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From parts lists to functional significance—RNA–protein interactions in gene regulation

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Abstract Hundreds of canonical RNA binding proteins facilitate diverse and essential RNA processing steps in cells forming a central regulatory point in gene expression. However, recent discoveries including the identification of a large number of noncanonical proteins bound to RNA have changed our view on RNA–protein interactions merely as necessary steps in RNA biogenesis. As the list of proteins interacting with RNA has expanded, so has the scope of regulation through RNA–protein interactions. In addition to facilitating RNA metabolism, RNA binding proteins help to form subcellular structures and membraneless organelles, and provide means to recruit components of macromolecular complexes to their sites of action. Moreover, RNA–protein interactions are not static in cells but the ribonucleoprotein (RNP) complexes are highly dynamic in response to cellular cues. The identification of novel proteins in complex with RNA and ways cells use these interactions to control cellular functions continues to broaden the scope of RNA regulation in cells and the current challenge is to move from cataloguing the components of RNPs into assigning them functions. This will not only facilitate our understanding of cellular homeostasis but may bring in key insights into human disease conditions where RNP components play a central role. This review brings together the classical view of regulation accomplished through RNA–protein interactions with the novel insights gained from the identification of RNA binding interactomes. We discuss the challenges in combining molecular mechanism with cellular functions on the journey towards a comprehensive understanding of the regulatory functions of RNA–protein interactions in cells. This article is categorized under: RNA Interactions with Proteins and Other Molecules > Protein–RNA Interactions: Functional Implications aRNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes RNA Interactions with Proteins and Other Molecules > Protein–RNA Recognition
RNA binding proteins facilitate each step of RNA biogenesis of both coding and noncoding RNAs in cells. They also play roles beyond these processes by forming different types of subcellular organelles through their interactions with RNA. The RNA biogenesis steps have been drawn to occur in a step‐wise manner for the purpose of visual presentation. However, they often take place simultaneously and/or co‐transcriptionally in cells
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The choice of RIC data normalization determines our perspective on RBPs. A representative RIC dataset from yeast was normalized to either a non‐crosslinked (noCL) control (left panel), or to cellular protein abundances (right panel). Proteins annotated with a classical RBD (RRM, KH, dsRNA, Piwi, DEAD, Pumilio, CSD, zinc finger‐CCCH) or any of the nonclassical RBDs identified in the initial human interactome or with the RBDmap approach (Castello et al., , ) are highlighted in black and turquoise, respectively. Normalization of RIC data to a non‐crosslinked control will yield the RNA's view of the RNA–protein interaction landscape (ochre). The normalization to protein abundances reveals the relative RNA binding activity of RNA interactors identified in the experiment (black). When combined, these viewpoints reflect the richness and the complexity of the RNA–protein interaction landscape
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Many modes of RNA binding through RBDs and other protein domains. Common canonical (yellow) and major novel (green) RNA binding domains or protein regions discussed in this review
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“Functional RNAomics” integrating sequencing, structural and molecular data with in vivo models will enable the comprehensive understanding of the functional significance of RNA regulation at the cellular and organism level and may reveal key insights into underlying mechanisms of human disease
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RNA Interactions with Proteins and Other Molecules > Protein–RNA Recognition
RNA Interactions with Proteins and Other Molecules > RNA–Protein Complexes
RNA Interactions with Proteins and Other Molecules > Protein–RNA Interactions: Functional Implications

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