Protein phosphatase 2a and glycogen synthase kinase 3 signaling modulate prepulse inhibition of the acoustic startle response by altering cortical M-type potassium channel activity
Open accessAbstract
There is considerable interest in the regulation of sensorimotor gating, since deficits in this process could play a critical role in the symptoms of schizophrenia and other psychiatric disorders. Sensorimotor gating is often studied in humans and rodents using the prepulse inhibition of the acoustic startle response (PPI) model, in which an acoustic prepulse suppresses behavioral output to a startle-inducing stimulus. However, the molecular and neural mechanisms underlying PPI are poorly understood. Here, we show that a regulatory pathway involving protein phosphatase 2A (PP2A), glycogen synthase kinase 3 beta (GSK3beta), and their downstream target, the M-type potassium channel, regulates PPI. Mice (Mus musculus) carrying a hypomorphic allele of Ppp2r5delta, encoding a regulatory subunit of PP2A, show attenuated PPI. This PPP2R5delta reduction increases the phosphorylation of GSK3beta at serine 9, which inactivates GSK3beta, indicating that PPP2R5delta positively regulates GSK3beta activity in the brain. Consistently, genetic and pharmacological manipulations that reduce GSK3beta function attenuate PPI. The M-type potassium channel subunit, KCNQ2, is a putative GSK3beta substrate. Genetic reduction of Kcnq2 also reduces PPI, as does systemic inhibition of M-channels with linopirdine. Importantly, both the GSK3 inhibitor 3-(2,4-dichlorophenyl)-4-(1-methyl-1H-indol-3-yl)1H-pyrrole-2,5-dione (SB216763) and linopirdine reduce PPI when directly infused into the medial prefrontal cortex (mPFC). Whole-cell electrophysiological recordings of mPFC neurons show that SB216763 and linopirdine have similar effects on firing, and GSK3 inhibition occludes the effects of M-channel inhibition. These data support a previously uncharacterized mechanism by which PP2A/GSK3beta signaling regulates M-type potassium channel activity in the mPFC to modulate sensorimotor gating.
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Mice heterozygous for a hypomorphic Ppp2r5d allele had approximately 50% reduction of B56δ protein in total brain lysates.
“mice, heterozygous for a hypomorphic Ppp2r5d allele, and showing a ~50% reduction of B56δ protein levels in total brain lysates [57].”
From Physiologic functions of PP2A: Lessons from genetically modified mice (2019) · cites this paper as [57]
These mice showed weakened prepulse inhibition.
“These animals showed a weakened prepulse inhibition (PPI)”
From Physiologic functions of PP2A: Lessons from genetically modified mice (2019) · cites this paper as [57]
Increased acoustic startle response in B56δ knockout mice correlated with GSK-3β Ser9 hyperphosphorylation and decreased phosphorylation of KCNQ2.
“The increased acoustic startle response in the B56δ KO mice correlated with GSK-3β hyperphosphorylation (Ser9), and decreased phosphorylation of the presumed GSK-3β substrate, KCNQ2, an M-type potassium channel protein [57].”
From Physiologic functions of PP2A: Lessons from genetically modified mice (2019) · cites this paper as [57]
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- Authors
- Kapfhamer, D., Berger, K. H., Hopf, F. W., Seif, T., Kharazia, V., Bonci, A., & Heberlein, U.
- Affiliations
- Ernest Gallo Clinic and Research Center (US)
- University of California, San Francisco (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-06-30
- Volume
- 30
- Issue
- 26
- Pages
- 8830-8840
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3842471
- OpenAlex
- W2014409883
- Cited by
- 71
- References
- 92
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 2 · 2022: 6 · 2021: 7 · 2020: 9 · 2019: 6 · 2018: 4 · 2017: 5 · 2016: 2 · 2015: 5 · 2014: 4 · 2013: 2 · 2012: 8
- FWCI
- 3.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health
- University of California, San Francisco
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- prepulse inhibition, acoustic startle response, sensorimotor gating, protein phosphatase 2A, glycogen synthase kinase-3β, M-type potassium channels, KCNQ2, medial prefrontal cortex, linopirdine, SB216763, schizophrenia
- MeSH terms
- Glycogen Synthase Kinase 3 beta, Amino Acid Sequence, Animals, Auditory Perception, Brain, Inhibition, Psychological, Mice, Inbred C57BL, Mice, Transgenic, Models, Neurological, Neurons, Phosphorylation, Reflex, Startle, Potassium Channels, Signal Transduction, Prefrontal Cortex, Glycogen Synthase Kinase 3, Mice, KCNQ2 Potassium Channel, Protein Phosphatase 2
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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