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Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease

Genes encoding cell-surface proteins control nervous system development and are implicated in neurological disorders. These genes produce alternative mRNA isoforms which remain poorly characterized, impeding understanding of how disease-associated mutations cause pathology. Here we introduce a strat...

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Autores principales: Ray, Thomas A., Cochran, Kelly, Kozlowski, Chris, Wang, Jingjing, Alexander, Graham, Cady, Martha A., Spencer, William J., Ruzycki, Philip A., Clark, Brian S., Laeremans, Annelies, He, Ming-Xiao, Wang, Xiaoming, Park, Emily, Hao, Ying, Iannaccone, Alessandro, Hu, Gary, Fedrigo, Olivier, Skiba, Nikolai P., Arshavsky, Vadim Y., Kay, Jeremy N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7335077/
https://www.ncbi.nlm.nih.gov/pubmed/32620864
http://dx.doi.org/10.1038/s41467-020-17009-7
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author Ray, Thomas A.
Cochran, Kelly
Kozlowski, Chris
Wang, Jingjing
Alexander, Graham
Cady, Martha A.
Spencer, William J.
Ruzycki, Philip A.
Clark, Brian S.
Laeremans, Annelies
He, Ming-Xiao
Wang, Xiaoming
Park, Emily
Hao, Ying
Iannaccone, Alessandro
Hu, Gary
Fedrigo, Olivier
Skiba, Nikolai P.
Arshavsky, Vadim Y.
Kay, Jeremy N.
author_facet Ray, Thomas A.
Cochran, Kelly
Kozlowski, Chris
Wang, Jingjing
Alexander, Graham
Cady, Martha A.
Spencer, William J.
Ruzycki, Philip A.
Clark, Brian S.
Laeremans, Annelies
He, Ming-Xiao
Wang, Xiaoming
Park, Emily
Hao, Ying
Iannaccone, Alessandro
Hu, Gary
Fedrigo, Olivier
Skiba, Nikolai P.
Arshavsky, Vadim Y.
Kay, Jeremy N.
author_sort Ray, Thomas A.
collection PubMed
description Genes encoding cell-surface proteins control nervous system development and are implicated in neurological disorders. These genes produce alternative mRNA isoforms which remain poorly characterized, impeding understanding of how disease-associated mutations cause pathology. Here we introduce a strategy to define complete portfolios of full-length isoforms encoded by individual genes. Applying this approach to neural cell-surface molecules, we identify thousands of unannotated isoforms expressed in retina and brain. By mass spectrometry we confirm expression of newly-discovered proteins on the cell surface in vivo. Remarkably, we discover that the major isoform of a retinal degeneration gene, CRB1, was previously overlooked. This CRB1 isoform is the only one expressed by photoreceptors, the affected cells in CRB1 disease. Using mouse mutants, we identify a function for this isoform at photoreceptor-glial junctions and demonstrate that loss of this isoform accelerates photoreceptor death. Therefore, our isoform identification strategy enables discovery of new gene functions relevant to disease.
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spelling pubmed-73350772020-07-09 Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease Ray, Thomas A. Cochran, Kelly Kozlowski, Chris Wang, Jingjing Alexander, Graham Cady, Martha A. Spencer, William J. Ruzycki, Philip A. Clark, Brian S. Laeremans, Annelies He, Ming-Xiao Wang, Xiaoming Park, Emily Hao, Ying Iannaccone, Alessandro Hu, Gary Fedrigo, Olivier Skiba, Nikolai P. Arshavsky, Vadim Y. Kay, Jeremy N. Nat Commun Article Genes encoding cell-surface proteins control nervous system development and are implicated in neurological disorders. These genes produce alternative mRNA isoforms which remain poorly characterized, impeding understanding of how disease-associated mutations cause pathology. Here we introduce a strategy to define complete portfolios of full-length isoforms encoded by individual genes. Applying this approach to neural cell-surface molecules, we identify thousands of unannotated isoforms expressed in retina and brain. By mass spectrometry we confirm expression of newly-discovered proteins on the cell surface in vivo. Remarkably, we discover that the major isoform of a retinal degeneration gene, CRB1, was previously overlooked. This CRB1 isoform is the only one expressed by photoreceptors, the affected cells in CRB1 disease. Using mouse mutants, we identify a function for this isoform at photoreceptor-glial junctions and demonstrate that loss of this isoform accelerates photoreceptor death. Therefore, our isoform identification strategy enables discovery of new gene functions relevant to disease. Nature Publishing Group UK 2020-07-03 /pmc/articles/PMC7335077/ /pubmed/32620864 http://dx.doi.org/10.1038/s41467-020-17009-7 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Ray, Thomas A.
Cochran, Kelly
Kozlowski, Chris
Wang, Jingjing
Alexander, Graham
Cady, Martha A.
Spencer, William J.
Ruzycki, Philip A.
Clark, Brian S.
Laeremans, Annelies
He, Ming-Xiao
Wang, Xiaoming
Park, Emily
Hao, Ying
Iannaccone, Alessandro
Hu, Gary
Fedrigo, Olivier
Skiba, Nikolai P.
Arshavsky, Vadim Y.
Kay, Jeremy N.
Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
title Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
title_full Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
title_fullStr Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
title_full_unstemmed Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
title_short Comprehensive identification of mRNA isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
title_sort comprehensive identification of mrna isoforms reveals the diversity of neural cell-surface molecules with roles in retinal development and disease
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7335077/
https://www.ncbi.nlm.nih.gov/pubmed/32620864
http://dx.doi.org/10.1038/s41467-020-17009-7
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