CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval

Jarome, Timothy J.; Ferrara, Nicole C.; Kwapis, Janine L.; Helmstetter, Fred J.

doi:10.1016/j.nlm.2016.01.001

Cited by 112Memory and Neural MechanismsMemory Processes and InfluencesUbiquitin and proteasome pathways

CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval

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Jarome, Timothy J., Ferrara, Nicole C., Kwapis, Janine L., Helmstetter, Fred J.·2016·Neurobiology of Learning and Memory

DOI 10.1016/j.nlm.2016.01.001PMC PMC4754128

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Abstract

Numerous studies have suggested that memories "destabilize" and require de novo protein synthesis in order to reconsolidate following retrieval, but very little is known about how this destabilization process is regulated. Recently, ubiquitin-proteasome mediated protein degradation has been identified as a critical regulator of memory trace destabilization following retrieval, though the specific mechanisms controlling retrieval-induced changes in ubiquitin-proteasome activity remain equivocal. Here, we found that proteasome activity is increased in the amygdala in a CaMKII-dependent manner following the retrieval of a contextual fear memory. We show that in vitro inhibition of CaMKII reversed retrieval-induced increases in proteasome activity. Additionally, in vivo pharmacological blockade of CaMKII abolished increases in proteolytic activity and activity related regulatory phosphorylation in the amygdala following retrieval, suggesting that CaMKII was "upstream" of protein degradation during the memory reconsolidation process. Consistent with this, while inhibiting CaMKII in the amygdala did not impair memory following retrieval, it completely attenuated the memory impairments that resulted from post-retrieval protein synthesis blockade. Collectively, these results suggest that CaMKII controls the initiation of the memory reconsolidation process through regulation of the proteasome.

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PSMC5 serves as a neuronal sensor that dynamically adjusts proteasome activity and localization to spines in response to protein turnover requirements through phosphorylation by CAMKIIα.
“As an ATPase, PSMC5 serves as a neuronal sensor that dynamically adjusts proteasome activity and localization to spines in response to protein turnover requirements through phosphorylation by CAMKIIα15,16.”
From Investigating the neuronal role of the proteasomal ATPase subunit gene PSMC5 in neurodevelopmental proteasomopathies (2025) · cites this paper as [16]
Results §3.2 reports that CaMKII inhibition prevented retrieval-induced increases in proteasome activity and Rpt6 phosphorylation in the amygdala. The paper does not establish that PSMC5 acts as a neuronal sensor, adjusts activity according to protein-turnover requirements, or controls proteasome localization to spines; it also does not specify CaMKIIα as the kinase responsible in that experiment. Page numbers were not available in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
The CaMKII-based mechanism of proteasomal regulation may be essential for memory reconsolidation.
“and that this CaMKII-based mechanism of proteasomal regulation may be essential for memory reconsolidation (Jarome et al., 2016).”
From Altered Phosphorylation of the Proteasome Subunit Rpt6 Has Minimal Impact on Synaptic Plasticity and Learning (2021) · cites this paper as Jarome et al., 2016

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Authors: Jarome, T. J., Ferrara, N. C., Kwapis, J. L., & Helmstetter, F. J.
Affiliations: University of Wisconsin–Milwaukee (US)
Corresponding author: Helmstetter, Fred J.
ORCID: Jarome, Timothy J.
Ferrara, Nicole C.
Kwapis, Janine L.
Helmstetter, Fred J.
Venue: Neurobiology of Learning and Memory
Publisher: Elsevier BV
Published: 2016-02
Volume: 128
Pages: 103-109
ISSN: 1074-7427 (ISSN-L)
DOI: 10.1016/j.nlm.2016.01.001
PMC: PMC4754128
OpenAlex: W2232242747
Cited by: 112
References: 49
Citations by year: 2026: 1 · 2025: 9 · 2024: 6 · 2023: 9 · 2022: 10 · 2021: 21 · 2020: 14 · 2019: 10 · 2018: 16 · 2017: 10 · 2016: 6
FWCI: 8.91
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurobiology of Learning and Memory (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Health (R01 MH069558, F31-MH088125)
American Psychological Foundation
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Keywords: CaMKII, proteasome, memory reconsolidation, memory destabilization, contextual fear memory, amygdala, ubiquitin-proteasome system, protein degradation, memory retrieval
MeSH terms: Memory Consolidation, ATPases Associated with Diverse Cellular Activities, Amygdala, Animals, Conditioning, Classical, Fear, Male, Phosphorylation, Mental Recall, Rats, Long-Evans, Proteasome Endopeptidase Complex, Calcium-Calmodulin-Dependent Protein Kinase Type 2

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CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval

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