Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake

Abstract The serotonin 2C receptor regulates food uptake, and its activity is regulated by alternative pre‐mRNA splicing. Alternative exon skipping is predicted to generate a truncated receptor protein isoform, whose existence was confirmed with a new antiserum. The truncated receptor sequesters the...

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Main Authors: Zhaiyi Zhang, Manli Shen, Paul J Gresch, Masoud Ghamari‐Langroudi, Alexander G Rabchevsky, Ronald B Emeson, Stefan Stamm
Format: Article
Language:English
Published: Springer Nature 2016-07-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201506030
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author Zhaiyi Zhang
Manli Shen
Paul J Gresch
Masoud Ghamari‐Langroudi
Alexander G Rabchevsky
Ronald B Emeson
Stefan Stamm
author_facet Zhaiyi Zhang
Manli Shen
Paul J Gresch
Masoud Ghamari‐Langroudi
Alexander G Rabchevsky
Ronald B Emeson
Stefan Stamm
author_sort Zhaiyi Zhang
collection DOAJ
description Abstract The serotonin 2C receptor regulates food uptake, and its activity is regulated by alternative pre‐mRNA splicing. Alternative exon skipping is predicted to generate a truncated receptor protein isoform, whose existence was confirmed with a new antiserum. The truncated receptor sequesters the full‐length receptor in intracellular membranes. We developed an oligonucleotide that promotes exon inclusion, which increases the ratio of the full‐length to truncated receptor protein. Decreasing the amount of truncated receptor results in the accumulation of full‐length, constitutively active receptor at the cell surface. After injection into the third ventricle of mice, the oligonucleotide accumulates in the arcuate nucleus, where it changes alternative splicing of the serotonin 2C receptor and increases pro‐opiomelanocortin expression. Oligonucleotide injection reduced food intake in both wild‐type and ob/ob mice. Unexpectedly, the oligonucleotide crossed the blood–brain barrier and its systemic delivery reduced food intake in wild‐type mice. The physiological effect of the oligonucleotide suggests that a truncated splice variant regulates the activity of the serotonin 2C receptor, indicating that therapies aimed to change pre‐mRNA processing could be useful to treat hyperphagia, characteristic for disorders like Prader–Willi syndrome.
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spelling doaj-art-a6f72dfd59c54ff8a4ad50a869f07a9b2025-08-20T03:46:24ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842016-07-018887889410.15252/emmm.201506030Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intakeZhaiyi Zhang0Manli Shen1Paul J Gresch2Masoud Ghamari‐Langroudi3Alexander G Rabchevsky4Ronald B Emeson5Stefan Stamm6Department of Molecular and Cellular Biochemistry, University of KentuckyDepartment of Molecular and Cellular Biochemistry, University of KentuckyDepartment of Pharmacology, Vanderbilt UniversityDepartment of Molecular Physiology & Biophysics, Vanderbilt UniversitySpinal Cord & Brain Injury, Research Center, University of KentuckyDepartment of Molecular Physiology & Biophysics, Vanderbilt UniversityDepartment of Molecular and Cellular Biochemistry, University of KentuckyAbstract The serotonin 2C receptor regulates food uptake, and its activity is regulated by alternative pre‐mRNA splicing. Alternative exon skipping is predicted to generate a truncated receptor protein isoform, whose existence was confirmed with a new antiserum. The truncated receptor sequesters the full‐length receptor in intracellular membranes. We developed an oligonucleotide that promotes exon inclusion, which increases the ratio of the full‐length to truncated receptor protein. Decreasing the amount of truncated receptor results in the accumulation of full‐length, constitutively active receptor at the cell surface. After injection into the third ventricle of mice, the oligonucleotide accumulates in the arcuate nucleus, where it changes alternative splicing of the serotonin 2C receptor and increases pro‐opiomelanocortin expression. Oligonucleotide injection reduced food intake in both wild‐type and ob/ob mice. Unexpectedly, the oligonucleotide crossed the blood–brain barrier and its systemic delivery reduced food intake in wild‐type mice. The physiological effect of the oligonucleotide suggests that a truncated splice variant regulates the activity of the serotonin 2C receptor, indicating that therapies aimed to change pre‐mRNA processing could be useful to treat hyperphagia, characteristic for disorders like Prader–Willi syndrome.https://doi.org/10.15252/emmm.201506030alternative splicingbrain functionfood uptakeobesitypre‐mRNA processing
spellingShingle Zhaiyi Zhang
Manli Shen
Paul J Gresch
Masoud Ghamari‐Langroudi
Alexander G Rabchevsky
Ronald B Emeson
Stefan Stamm
Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake
EMBO Molecular Medicine
alternative splicing
brain function
food uptake
obesity
pre‐mRNA processing
title Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake
title_full Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake
title_fullStr Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake
title_full_unstemmed Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake
title_short Oligonucleotide‐induced alternative splicing of serotonin 2C receptor reduces food intake
title_sort oligonucleotide induced alternative splicing of serotonin 2c receptor reduces food intake
topic alternative splicing
brain function
food uptake
obesity
pre‐mRNA processing
url https://doi.org/10.15252/emmm.201506030
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AT manlishen oligonucleotideinducedalternativesplicingofserotonin2creceptorreducesfoodintake
AT pauljgresch oligonucleotideinducedalternativesplicingofserotonin2creceptorreducesfoodintake
AT masoudghamarilangroudi oligonucleotideinducedalternativesplicingofserotonin2creceptorreducesfoodintake
AT alexandergrabchevsky oligonucleotideinducedalternativesplicingofserotonin2creceptorreducesfoodintake
AT ronaldbemeson oligonucleotideinducedalternativesplicingofserotonin2creceptorreducesfoodintake
AT stefanstamm oligonucleotideinducedalternativesplicingofserotonin2creceptorreducesfoodintake