Extensive Association of Functionally and Cytotopically Related mRNAs with Puf Family RNA-Binding Proteins in Yeast

By André P. Gerber, Daniel Herschlag, Patrick O. Brown. PLoS Biology, 2004

698 citations recorded by the source corpus.

Genes encoding RNA-binding proteins are diverse and abundant in eukaryotic genomes. Although some have been shown to have roles in post-transcriptional regulation of the expression of specific genes, few of these proteins have been studied systematically. We have used an affinity tag to isolate each of the five members of the Puf family of RNA-binding proteins in Saccharomyces cerevisiae and DNA microarrays to comprehensively identify the associated mRNAs. Distinct groups of 40–220 different mRNAs with striking common themes in the functions and subcellular localization of the proteins they encode are associated with each of the five Puf proteins: Puf3p binds nearly exclusively to cytoplasmic mRNAs that encode mitochondrial proteins; Puf1p and Puf2p interact preferentially with mRNAs encoding membrane-associated proteins; Puf4p preferentially binds mRNAs encoding nucleolar ribosomal RNA-processing factors; and Puf5p is associated with mRNAs encoding chromatin modifiers and components of the spindle pole body. We identified distinct sequence motifs in the 3′-untranslated regions of the mRNAs bound by Puf3p, Puf4p, and Puf5p. Three-hybrid assays confirmed the role of these motifs in specific RNA–protein interactions in vivo. The results suggest that combinatorial tagging of transcripts by specific RNA-binding proteins may be a general mechanism for coordinated control of the localization, translation, and decay of mRNAs and thus an integral part of the global gene expression program.

Subfields: Molecular Biology

View Paper: https://www.semanticscholar.org/paper/420271222d3206ef94fdee962e8123484a32e3ad

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Citations in the corpus

RIP-Chip: the isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts (2006, methodology): “It may also be possible to further reduce background in a RIP-Chip assay by the use of tandem affinity purified (TAP) tag”
RNA‐binding proteins and post‐transcriptional gene regulation (2008, positive): “been successfully used to identify RNAs that associate with PUF proteins in Saccharomyces cerevisiae [23].”
A universal framework for regulatory element discovery across all genomes and data types. (2007, background): “For example, the 3′UTR motif in Figure 3 that matches the binding site for Puf3, an mRNA degradation factor in yeast (Olivas and Parker, 2000), is over-represented within two clusters enriched with mitochondrial ribosomal genes, consistent with (Gerber et al., 2004).”
The mathematics of tanning (2009, neutral): “Transcript stability is often regulated by specific interactions between cis-elements in the 3' untranslated region (UTR) of mRNAs and hundreds of different RNA binding proteins (RBPs) in the cell [41,42].”
Regulation of Translation Initiation in Eukaryotes: Mechanisms and Biological Targets (2009, positive): “The precedents for coordinate regulation of classes of mRNAs at the translational level have already been documented in yeast via Puf RNA-binding proteins (Gerber et al., 2004) and in mammalian systems where the coordinately expressed mRNAs were called “RNA operons” (reviewed in Keene, 2007).”
RNA regulons: coordination of post-transcriptional events (2007, background): “cerevisiae and found that each binds a distinct subpopulation of mRNAs that encode proteins with related function”
Predicting RNA-Protein Interactions Using Only Sequence Information (2011, methodology): “Currently, two basic types of information regarding RNA-protein interaction partners are widely available: i) experimentally-deter-mined structures of RNA-protein complexes, available in primary resources such as the PDB [26] and NDB [41], and secondary resources such as PRIDB [34] and BIPA [42]; an”
Diverse RNA-Binding Proteins Interact with Functionally Related Sets of RNAs, Suggesting an Extensive Regulatory System (2008, background): “To identify RNAs associated with each putative RBP, Cterminal tandem affinity purification (TAP)-tagged proteins, expressed under control of their native promoters, were affinity purified from whole-cell extracts of cultures grown to mid-log phase in rich medium [14,26,43].”
PARalyzer: definition of RNA binding sites from PAR-CLIP short-read sequence data (2011, background): “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].”
Inaugural Article: Three-dimensional tracking of single mRNA particles in Saccharomyces cerevisiae using a double-helix point spread function (2010, neutral): “Indeed specific subcellular localization may be a genetically encoded feature of the expression program of most, and perhaps all, mRNAs in complex organisms (29, 30).”
Genome regulation by long noncoding RNAs (2012, methodology): “These studies employ protein immunoprecipitation followed by microarray or deep-sequencing to enumerate all RNAs associated with a protein complex of interest (RIPseq) (108) (49, 109); often times crosslinking is performed to trap the relevant interactions in living cells (CLIP-seq) (110).”