Dimerization of ADAR1 modulates site-specificity of RNA editing

Abstract Adenosine-to-inosine editing is catalyzed by adenosine deaminases acting on RNA (ADARs) in double-stranded RNA (dsRNA) regions. Although three ADARs exist in mammals, ADAR1 is responsible for the vast majority of the editing events and acts on thousands of sites in the human transcriptome....

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Main Authors: Allegra Mboukou, Vinod Rajendra, Serafina Messmer, Therese C. Mandl, Marjorie Catala, Carine Tisné, Michael F. Jantsch, Pierre Barraud
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-53777-2
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author Allegra Mboukou
Vinod Rajendra
Serafina Messmer
Therese C. Mandl
Marjorie Catala
Carine Tisné
Michael F. Jantsch
Pierre Barraud
author_facet Allegra Mboukou
Vinod Rajendra
Serafina Messmer
Therese C. Mandl
Marjorie Catala
Carine Tisné
Michael F. Jantsch
Pierre Barraud
author_sort Allegra Mboukou
collection DOAJ
description Abstract Adenosine-to-inosine editing is catalyzed by adenosine deaminases acting on RNA (ADARs) in double-stranded RNA (dsRNA) regions. Although three ADARs exist in mammals, ADAR1 is responsible for the vast majority of the editing events and acts on thousands of sites in the human transcriptome. ADAR1 has been proposed to form a stable homodimer and dimerization is suggested to be important for editing activity. In the absence of a structural basis for the dimerization of ADAR1, and without a way to prevent dimer formation, the effect of dimerization on enzyme activity or site specificity has remained elusive. Here, we report on the structural analysis of the third double-stranded RNA-binding domain of ADAR1 (dsRBD3), which reveals stable dimer formation through a large inter-domain interface. Exploiting these structural insights, we engineered an interface-mutant disrupting ADAR1-dsRBD3 dimerization. Notably, dimerization disruption did not abrogate ADAR1 editing activity but intricately affected editing efficiency at selected sites. This suggests a complex role for dimerization in the selection of editing sites by ADARs, and makes dimerization a potential target for modulating ADAR1 editing activity.
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spelling doaj-art-bec12aa3a4b14de3ba77fce667ddf20a2024-11-24T12:33:18ZengNature PortfolioNature Communications2041-17232024-11-0115111410.1038/s41467-024-53777-2Dimerization of ADAR1 modulates site-specificity of RNA editingAllegra Mboukou0Vinod Rajendra1Serafina Messmer2Therese C. Mandl3Marjorie Catala4Carine Tisné5Michael F. Jantsch6Pierre Barraud7Expression génétique microbienne, Université Paris Cité, CNRS, Institut de biologie physico-chimiqueDivision of Cell and Developmental Biology, Center for Anatomy and Cell Biology, Medical University of ViennaDivision of Cell and Developmental Biology, Center for Anatomy and Cell Biology, Medical University of ViennaDivision of Cell and Developmental Biology, Center for Anatomy and Cell Biology, Medical University of ViennaExpression génétique microbienne, Université Paris Cité, CNRS, Institut de biologie physico-chimiqueExpression génétique microbienne, Université Paris Cité, CNRS, Institut de biologie physico-chimiqueDivision of Cell and Developmental Biology, Center for Anatomy and Cell Biology, Medical University of ViennaExpression génétique microbienne, Université Paris Cité, CNRS, Institut de biologie physico-chimiqueAbstract Adenosine-to-inosine editing is catalyzed by adenosine deaminases acting on RNA (ADARs) in double-stranded RNA (dsRNA) regions. Although three ADARs exist in mammals, ADAR1 is responsible for the vast majority of the editing events and acts on thousands of sites in the human transcriptome. ADAR1 has been proposed to form a stable homodimer and dimerization is suggested to be important for editing activity. In the absence of a structural basis for the dimerization of ADAR1, and without a way to prevent dimer formation, the effect of dimerization on enzyme activity or site specificity has remained elusive. Here, we report on the structural analysis of the third double-stranded RNA-binding domain of ADAR1 (dsRBD3), which reveals stable dimer formation through a large inter-domain interface. Exploiting these structural insights, we engineered an interface-mutant disrupting ADAR1-dsRBD3 dimerization. Notably, dimerization disruption did not abrogate ADAR1 editing activity but intricately affected editing efficiency at selected sites. This suggests a complex role for dimerization in the selection of editing sites by ADARs, and makes dimerization a potential target for modulating ADAR1 editing activity.https://doi.org/10.1038/s41467-024-53777-2
spellingShingle Allegra Mboukou
Vinod Rajendra
Serafina Messmer
Therese C. Mandl
Marjorie Catala
Carine Tisné
Michael F. Jantsch
Pierre Barraud
Dimerization of ADAR1 modulates site-specificity of RNA editing
Nature Communications
title Dimerization of ADAR1 modulates site-specificity of RNA editing
title_full Dimerization of ADAR1 modulates site-specificity of RNA editing
title_fullStr Dimerization of ADAR1 modulates site-specificity of RNA editing
title_full_unstemmed Dimerization of ADAR1 modulates site-specificity of RNA editing
title_short Dimerization of ADAR1 modulates site-specificity of RNA editing
title_sort dimerization of adar1 modulates site specificity of rna editing
url https://doi.org/10.1038/s41467-024-53777-2
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