A bidirectional competitive interaction between circHomer1 and Homer1b within the orbitofrontal cortex regulates reversal learning

Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived...

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Published inCell reports (Cambridge) Vol. 38; no. 3; p. 110282
Main Authors Hafez, Alexander K., Zimmerman, Amber J., Papageorgiou, Grigorios, Chandrasekaran, Jayapriya, Amoah, Stephen K., Lin, Rixing, Lozano, Evelyn, Pierotti, Caroline, Dell’Orco, Michela, Hartley, Brigham J., Alural, Begüm, Lalonde, Jasmin, Esposito, John Matthew, Berretta, Sabina, Squassina, Alessio, Chillotti, Caterina, Voloudakis, Georgios, Shao, Zhiping, Fullard, John F., Brennand, Kristen J., Turecki, Gustavo, Roussos, Panos, Perlis, Roy H., Haggarty, Stephen J., Perrone-Bizzozero, Nora, Brigman, Jonathan L., Mellios, Nikolaos
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 18.01.2022
Subjects
Animals
bipolar disorder
Bipolar Disorder - metabolism
circHomer1
circRNAs
cognitive flexibility
Gene Expression Regulation - physiology
Gene Knockdown Techniques
Homer Scaffolding Proteins - metabolism
Homer1
Humans
Male
Mice
Mice, Inbred C57BL
OFC
Prefrontal Cortex - metabolism
reversal learning
Reversal Learning - physiology
RNA, Circular - metabolism
reversal learning
circRNAs
Homer1
bipolar disorder
circHomer1
cognitive flexibility
OFC
Online AccessGet full text
ISSN2211-1247
2639-1856
2211-1247
DOI10.1016/j.celrep.2021.110282

