Evolution of a tissue-specific splicing network

Taliaferro, J. Matthew; Alvarez, Nehemiah; Green, Edward; Blanchette, Marco; Rio, Donald C.

doi:10.1101/gad.2009011

Cited by 18 publications

(22 citation statements)

References 56 publications

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“…We investigated the effects that four Drosophila small RNA-related proteins-Dicer-1 (Dcr-1), Dicer-2 (Dcr-2), Ago-1, and Ago-2-had on pre-mRNA splicing patterns in Drosophila tissue culture cells by first using RNAi to knock down expression of each protein and then analyzing the resulting RNA by splice junction microarray (Blanchette et al 2005(Blanchette et al , 2009Taliaferro et al 2011). Importantly, RNAi knockdown of components of the RNAi pathway themselves was possible and efficient, as evidenced by knockdown efficiencies of >90% (Supplemental Fig.…”

Section: Resultsmentioning

confidence: 99%

Two new and distinct roles for Drosophila Argonaute-2 in the nucleus: alternative pre-mRNA splicing and transcriptional repression

et al. 2013

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Transcription and pre-mRNA alternative splicing are highly regulated processes that play major roles in modulating eukaryotic gene expression. It is increasingly apparent that other pathways of RNA metabolism, including small RNA biogenesis, can regulate these processes. However, a direct link between alternative premRNA splicing and small RNA pathways has remained elusive. Here we show that the small RNA pathway protein Argonaute-2 (Ago-2) regulates alternative pre-mRNA splicing patterns of specific transcripts in the Drosophila nucleus using genome-wide methods in conjunction with RNAi in cell culture and Ago-2 deletion or catalytic site mutations in Drosophila adults. Moreover, we show that nuclear Argonaute-2 binds to specific chromatin sites near gene promoters and negatively regulates the transcription of the Ago-2-associated target genes. These transcriptional target genes are also bound by Polycomb group (PcG) transcriptional repressor proteins and change during development, implying that Ago-2 may regulate Drosophila development. Importantly, both of these activities were independent of the catalytic activity of Ago-2, suggesting new roles for Ago-2 in the nucleus. Finally, we determined the nuclear RNA-binding profile of Ago-2, found it bound to several splicing target transcripts, and identified a G-rich RNA-binding site for Ago-2 that was enriched in these transcripts. These results suggest two new nuclear roles for Ago-2: one in pre-mRNA splicing and one in transcriptional repression.

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Section: Resultsmentioning

confidence: 99%

Two new and distinct roles for Drosophila Argonaute-2 in the nucleus: alternative pre-mRNA splicing and transcriptional repression

et al. 2013

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“…The complexity of the processing that occurs during the formation of a mature mRNA provides a basis for the multilayered regulation of gene expression. These regulatory networks correlate with the organizational complexity of a given organism and with the specialization of tissues such as the components of the central nervous system and the cardiac muscle (Maniatis and Tasic, 2002;Mendes Soares and Valcarcel, 2006;Taliaferro et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Functional coupling of transcription and splicing

Montes

Becerra

Sánchez-Álvarez

et al. 2012

Gene

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The tightly regulated process of precursor messenger RNA (pre-mRNA) alternative splicing is a key mechanism to increase the number and complexity of proteins encoded by the genome. Evidence gathered in recent years has established that transcription and splicing are physically and functionally coupled and that this coupling may be an essential aspect of the regulation of splicing and alternative splicing. Recent advances in our understanding of transcription and of splicing regulation have uncovered the multiple interactions between components from both types of machinery. These interactions help to explain the functional coupling of RNAPII transcription and pre-mRNA alternative splicing for efficient and regulated gene expression at the molecular level. Recent technological advances, in addition to novel cell and molecular biology approaches, have led to the development of new tools for addressing mechanistic questions to achieve an integrated and global understanding of the functional coupling of RNAPII transcription and pre-mRNA alternative splicing. Here, we review major milestones and insights into RNA polymerase II transcription and pre-mRNA alternative splicing as well as new concepts and challenges that have arisen from multiple genome-wide approaches and analyses at the single-cell resolution.

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“…Depending upon the resolution of the particular experimental analysis, regulatory inputs may be understood only at the level of functional (epistatic) gene interactions, or they may be understood much more completely, that is, at the level of direct interactions betweens specific TFs and their binding sites within CREs. Some of the same methods that are used in GRN analysis can be applied to various post-transcriptional regulatory networks that operate in embryonic cells, for example, splicing networks and miRNA networks (Hobert, 2006;Taliaferro et al, 2011;Gagan et al, 2012), and in the future it should be possible to integrate such networks with transcriptional GRNs.…”

mentioning

confidence: 99%

Encoding anatomy: Developmental gene regulatory networks and morphogenesis

Ettensohn

2013

Genesis

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A central challenge of developmental and evolutionary biology is to explain how anatomy is encoded in the genome. Anatomy emerges progressively during embryonic development, as a consequence of morphogenetic processes. The specialized properties of embryonic cells and tissues that drive morphogenesis, like other specialized properties of cells, arise as a consequence of differential gene expression. Recently, gene regulatory networks (GRNs) have proven to be powerful conceptual and experimental tools for analyzing the genetic control and evolution of developmental processes. A major current goal is to link these transcriptional networks directly to morphogenetic processes. This review highlights three experimental models (sea urchin skeletogenesis, ascidian notochord morphogenesis, and the formation of somatic muscles in Drosophila) that are currently being used to analyze the genetic control of anatomy by integrating information of several important kinds: (1) morphogenetic mechanisms at the molecular, cellular and tissue levels that are responsible for shaping a specific anatomical feature, (2) the underlying GRN circuitry deployed in the relevant cells, and (3) modifications to gene regulatory circuitry that have accompanied evolutionary changes in the anatomical feature.

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Evolution of a tissue-specific splicing network

Cited by 18 publications

References 56 publications

Two new and distinct roles for Drosophila Argonaute-2 in the nucleus: alternative pre-mRNA splicing and transcriptional repression

Two new and distinct roles for Drosophila Argonaute-2 in the nucleus: alternative pre-mRNA splicing and transcriptional repression

Functional coupling of transcription and splicing

Encoding anatomy: Developmental gene regulatory networks and morphogenesis

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