A Novel Role of the WNT-Dishevelled-GSK3 Signaling Cascade in the Mouse Nucleus Accumbens in a Social Defeat Model of Depression
Open accessAbstract
Based on earlier gene expression and chromatin array data, we identified the protein, dishevelled (DVL)-2, as being regulated in the nucleus accumbens (NAc), a key brain reward region, in the mouse social defeat model of depression. Here, we validate these findings by showing that DVL2 mRNA and protein levels are downregulated in NAc of mice susceptible to social defeat stress, effects not seen in resilient mice. Other DVL isoforms, DVL1 and DVL3, show similar patterns of regulation. Downregulation of DVL was also demonstrated in the NAc of depressed humans examined postmortem. Interestingly, several members of the WNT (Wingless)-DVL signaling cascade, including phospho-GSK3β (glycogen synthase kinase-3β), also show significant downregulation in the NAc of susceptible, but not resilient, mice, demonstrating concerted regulation of this pathway in the NAc due to social defeat stress. By using viral-mediated gene transfer to overexpress a dominant-negative mutant of DVL in NAc, or by using a pharmacological inhibitor of DVL administered into this brain region, we show that blockade of DVL function renders mice more susceptible to social defeat stress and promotes depression-like behavior in other assays. Similar prodepression-like effects were induced upon overexpressing GSK3β in the NAc, while overexpressing a dominant-negative mutant of GSK3β promoted resilience to social defeat stress. These findings are consistent with the knowledge that downregulation of DVL and phospho-GSK3β reflects an increase in GSK3β activity. These studies reveal a novel role for the DVL-GSK3β signaling pathway, acting within the brain's reward circuitry, in regulating susceptibility to chronic stress.
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DVL1 is markedly downregulated in the nucleus accumbens of people with depression.
“Disheveled (DVL1) activity inhibition in the WNT-DVL-β-catenin signaling cascade promotes susceptibility to CSDS and DVL1 is found to be significantly downregulated in the NAc of human depressed patients.”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [91]
Pharmacological and dominant-negative inhibition of GSK3β increases resilience to chronic social defeat stress.
“Comparatively, pharmacological and dominant negative activity inhibition of the downstream inhibition target of DVL1, GSK3β, promotes resilience to CSDS (91).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [91]
Inhibiting DVL1 activity in the WNT-DVL-β-catenin cascade increases susceptibility to chronic social defeat stress.
“Disheveled (DVL1) activity inhibition in the WNT-DVL-β-catenin signaling cascade promotes susceptibility to CSDS and DVL1 is found to be significantly downregulated in the NAc of human depressed patients.”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [91]
Examples of resilience-associated molecular changes include ΔFosB, SRF, HDAC2, and the WNT-DVL-GSK3β signaling cascade.
“Examples include ΔFosB and SRF, discussed above, as well as HDAC2 (histone deacetylase–2) and the WNT (wingless)–DVL (disheveled)–GSK3β (glycogen synthase kinase–3β) signaling cascade71, 72, 94”
From Neurobiology of resilience (2012) · cites this paper as [94]
GSK3β inhibition promotes CSDS-resilience.
“DVL is downregulated in the NAc of postmortem MDD patients and GSK3β inhibition promotes CSDS-resilience [126].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [126]
DVL is downregulated in the NAc of postmortem MDD patients.
“DVL is downregulated in the NAc of postmortem MDD patients and GSK3β inhibition promotes CSDS-resilience [126].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [126]
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- Authors
- Wilkinson, M. B., Dias, C., Magida, J., Mazei-Robison, M., Lobo, M., Kennedy, P., Dietz, D., Covington, H., Russo, S., Neve, R., Ghose, S., Tamminga, C., & Nestler, E. J.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Duke University (US)
- Massachusetts Institute of Technology (US)
- The University of Texas Southwestern Medical Center (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-06-22
- Volume
- 31
- Issue
- 25
- Pages
- 9084-9092
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3133937
- OpenAlex
- W2093765498
- Cited by
- 170
- References
- 39
- Citations by year
- 2026: 3 · 2025: 10 · 2024: 6 · 2023: 6 · 2022: 10 · 2021: 15 · 2020: 13 · 2019: 12 · 2018: 10 · 2017: 6 · 2016: 16 · 2015: 9 · 2014: 20 · 2013: 5 · 2012: 23
- FWCI
- 12.65
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Institute of Mental Health (R01MH051399, P50MH066172)
- Topics
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- Wnt signaling, Dishevelled, GSK3β, nucleus accumbens, social defeat stress, depression, resilience, brain reward system, gene expression regulation
- MeSH terms
- Glycogen Synthase Kinase 3 beta, Dishevelled Proteins, Animals, Depression, Disease Models, Animal, Dominance-Subordination, Humans, Male, Mice, Inbred C57BL, Nucleus Accumbens, Phosphoproteins, Stress, Psychological, Signal Transduction, Glycogen Synthase Kinase 3, Adaptor Proteins, Signal Transducing, Wnt Proteins, Mice
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