Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells

Recent footprinting studies have made the surprising observation that long noncoding RNAs (lncRNAs) physically interact with ribosomes. However, these findings remain controversial, and the overall proportion of cytoplasmic lncRNAs involved is unknown. Here we make a global, absolute estimate of the...

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Main Authors: Carlevaro-Fita, Joana, Rahim, Anisa, Guigó, Roderic, Johnson, Rory, Vardy, Leah Karen Anne
Other Authors: School of Biological Sciences
Format: Journal Article
Language:English
Published: 2016
Subjects:
Online Access:https://hdl.handle.net/10356/81504
http://hdl.handle.net/10220/40809
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author Carlevaro-Fita, Joana
Rahim, Anisa
Guigó, Roderic
Johnson, Rory
Vardy, Leah Karen Anne
author2 School of Biological Sciences
author_facet School of Biological Sciences
Carlevaro-Fita, Joana
Rahim, Anisa
Guigó, Roderic
Johnson, Rory
Vardy, Leah Karen Anne
author_sort Carlevaro-Fita, Joana
collection NTU
description Recent footprinting studies have made the surprising observation that long noncoding RNAs (lncRNAs) physically interact with ribosomes. However, these findings remain controversial, and the overall proportion of cytoplasmic lncRNAs involved is unknown. Here we make a global, absolute estimate of the cytoplasmic and ribosome-associated population of stringently filtered lncRNAs in a human cell line using polysome profiling coupled to spike-in normalized microarray analysis. Fifty-four percent of expressed lncRNAs are detected in the cytoplasm. The majority of these (70%) have >50% of their cytoplasmic copies associated with polysomal fractions. These interactions are lost upon disruption of ribosomes by puromycin. Polysomal lncRNAs are distinguished by a number of 5′ mRNA-like features, including capping and 5′UTR length. On the other hand, nonpolysomal “free cytoplasmic” lncRNAs have more conserved promoters and a wider range of expression across cell types. Exons of polysomal lncRNAs are depleted of endogenous retroviral insertions, suggesting a role for repetitive elements in lncRNA localization. Finally, we show that blocking of ribosomal elongation results in stabilization of many associated lncRNAs. Together these findings suggest that the ribosome is the default destination for the majority of cytoplasmic long noncoding RNAs and may play a role in their degradation.
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spelling ntu-10356/815042023-02-28T16:58:51Z Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells Carlevaro-Fita, Joana Rahim, Anisa Guigó, Roderic Johnson, Rory Vardy, Leah Karen Anne School of Biological Sciences Cytoplasm Transposable element Ribosome profiling Degradation Long noncoding RNA Ribosome Translation Recent footprinting studies have made the surprising observation that long noncoding RNAs (lncRNAs) physically interact with ribosomes. However, these findings remain controversial, and the overall proportion of cytoplasmic lncRNAs involved is unknown. Here we make a global, absolute estimate of the cytoplasmic and ribosome-associated population of stringently filtered lncRNAs in a human cell line using polysome profiling coupled to spike-in normalized microarray analysis. Fifty-four percent of expressed lncRNAs are detected in the cytoplasm. The majority of these (70%) have >50% of their cytoplasmic copies associated with polysomal fractions. These interactions are lost upon disruption of ribosomes by puromycin. Polysomal lncRNAs are distinguished by a number of 5′ mRNA-like features, including capping and 5′UTR length. On the other hand, nonpolysomal “free cytoplasmic” lncRNAs have more conserved promoters and a wider range of expression across cell types. Exons of polysomal lncRNAs are depleted of endogenous retroviral insertions, suggesting a role for repetitive elements in lncRNA localization. Finally, we show that blocking of ribosomal elongation results in stabilization of many associated lncRNAs. Together these findings suggest that the ribosome is the default destination for the majority of cytoplasmic long noncoding RNAs and may play a role in their degradation. ASTAR (Agency for Sci., Tech. and Research, S’pore) Published version 2016-06-27T09:00:29Z 2019-12-06T14:32:29Z 2016-06-27T09:00:29Z 2019-12-06T14:32:29Z 2016 Journal Article Carlevaro-Fita, J., Rahim, A., Guigó, R., Vardy, L. A., & Johnson, R. (2016). Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells. RNA, 22(6), 867-882. 1355-8382 https://hdl.handle.net/10356/81504 http://hdl.handle.net/10220/40809 10.1261/rna.053561.115 27090285 en RNA © 2016 Carlevaro-Fita et al. This article, published in RNA, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/. 16 p. application/pdf
spellingShingle Cytoplasm
Transposable element
Ribosome profiling
Degradation
Long noncoding RNA
Ribosome
Translation
Carlevaro-Fita, Joana
Rahim, Anisa
Guigó, Roderic
Johnson, Rory
Vardy, Leah Karen Anne
Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
title Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
title_full Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
title_fullStr Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
title_full_unstemmed Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
title_short Cytoplasmic long noncoding RNAs are frequently bound to and degraded at ribosomes in human cells
title_sort cytoplasmic long noncoding rnas are frequently bound to and degraded at ribosomes in human cells
topic Cytoplasm
Transposable element
Ribosome profiling
Degradation
Long noncoding RNA
Ribosome
Translation
url https://hdl.handle.net/10356/81504
http://hdl.handle.net/10220/40809
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