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Ribonomic Analysis of Human Pum1 Reveals cis-trans Conservation across Species despite Evolution of Diverse mRNA Target Sets
Open accessAbstract
PUF family proteins are among the best-characterized regulatory RNA-binding proteins in nonmammalian species, but relatively little is known about mRNA targets or functions of mammalian PUF proteins. In this study, we used ribonomic analysis to identify and analyze mRNAs associated with ribonucleoproteins containing an endogenous human PUF protein, Pum1. Pum1-associated mRNAs were highly enriched for genes encoding proteins that function in transcriptional regulation and cell cycle/proliferation, results consistent with the posttranscriptional RNA regulon model and the proposed ancestral functions of PUF proteins in stem cell biology. Analysis of 3' untranslated region sequences of Pum1-associated mRNAs revealed a core Pum1 consensus sequence, UGUAHAUA. Pum1 knockdown demonstrated that Pum1 enhances decay of associated mRNAs, and relocalization of Pum1 to stress granules suggested that Pum1 functions in repression of translation. This study is the first in vivo genome-wide mRNA target identification of a mammalian PUF protein and provides direct evidence that human PUF proteins regulate stability of associated mRNAs. Comparison of Pum1-associated mRNAs to mRNA targets of PUF proteins from Saccharomyces cerevisiae and Drosophila melanogaster demonstrates how a well-conserved RNA-binding domain and cognate binding sequence have been evolutionarily rewired to regulate the collective expression of different sets of functionally related genes.
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“motifs for the alternative splicing factorsRBFOX1, RBFOX2 and RBFOX3 (ref. 4) are conserved in introns downstream of alternative exons, whereas sites for the stability/translation factors PUM1 and PUM2 are most highly conserved in 3′ UTRs24,25”
From A compendium of RNA-binding motifs for decoding gene regulation (2013) · cites this paper as [25]
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A compendium of RNA-binding motifs for decoding gene regulation
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“In fact, several other cell cycle regulators have been identified as human PUM1 targets and are repressed through their mRNA 3′ UT”
BackgroundA Pumilio-induced RNA structure switch in p27-3′ UTR controls miR-221 and miR-222 accessibility
Kedde, M., van Kouwenhove, M., Zwart, W. T., Vrielink, J. A. F. O., Elkon, R., & Agami, R. (2010) · Nature Cell Biology · doi:10.1038/ncb2105 · Cited by 406
“Pumilio-1 (PUM1) is a ubiquitously expressed RBP that was shown to interact with p27-3′ UT”
BackgroundPARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data
Corcoran, D. L., Georgiev, S., Mukherjee, N., Gottwein, E., Skalsky, R. L., Keene, J. D., & Ohler, U. (2011) · Genome biology · doi:10.1186/gb-2011-12-8-r79 · Cited by 342
“The functions of Pumilio are widely studied in a variety of species, and its global RNA targeting properties has been examined across a large phylogeny [12-17].”
BackgroundSelf-citation
Metadata
- Authors
- Morris, A. R., Mukherjee, N., & Keene, J. D.
- Affiliations
- Duke Medical Center (US)
- Corresponding author
- Keene, Jack D.
- ORCID
- Mukherjee, Neelanjan
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2008-06-01
- Volume
- 28
- Issue
- 12
- Pages
- 4093-4103
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC2423135
- OpenAlex
- W2109821031
- Cited by
- 155
- References
- 62
- Citations by year
- 2026: 6 · 2025: 1 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 5 · 2020: 10 · 2019: 13 · 2018: 11 · 2017: 7 · 2016: 11 · 2015: 5 · 2014: 12 · 2013: 12 · 2012: 9
- FWCI
- 6.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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 › Developmental Biology and Gene Regulation
- Keywords
- PUM1, PUF proteins, mRNA stability, post-transcriptional regulation, 3' untranslated region, cis-regulatory sequences, stress granules, protein synthesis inhibition, ribonucleoprotein, Saccharomyces cerevisiae, Drosophila melanogaster, transcriptional regulation
- MeSH terms
- Animals, Drosophila melanogaster, HeLa Cells, Humans, Models, Biological, Ribosomes, RNA, Messenger, Saccharomyces cerevisiae, Species Specificity, Protein Biosynthesis, RNA-Binding Proteins, Conserved Sequence, Oxidative Stress, Evolution, Molecular, Oligonucleotide Array Sequence Analysis
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