates the animal, reversing this expression.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
HAB mice display an overexpression of CRHR1 in the basal amygdala compared with LAB mice.
“researchers reported that not only do HAB mice display an overexpression of CRHR1 (CRH receptor) in the basal amygdala compared with LAB mice, but that exposure of HAB mice to an enriched environment (EE) positively stimulates the animal, reversing this expression.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
Increased methylation at CpG1 of Crhr1 in LAB-CMS anxiety-exhibiting mice does not repress CRHR expression when YY1 expression is increased.
“suggesting that increased methylation at CpG1 of Crhr1 in LAB-CMS anxiety-exhibiting mice does not repress CRHR expression when YY1 expression is increased (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
An increase in YY1 in LAB-CMS with an increase in methylation correlated with the upregulation of Crhr1 expression.
“An increase in YY1 in LAB-CMS with an increase in methylation, correlated with the upregulation of Crhr1 expression (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
Overexpression of YY1 in mouse neuroblastoma cells (N2a) was shown to enhance CRHR expression by increased promoter activity.
“Overexpression of YY1 in mouse neuroblastoma cells (N2a) was shown to enhance CRHR expression by increased promoter activity, suggesting that increased methylation at CpG1 of Crhr1 in LAB-CMS anxiety-exhibiting mice does not repress CRHR expression when YY1 expression is increased (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
In HAB-EE mice, lower levels of YY1 expression coupled with an increase in methylation correlated with downregulation of Crhr1 expression.
“In HAB-EE mice, lower levels of YY1 expression coupled with an increase in methylation correlated with a downregulation of Crhr1 expression.”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
Use of a CRHR antagonist in HAB mice had an anxiolytic effect.
“The use of a CRHR antagonist in HAB mice had an anxiolytic effect, further supporting the role of overexpressed Crhr in various brain regions in observable anxiety phenotypes (Sotnikov et al., 2014).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Sotnikov et al., 2014
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Wahl, K. (2023) · Springer eBooks · doi:10.1007/978-3-031-23577-1_3
From systems thinking to P4 medicine
Hedayat, K. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-22326-6.00022-5
- Authors
- Sotnikov, S. V., Markt, P. O., Malik, V, Chekmareva, N. Y., Naik, R. R., Sah, A., Singewald, N., Holsboer, F., Czibere, L., & Landgraf, R.
- Affiliations
- Sechenov University (RU)
- Max Planck Institute of Psychiatry (DE)
- Universität Innsbruck (AT)
- Corresponding author
- Sotnikov, S V
- Markt, P O
- Venue
- Translational Psychiatry
- Published
- 2014-02-11
- Volume
- 4
- Issue
- 2
- Pages
- e359-e359
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC3944631
- OpenAlex
- W2026608133
- Cited by
- 49
- References
- 27
- Citations by year
- 2024: 2 · 2023: 1 · 2022: 5 · 2021: 2 · 2020: 3 · 2019: 4 · 2018: 8 · 2017: 7 · 2016: 7 · 2015: 4 · 2014: 5 · 2013: 1
- FWCI
- 3.76
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (unspecified)
- Locations
- Translational Psychiatry (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion, cc-by-nc-nd)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- anxiety, genetic susceptibility, corticotropin-releasing hormone receptor 1, CRHR1, epigenetic plasticity, DNA methylation, promoter methylation, YY1, transcription factor binding, basolateral amygdala, environmental enrichment, chronic mild stress, gene-environment interaction, trait anxiety, neuroendocrine stress response
- MeSH terms
- CRF Receptor, Type 1, Animals, Anxiety, Environment, Mice, Inbred Strains, Gene Expression, Receptors, Corticotropin-Releasing Hormone, Genetic Predisposition to Disease, Epigenesis, Genetic, YY1 Transcription Factor, Mice, Gene-Environment Interaction, Basolateral Nuclear Complex
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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