Molecular insights into the regulation of constitutive activity by RNA editing of 5HT2C serotonin receptors
RNA editing is a process by which post-transcriptional changes of mRNA nucleotides alter protein function through modification of the amino acid content. The 5HT2C serotonin receptor, which undergoes 32 distinct RNA-editing events leading to 24 protein isoforms, is a notable example of this process....
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| Published in | Cell reports (Cambridge) Vol. 40; no. 7; p. 111211 |
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| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
Elsevier Inc
16.08.2022
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| Subjects | |
| Online Access | Get full text |
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| Abstract | RNA editing is a process by which post-transcriptional changes of mRNA nucleotides alter protein function through modification of the amino acid content. The 5HT2C serotonin receptor, which undergoes 32 distinct RNA-editing events leading to 24 protein isoforms, is a notable example of this process. These 5HT2C isoforms display differences in constitutive activity, agonist/inverse agonist potencies, and efficacies. To elucidate the molecular mechanisms responsible for these effects of RNA editing, we present four active-state 5HT2C-transducer-coupled structures of three representative isoforms (INI, VGV, and VSV) with the selective drug lorcaserin (Belviq) and the classic psychedelic psilocin. We also provide a comprehensive analysis of agonist activation and constitutive activity across all 24 protein isoforms. Collectively, these findings reveal a unique hydrogen-bonding network located on intracellular loop 2 that is subject to RNA editing, which differentially affects GPCR constitutive and agonist signaling activities.
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•5HT2C receptor RNA editing modulates constitutive activity through interactions on ICL2•Structural evidence reveals that RNA editing modulates a hydrogen-bonding network on ICL2•Evidence of ICL2 isomerization and changes in G-protein affinity that alter basal activity
It is established that the 5HT2C receptor undergoes RNA editing leading to 24 isoforms. Several isoforms exhibit changes in basal activity and are linked to pathologies. Gumpper et al. have done a systematic structure-function characterization of all the isoforms revealing the underlying mechanisms that govern basal activity of the 5HT2C receptor. |
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| AbstractList | RNA editing is a process by which post-transcriptional changes of mRNA nucleotides alter protein function through modification of the amino acid content. The 5HT2C serotonin receptor, which undergoes 32 distinct RNA-editing events leading to 24 protein isoforms, is a notable example of this process. These 5HT2C isoforms display differences in constitutive activity, agonist/inverse agonist potencies, and efficacies. To elucidate the molecular mechanisms responsible for these effects of RNA editing, we present four active-state 5HT2C-transducer-coupled structures of three representative isoforms (INI, VGV, and VSV) with the selective drug lorcaserin (Belviq) and the classic psychedelic psilocin. We also provide a comprehensive analysis of agonist activation and constitutive activity across all 24 protein isoforms. Collectively, these findings reveal a unique hydrogen-bonding network located on intracellular loop 2 that is subject to RNA editing, which differentially affects GPCR constitutive and agonist signaling activities.
