Cited by 188RNA Research and SplicingRNA and protein synthesis mechanismsRNA regulation and disease

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Systematic discovery of structural elements governing stability of mammalian messenger RNAs

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Goodarzi, Hani, Najafabadi, Hamed S., Oikonomou, Panos, Greco, Todd M., Fish, Lisa, Salavati, Reza, Cristea, Ileana M., Tavazoie, Saeed·2012·Nature

DOI 10.1038/nature11013PMC PMC3350620

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Abstract

Decoding post-transcriptional regulatory programs in RNA is a critical step towards the larger goal of developing predictive dynamical models of cellular behaviour. Despite recent efforts, the vast landscape of RNA regulatory elements remains largely uncharacterized. A long-standing obstacle is the contribution of local RNA secondary structure to the definition of interaction partners in a variety of regulatory contexts, including--but not limited to--transcript stability, alternative splicing and localization. There are many documented instances where the presence of a structural regulatory element dictates alternative splicing patterns (for example, human cardiac troponin T) or affects other aspects of RNA biology. Thus, a full characterization of post-transcriptional regulatory programs requires capturing information provided by both local secondary structures and the underlying sequence. Here we present a computational framework based on context-free grammars and mutual information that systematically explores the immense space of small structural elements and reveals motifs that are significantly informative of genome-wide measurements of RNA behaviour. By applying this framework to genome-wide human mRNA stability data, we reveal eight highly significant elements with substantial structural information, for the strongest of which we show a major role in global mRNA regulation. Through biochemistry, mass spectrometry and in vivo binding studies, we identified human HNRPA2B1 (heterogeneous nuclear ribonucleoprotein A2/B1, also known as HNRNPA2B1) as the key regulator that binds this element and stabilizes a large number of its target genes. We created a global post-transcriptional regulatory map based on the identity of the discovered linear and structural cis-regulatory elements, their regulatory interactions and their target pathways. This approach could also be used to reveal the structural elements that modulate other aspects of RNA behaviour.

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Additional file 10 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 11 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 5 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 2 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 9 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 3 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 8 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
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Additional file 7 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
Zhang, Y., Huang, W., Yuan, Y., Li, J., Wu, J., Yu, J., He, Y., Wei, Z., & Zhang, C. (2020) · Figshare · doi:10.6084/m9.figshare.12703725
Additional file 6 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
Zhang, Y., Huang, W., Yuan, Y., Li, J., Wu, J., Yu, J., He, Y., Wei, Z., & Zhang, C. (2020) · Figshare · doi:10.6084/m9.figshare.12703722
Additional file 1 of Long non-coding RNA H19 promotes colorectal cancer metastasis via binding to hnRNPA2B1
Zhang, Y., Huang, W., Yuan, Y., Li, J., Wu, J., Yu, J., He, Y., Wei, Z., & Zhang, C. (2020) · Figshare · doi:10.6084/m9.figshare.12703707
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Self-citation

Authors: Goodarzi, H., Najafabadi, H. S., Oikonomou, P., Greco, T. M., Fish, L., Salavati, R., Cristea, I. M., & Tavazoie, S.
Affiliations: Princeton University (US)
McGill University (CA)
Rockefeller University (US)
Corresponding author: Tavazoie, Saeed
ORCID: Goodarzi, Hani
Najafabadi, Hamed S.
Oikonomou, Panos
Greco, Todd M.
Fish, Lisa
Salavati, Reza
Cristea, Ileana M.
Tavazoie, Saeed
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-04-08
Volume: 485
Issue: 7397
Pages: 264-268
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11013
PMC: PMC3350620
OpenAlex: W2030581432
Cited by: 187
References: 26
Citations by year: 2026: 7 · 2025: 10 · 2024: 6 · 2023: 7 · 2022: 12 · 2021: 9 · 2020: 23 · 2019: 8 · 2018: 9 · 2017: 13 · 2016: 13 · 2015: 17 · 2014: 17 · 2013: 25 · 2012: 11
FWCI: 8.99
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health (DP1OD003787)
National Institute on Drug Abuse (DP1DA026192)
National Human Genome Research Institute (R01HG003219)
National Institute of General Medical Sciences (T32GM066699)
National Institute of Environmental Health Sciences (DP1ES022578)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
Keywords: mRNA secondary structure, RNA stability, post-transcriptional regulation, RNA-binding proteins, HNRNPA2B1, cis-regulatory elements, context-free grammars, mutual information, alternative splicing, transcript localization, structural motifs
MeSH terms: Algorithms, Animals, Breast Neoplasms, Humans, Nucleic Acid Conformation, RNA, Messenger, Time Factors, Transcription, Genetic, Genome, Human, Gene Expression Regulation, Neoplastic, 3' Untranslated Regions, Gene Expression Profiling, RNA Stability, Genomics, Heterogeneous-Nuclear Ribonucleoprotein Group A-B, RNA, Small Interfering, Cell Line, Tumor, Mice, Gene Knockdown Techniques, Nucleotide Motifs

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Systematic discovery of structural elements governing stability of mammalian messenger RNAs

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