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Abstract Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived neuronal cultures of subjects with psychiatric disorders. We further demonstrate that in vivo circHomer1 knockdown (KD) within the OFC can inhibit the synaptic expression of Homer1b mRNA. Furthermore, we show that circHomer1 directly binds to Homer1b mRNA and that Homer1b-specific KD increases synaptic circHomer1 levels and improves OFC-mediated behavioral flexibility. Importantly, double circHomer1 and Homer1b in vivo co-KD results in a complete rescue in circHomer1-associated alterations in both chance reversal learning and synaptic gene expression. Lastly, we uncover an RNA-binding protein that can directly bind to circHomer1 and promote its biogenesis. Taken together, our data provide mechanistic insights into the importance of circRNAs in brain function and disease. [Display omitted] •Expression of circHomer1 is inversely associated with relative HOMER1B mRNA levels•CircHomer1 and Homer1b bind to each other and inhibit each other's synaptic expression•In vivo KD of Homer1b improves OFC-mediated chance reversal learning•Co-KD of Homer1b and circHomer1 restores chance reversal learning Through in vivo circRNA and mRNA isoform-specific knockdown in mouse orbitofrontal cortex (OFC), Hafez et al. elucidate the antagonistic interaction between the psychiatric-disease-associated circHomer1 and Homer1b mRNA and their opposing effects on OFC-mediated reversal learning.
AbstractList Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived neuronal cultures of subjects with psychiatric disorders. We further demonstrate that in vivo circHomer1 knockdown (KD) within the OFC can inhibit the synaptic expression of Homer1b mRNA. Furthermore, we show that circHomer1 directly binds to Homer1b mRNA and that Homer1b-specific KD increases synaptic circHomer1 levels and improves OFC-mediated behavioral flexibility. Importantly, double circHomer1 and Homer1b in vivo co-KD results in a complete rescue in circHomer1-associated alterations in both chance reversal learning and synaptic gene expression. Lastly, we uncover an RNA-binding protein that can directly bind to circHomer1 and promote its biogenesis. Taken together, our data provide mechanistic insights into the importance of circRNAs in brain function and disease.Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived neuronal cultures of subjects with psychiatric disorders. We further demonstrate that in vivo circHomer1 knockdown (KD) within the OFC can inhibit the synaptic expression of Homer1b mRNA. Furthermore, we show that circHomer1 directly binds to Homer1b mRNA and that Homer1b-specific KD increases synaptic circHomer1 levels and improves OFC-mediated behavioral flexibility. Importantly, double circHomer1 and Homer1b in vivo co-KD results in a complete rescue in circHomer1-associated alterations in both chance reversal learning and synaptic gene expression. Lastly, we uncover an RNA-binding protein that can directly bind to circHomer1 and promote its biogenesis. Taken together, our data provide mechanistic insights into the importance of circRNAs in brain function and disease.
Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived neuronal cultures of subjects with psychiatric disorders. We further demonstrate that in vivo circHomer1 knockdown (KD) within the OFC can inhibit the synaptic expression of Homer1b mRNA. Furthermore, we show that circHomer1 directly binds to Homer1b mRNA and that Homer1b-specific KD increases synaptic circHomer1 levels and improves OFC-mediated behavioral flexibility. Importantly, double circHomer1 and Homer1b in vivo co-KD results in a complete rescue in circHomer1-associated alterations in both chance reversal learning and synaptic gene expression. Lastly, we uncover an RNA-binding protein that can directly bind to circHomer1 and promote its biogenesis. Taken together, our data provide mechanistic insights into the importance of circRNAs in brain function and disease. Through in vivo circRNA and mRNA isoform-specific knockdown in mouse orbitofrontal cortex (OFC), Hafez et al. elucidate the antagonistic interaction between the psychiatric-disease-associated circHomer1 and Homer1b mRNA and their opposing effects on OFC-mediated reversal learning.
Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived neuronal cultures of subjects with psychiatric disorders. We further demonstrate that in vivo circHomer1 knockdown (KD) within the OFC can inhibit the synaptic expression of Homer1b mRNA. Furthermore, we show that circHomer1 directly binds to Homer1b mRNA and that Homer1b-specific KD increases synaptic circHomer1 levels and improves OFC-mediated behavioral flexibility. Importantly, double circHomer1 and Homer1b in vivo co-KD results in a complete rescue in circHomer1-associated alterations in both chance reversal learning and synaptic gene expression. Lastly, we uncover an RNA-binding protein that can directly bind to circHomer1 and promote its biogenesis. Taken together, our data provide mechanistic insights into the importance of circRNAs in brain function and disease. [Display omitted] •Expression of circHomer1 is inversely associated with relative HOMER1B mRNA levels•CircHomer1 and Homer1b bind to each other and inhibit each other's synaptic expression•In vivo KD of Homer1b improves OFC-mediated chance reversal learning•Co-KD of Homer1b and circHomer1 restores chance reversal learning Through in vivo circRNA and mRNA isoform-specific knockdown in mouse orbitofrontal cortex (OFC), Hafez et al. elucidate the antagonistic interaction between the psychiatric-disease-associated circHomer1 and Homer1b mRNA and their opposing effects on OFC-mediated reversal learning.
Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show that circHomer1 is inversely associated with relative HOMER1B mRNA isoform levels in both the orbitofrontal cortex (OFC) and stem-cell-derived neuronal cultures of subjects with psychiatric disorders. We further demonstrate that in vivo circHomer1 knockdown (KD) within the OFC can inhibit the synaptic expression of Homer1b mRNA. Furthermore, we show that circHomer1 directly binds to Homer1b mRNA and that Homer1b-specific KD increases synaptic circHomer1 levels and improves OFC-mediated behavioral flexibility. Importantly, double circHomer1 and Homer1b in vivo co-KD results in a complete rescue in circHomer1-associated alterations in both chance reversal learning and synaptic gene expression. Lastly, we uncover an RNA-binding protein that can directly bind to circHomer1 and promote its biogenesis. Taken together, our data provide mechanistic insights into the importance of circRNAs in brain function and disease.
ArticleNumber 110282
Author Mellios, Nikolaos
Papageorgiou, Grigorios
Amoah, Stephen K.
Perlis, Roy H.
Pierotti, Caroline
Berretta, Sabina
Voloudakis, Georgios
Lozano, Evelyn
Chandrasekaran, Jayapriya
Lalonde, Jasmin
Fullard, John F.
Haggarty, Stephen J.
Hartley, Brigham J.
Brigman, Jonathan L.
Shao, Zhiping
Brennand, Kristen J.
Esposito, John Matthew
Roussos, Panos
Squassina, Alessio
Chillotti, Caterina
Zimmerman, Amber J.
Lin, Rixing
Alural, Begüm
Perrone-Bizzozero, Nora
Dell’Orco, Michela
Hafez, Alexander K.
Turecki, Gustavo
AuthorAffiliation 11 Pamela Sklar Division of Psychiatric Genomics, New York, NY, USA
13 Icahn Institute for Data Science and Genomic Technology, New York, NY, USA
19 Present address: Departments of Psychiatry and Genetics, Division of Molecular Psychiatry, Yale University School of Medicine, New Haven, CT, USA
10 Unit of Clinical Pharmacology, University Hospital Agency of Cagliari, Cagliari, Italy
6 Translational Neuroscience Laboratory, Mclean Hospital, Belmont, MA, USA
15 Mental Illness Research, Education and Clinical Centers, James J. Peters VA Medical Center, Bronx, NY, USA
5 Center for Genomic Medicine, Chemical Neurobiology Laboratory, Departments of Neurology and Psychiatry, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA
20 Present address: Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, Canada
22 Lead contact
2 Autophagy Inflammation and Metabolism Center of Biomedical Research Excellence, University of New Mexico Health Sciences Center, Albu
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Thu Jul 10 22:33:15 EDT 2025
Mon Jul 21 05:55:49 EDT 2025
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Issue 3
Keywords reversal learning
circRNAs
Homer1
bipolar disorder
circHomer1
cognitive flexibility
OFC
Language English
License This is an open access article under the CC BY license.
Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.
cc-by
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content type line 23
AUTHOR CONTRIBUTIONS
N.M. conceived the hypothesis; designed, performed, and supervised experiments; analyzed data; and wrote the manuscript. J.L.B. and N.P.-B. designed and supervised experiments, analyzed data, and provided feedback on the hypothesis and manuscript. A.K.H., A.J.Z., and G.P. designed and performed experiments, analyzed data, provided feedback on the hypothesis, and helped in manuscript preparation. All other authors performed experiments and analyzed data. All authors reviewed the paper.
OpenAccessLink https://www.sciencedirect.com/science/article/pii/S2211124721017976
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Snippet Although circular RNAs (circRNAs) are enriched in the brain, their relevance for brain function and psychiatric disorders is poorly understood. Here, we show...
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SubjectTerms Animals
bipolar disorder
Bipolar Disorder - metabolism
circHomer1
circRNAs
cognitive flexibility
Gene Expression Regulation - physiology
Gene Knockdown Techniques
Homer Scaffolding Proteins - metabolism
Homer1
Humans
Male
Mice
Mice, Inbred C57BL
OFC
Prefrontal Cortex - metabolism
reversal learning
Reversal Learning - physiology
RNA, Circular - metabolism
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Title A bidirectional competitive interaction between circHomer1 and Homer1b within the orbitofrontal cortex regulates reversal learning
URI https://dx.doi.org/10.1016/j.celrep.2021.110282
https://www.ncbi.nlm.nih.gov/pubmed/35045295
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https://pubmed.ncbi.nlm.nih.gov/PMC8809079
http://www.cell.com/article/S2211124721017976/pdf
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