[Display omitted]
•5HT2C receptor RNA editing modulates constitutive activity through interactions on ICL2•Structural evidence reveals that RNA editing modulates a hydrogen-bonding network on ICL2•Evidence of ICL2 isomerization and changes in G-protein affinity that alter basal activity
It is established that the 5HT2C receptor undergoes RNA editing leading to 24 isoforms. Several isoforms exhibit changes in basal activity and are linked to pathologies. Gumpper et al. have done a systematic structure-function characterization of all the isoforms revealing the underlying mechanisms that govern basal activity of the 5HT2C receptor. RNA editing is a process by which post-transcriptional changes of mRNA nucleotides alter protein function through modification of the amino acid content. The 5HT 2C serotonin receptor, which undergoes 32 distinct RNA-editing events leading to 24 protein isoforms, is a notable example of this process. These 5HT 2C isoforms display differences in constitutive activity, agonist/inverse agonist potencies, and efficacies. To elucidate the molecular mechanisms responsible for these effects of RNA editing, we present four active-state 5HT 2C -transducer-coupled structures of three representative isoforms (INI, VGV, and VSV) with the selective drug lorcaserin (Belviq) and the classic psychedelic psilocin. We also provide a comprehensive analysis of agonist activation and constitutive activity across all 24 protein isoforms. Collectively, these findings reveal a unique hydrogen-bonding network located on intracellular loop 2 that is subject to RNA editing, which differentially affects GPCR constitutive and agonist signaling activities. It is established that the 5HT 2C receptor undergoes RNA editing leading to 24 isoforms. Several isoforms exhibit changes in basal activity and are linked to pathologies. Gumpper et al. have done a systematic structure-function characterization of all the isoforms revealing the underlying mechanisms that govern basal activity of the 5HT 2C receptor. RNA editing is a process by which post-transcriptional changes of mRNA nucleotides alter protein function through modification of the amino acid content. The 5HT2C serotonin receptor, which undergoes 32 distinct RNA-editing events leading to 24 protein isoforms, is a notable example of this process. These 5HT2C isoforms display differences in constitutive activity, agonist/inverse agonist potencies, and efficacies. To elucidate the molecular mechanisms responsible for these effects of RNA editing, we present four active-state 5HT2C-transducer-coupled structures of three representative isoforms (INI, VGV, and VSV) with the selective drug lorcaserin (Belviq) and the classic psychedelic psilocin. We also provide a comprehensive analysis of agonist activation and constitutive activity across all 24 protein isoforms. Collectively, these findings reveal a unique hydrogen-bonding network located on intracellular loop 2 that is subject to RNA editing, which differentially affects GPCR constitutive and agonist signaling activities.RNA editing is a process by which post-transcriptional changes of mRNA nucleotides alter protein function through modification of the amino acid content. The 5HT2C serotonin receptor, which undergoes 32 distinct RNA-editing events leading to 24 protein isoforms, is a notable example of this process. These 5HT2C isoforms display differences in constitutive activity, agonist/inverse agonist potencies, and efficacies. To elucidate the molecular mechanisms responsible for these effects of RNA editing, we present four active-state 5HT2C-transducer-coupled structures of three representative isoforms (INI, VGV, and VSV) with the selective drug lorcaserin (Belviq) and the classic psychedelic psilocin. We also provide a comprehensive analysis of agonist activation and constitutive activity across all 24 protein isoforms. Collectively, these findings reveal a unique hydrogen-bonding network located on intracellular loop 2 that is subject to RNA editing, which differentially affects GPCR constitutive and agonist signaling activities. |
| ArticleNumber | 111211 |
| Author | Fay, Jonathan F. Gumpper, Ryan H. Roth, Bryan L. |
| AuthorAffiliation | 2 Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA 1 Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA 3 Lead contact |
| AuthorAffiliation_xml | – name: 1 Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA – name: 2 Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA – name: 3 Lead contact |
| Author_xml | – sequence: 1 givenname: Ryan H. surname: Gumpper fullname: Gumpper, Ryan H. email: rgumpper@email.unc.edu organization: Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA – sequence: 2 givenname: Jonathan F. surname: Fay fullname: Fay, Jonathan F. organization: Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA – sequence: 3 givenname: Bryan L. surname: Roth fullname: Roth, Bryan L. email: bryan_roth@med.unc.edu organization: Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC 27599, USA |
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| Copyright | 2022 The Author(s) Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved. |
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| Keywords | Gq protein serotonin constitutive activity G-protein-coupled receptor CP: Molecular biology lorcaserin structural biology psilocin 5HT2CR |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS R.H.G. designed experiments; performed cloning, expression, and purification of protein samples for cryo-EM, PI hydrolysis, and TRUPATH studies; processed cryo-EM data; performed model refinement; analyzed data; and prepared figures and the manuscript. J.F.F. performed the cryo-EM data collection and processing and helped with model refinement/map quality and assisted with manuscript preparation. B.L.R. supervised and proposed the project, guided structural and functional studies, and prepared the manuscript. |
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| Title | Molecular insights into the regulation of constitutive activity by RNA editing of 5HT2C serotonin receptors |
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