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Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus

The nucleolus is a plurifunctional organelle in which structure and function are intimately linked. Its structural plasticity has long been appreciated, particularly in response to transcriptional inhibition and other cellular stresses, although the mechanism and physiological relevance of these phe...

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Autores principales: Jacob, Mathieu D., Audas, Timothy E., Uniacke, James, Trinkle-Mulcahy, Laura, Lee, Stephen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3771955/
https://www.ncbi.nlm.nih.gov/pubmed/23904269
http://dx.doi.org/10.1091/mbc.E13-04-0223
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author Jacob, Mathieu D.
Audas, Timothy E.
Uniacke, James
Trinkle-Mulcahy, Laura
Lee, Stephen
author_facet Jacob, Mathieu D.
Audas, Timothy E.
Uniacke, James
Trinkle-Mulcahy, Laura
Lee, Stephen
author_sort Jacob, Mathieu D.
collection PubMed
description The nucleolus is a plurifunctional organelle in which structure and function are intimately linked. Its structural plasticity has long been appreciated, particularly in response to transcriptional inhibition and other cellular stresses, although the mechanism and physiological relevance of these phenomena are unclear. Using MCF-7 and other mammalian cell lines, we describe a structural and functional adaptation of the nucleolus, triggered by heat shock or physiological acidosis, that depends on the expression of ribosomal intergenic spacer long noncoding RNA (IGS lncRNA). At the heart of this process is the de novo formation of a large subnucleolar structure, termed the detention center (DC). The DC is a spatially and dynamically distinct region, characterized by an 8-anilino-1-naphthalenesulfonate–positive hydrophobic signature. Its formation is accompanied by redistribution of nucleolar factors and arrest in ribosomal biogenesis. Silencing of regulatory IGS lncRNA prevents the creation of this structure and allows the nucleolus to retain its tripartite organization and transcriptional activity. Signal termination causes a decrease in IGS transcript levels and a return to the active nucleolar conformation. We propose that the induction of IGS lncRNA by environmental signals operates as a molecular switch that regulates the structure and function of the nucleolus.
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spelling pubmed-37719552013-11-30 Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus Jacob, Mathieu D. Audas, Timothy E. Uniacke, James Trinkle-Mulcahy, Laura Lee, Stephen Mol Biol Cell Articles The nucleolus is a plurifunctional organelle in which structure and function are intimately linked. Its structural plasticity has long been appreciated, particularly in response to transcriptional inhibition and other cellular stresses, although the mechanism and physiological relevance of these phenomena are unclear. Using MCF-7 and other mammalian cell lines, we describe a structural and functional adaptation of the nucleolus, triggered by heat shock or physiological acidosis, that depends on the expression of ribosomal intergenic spacer long noncoding RNA (IGS lncRNA). At the heart of this process is the de novo formation of a large subnucleolar structure, termed the detention center (DC). The DC is a spatially and dynamically distinct region, characterized by an 8-anilino-1-naphthalenesulfonate–positive hydrophobic signature. Its formation is accompanied by redistribution of nucleolar factors and arrest in ribosomal biogenesis. Silencing of regulatory IGS lncRNA prevents the creation of this structure and allows the nucleolus to retain its tripartite organization and transcriptional activity. Signal termination causes a decrease in IGS transcript levels and a return to the active nucleolar conformation. We propose that the induction of IGS lncRNA by environmental signals operates as a molecular switch that regulates the structure and function of the nucleolus. The American Society for Cell Biology 2013-09-15 /pmc/articles/PMC3771955/ /pubmed/23904269 http://dx.doi.org/10.1091/mbc.E13-04-0223 Text en © 2013 Jacob et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Jacob, Mathieu D.
Audas, Timothy E.
Uniacke, James
Trinkle-Mulcahy, Laura
Lee, Stephen
Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus
title Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus
title_full Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus
title_fullStr Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus
title_full_unstemmed Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus
title_short Environmental cues induce a long noncoding RNA–dependent remodeling of the nucleolus
title_sort environmental cues induce a long noncoding rna–dependent remodeling of the nucleolus
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3771955/
https://www.ncbi.nlm.nih.gov/pubmed/23904269
http://dx.doi.org/10.1091/mbc.E13-04-0223
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