Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation
Abstract Reconsolidation has been considered a process in which a consolidated memory is turned into a labile stage. Within the reconsolidation window, the labile memory can be either erased or strengthened. Manipulating acid-sensing ion channels (ASICs) in the amygdala via carbon dioxide (CO2) inha...
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| Format: | Article |
| Language: | English |
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BMC
2021-05-01
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| Series: | Molecular Brain |
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| Online Access: | https://doi.org/10.1186/s13041-021-00786-7 |
| _version_ | 1818624389780865024 |
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| author | Boren Lin Khaled Alganem Sinead M. O’Donovan Zhen Jin FarzanehSadat Naghavi Olivia A. Miller Tyler C. Ortyl Ye Chun Ruan Robert E. McCullumsmith Jianyang Du |
| author_facet | Boren Lin Khaled Alganem Sinead M. O’Donovan Zhen Jin FarzanehSadat Naghavi Olivia A. Miller Tyler C. Ortyl Ye Chun Ruan Robert E. McCullumsmith Jianyang Du |
| author_sort | Boren Lin |
| collection | DOAJ |
| description | Abstract Reconsolidation has been considered a process in which a consolidated memory is turned into a labile stage. Within the reconsolidation window, the labile memory can be either erased or strengthened. Manipulating acid-sensing ion channels (ASICs) in the amygdala via carbon dioxide (CO2) inhalation enhances memory retrieval and its lability within the reconsolidation window. Moreover, pairing CO2 inhalation with retrieval bears the reactivation of the memory trace and enhances the synaptic exchange of the calcium-impermeable AMPA receptors to calcium-permeable AMPA receptors. Our patch-clamp data suggest that the exchange of the AMPA receptors depends on the ubiquitin-proteasome system (UPS), via protein degradation. Ziram (50 µM), a ubiquitination inhibitor, reduces the turnover of the AMPA receptors. CO2 inhalation with retrieval boosts the ubiquitination without altering the proteasome activity. Several calcium-dependent kinases potentially involved in the CO2-inhalation regulated memory liability were identified using the Kinome assay. These results suggest that the UPS plays a key role in regulating the turnover of AMPA receptors during CO2 inhalation. |
| first_indexed | 2024-12-16T18:56:11Z |
| format | Article |
| id | doaj.art-f2eef7bfc2ca41ef902828beeefe4684 |
| institution | Directory Open Access Journal |
| issn | 1756-6606 |
| language | English |
| last_indexed | 2024-12-16T18:56:11Z |
| publishDate | 2021-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Molecular Brain |
| spelling | doaj.art-f2eef7bfc2ca41ef902828beeefe46842022-12-21T22:20:31ZengBMCMolecular Brain1756-66062021-05-0114111110.1186/s13041-021-00786-7Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidationBoren Lin0Khaled Alganem1Sinead M. O’Donovan2Zhen Jin3FarzanehSadat Naghavi4Olivia A. Miller5Tyler C. Ortyl6Ye Chun Ruan7Robert E. McCullumsmith8Jianyang Du9Department of Anatomy and Neurobiology, The University of Tennessee Health Science CenterDepartment of Neurosciences, The University of Toledo Medical CenterDepartment of Neurosciences, The University of Toledo Medical CenterDepartment of Anatomy and Neurobiology, The University of Tennessee Health Science CenterDepartment of Neurosciences, The University of Toledo Medical CenterDepartment of Biological Sciences, The University of ToledoDepartment of Anatomy and Neurobiology, The University of Tennessee Health Science CenterDepartment of Biomedical Engineering, Faculty of Engineering, The Hong Kong Polytechnic UniversityDepartment of Neurosciences, The University of Toledo Medical CenterDepartment of Anatomy and Neurobiology, The University of Tennessee Health Science CenterAbstract Reconsolidation has been considered a process in which a consolidated memory is turned into a labile stage. Within the reconsolidation window, the labile memory can be either erased or strengthened. Manipulating acid-sensing ion channels (ASICs) in the amygdala via carbon dioxide (CO2) inhalation enhances memory retrieval and its lability within the reconsolidation window. Moreover, pairing CO2 inhalation with retrieval bears the reactivation of the memory trace and enhances the synaptic exchange of the calcium-impermeable AMPA receptors to calcium-permeable AMPA receptors. Our patch-clamp data suggest that the exchange of the AMPA receptors depends on the ubiquitin-proteasome system (UPS), via protein degradation. Ziram (50 µM), a ubiquitination inhibitor, reduces the turnover of the AMPA receptors. CO2 inhalation with retrieval boosts the ubiquitination without altering the proteasome activity. Several calcium-dependent kinases potentially involved in the CO2-inhalation regulated memory liability were identified using the Kinome assay. These results suggest that the UPS plays a key role in regulating the turnover of AMPA receptors during CO2 inhalation.https://doi.org/10.1186/s13041-021-00786-7Carbon dioxideAcid‐sensing ion channelsReconsolidationAversive conditioningMemory retrievalAMPA receptors |
| spellingShingle | Boren Lin Khaled Alganem Sinead M. O’Donovan Zhen Jin FarzanehSadat Naghavi Olivia A. Miller Tyler C. Ortyl Ye Chun Ruan Robert E. McCullumsmith Jianyang Du Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation Molecular Brain Carbon dioxide Acid‐sensing ion channels Reconsolidation Aversive conditioning Memory retrieval AMPA receptors |
| title | Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation |
| title_full | Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation |
| title_fullStr | Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation |
| title_full_unstemmed | Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation |
| title_short | Activation of acid‐sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation |
| title_sort | activation of acid sensing ion channels by carbon dioxide regulates amygdala synaptic protein degradation in memory reconsolidation |
| topic | Carbon dioxide Acid‐sensing ion channels Reconsolidation Aversive conditioning Memory retrieval AMPA receptors |
| url | https://doi.org/10.1186/s13041-021-00786-7 |
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