IGF2BP3 Modulates the Interaction of Invasion-Associated Transcripts with RISC

Ennajdaoui, Hanane; Howard, Jonathan M.; Sterne-Weiler, Timothy; Jahanbani, Fereshteh; Coyne, Doyle J.; Uren, Philip J.; Dargyte, Marija; Katzman, Sol; Draper, Jolene M.; Wallace, Andrew; Cazarez, Oscar; Burns, Suzanne Perea; Qiao, Mu; Hinck, Lindsay; Smith, Andrew D.; Toloue, Masoud; Blencowe, Benjamin J.; Penalva, Luiz O. F.; Sanford, Jeremy R.

doi:10.1016/j.celrep.2016.04.083

Cited by 69 publications

(95 citation statements)

References 44 publications

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“…Sequestration into AGO2/ RISC-free mRNP granules may therefore be the principal mechanism of IMP3-mediated mRNA protection from let-7-dependent silencing. In contrast, in pancreatic ductal adenocarcinoma cells (PDACs), IMP3 was reported to compete with miRNAs for common binding sites in target mRNA 3 ′ UTRs but also promote association of mRNAs with AGO2/RISC, suggesting a function as a bimodal regulator of target mRNA stability (Ennajdaoui et al 2016). Taken together, these observations suggest that IMP1 and IMP3 may regulate mRNA stability by multiple mechanisms, including sequestration in RISC-free mRNP granules, protection from miRNA-dependent degradation by competing for common binding sites, and enhancement of degradation by recruitment of AGO2/RISC to target mRNAs.…”

Section: Mechanisms Of Actionmentioning

confidence: 99%

“…Cell context-specific events, such as the presence of other RBPs and miRNA expression repertoires that modulate IMP1 activity, may help determine whether IMP1 preferentially promotes polarity or migration. More recently, the loss of IMP3 was reported to reduce PDAC invasiveness (Ennajdaoui et al 2016). Numerous IMP3 targets related to invasiveness and implicated in focal adhesions, adherens junctions, actin cytoskeleton, and cell migration were identified by iCLIP in PDAC cells.…”

Section: Regulation Of Imp Expressionmentioning

confidence: 99%

“…2; Jonson et al 2014). However, IMP3 may further promote CSC development and maintenance by destabilizing mRNAs that encode proteins implicated in differentiation and/or tumor suppression based on the discovery that IMP3 can recruit AGO/RISC to some of its mRNA targets (Ennajdaoui et al 2016).…”

Section: Regulation Of Imp Expressionmentioning

confidence: 99%

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IMPs: an RNA-binding protein family that provides a link between stem cell maintenance in normal development and cancer

et al. 2016

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IMPs, also known as insulin-like growth factor 2 (IGF2) messenger RNA (mRNA)-binding proteins (IGF2BPs), are highly conserved oncofetal RNA-binding proteins (RBPs) that regulate RNA processing at several levels, including localization, translation, and stability. Three mammalian IMP paralogs (IMP1–3) have been identified that are expressed in most organs during embryogenesis, where they are believed to play an important role in cell migration, metabolism, and stem cell renewal. Whereas some IMP2 expression is retained in several adult mouse organs, IMP1 and IMP3 are either absent or expressed at very low levels in most tissues after birth. However, all three paralogs can be re-expressed upon malignant transformation and are found in a broad range of cancer types where their expression often correlates with poor prognosis. IMPs appear to resume their physiological functions in malignant cells, which not only contribute to tumor progression but participate in the establishment and maintenance of tumor cell hierarchies. This review summarizes our current understanding of the functions of IMPs during normal development and focuses on a series of recent observations that have provided new insight into how their physiological functions enable IMPs to play a potentially key role in cancer stem cell maintenance and tumor growth.

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Section: Mechanisms Of Actionmentioning

confidence: 99%

Section: Regulation Of Imp Expressionmentioning

confidence: 99%

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IMPs: an RNA-binding protein family that provides a link between stem cell maintenance in normal development and cancer

et al. 2016

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“…Notably, Chtf18 is the only conserved DNA methylation target gene that was identified in this Chapter, supporting a previous study that has demonstrated its conservation for DNA replication between yeast, flies and mammals (Berkowitz et al, 2008). Furthermore, Igf2bp3 is an important member of a critical upstream signalling pathway that drives cell proliferation (Ennajdaoui et al, 2016;Lederer et al, 2014, Chernoff, 1999. In particular, Igf2bp3 (Palanichamy et al, 2016;Schaeffer et al, 2010) and Ube2c (Bajaj et al, 2016;Chou et al, 2014;Shen et al, 2013;Shuliang et al, 2013) have been widely studied in various cancers, confirming their ability to promote cell proliferation.…”

Section: Discussionsupporting

confidence: 59%

DNA methylation and chromatin dynamics during postnatal cardiomyocyte maturation

Sim

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“…Despite their different methodologies, RIP and CLIP can produce complementary data when used to study the same RBPs under similar conditions (van der Brug et al 2008;Sanford et al 2009;Kershner and Kimble 2010;Jungkamp et al 2011;Mukherjee et al 2011;Brooks et al 2015;Hansen et al 2015;Ennajdaoui et al 2016;Prasad et al 2016;Uren et al 2016). Therefore, our goal has been to combine aspects of both techniques to produce a single procedure that quantifies RBP-RNA interactions at the whole-transcript level and at the binding site level.…”

Section: Introductionmentioning

confidence: 99%

Quantifying RNA binding sites transcriptome-wide using DO-RIP-seq

Nicholson

Friedersdorf

Keene

2016

RNA

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RNA-binding proteins (RBPs) and noncoding RNAs orchestrate post-transcriptional processes through the recognition of specific sites on targeted transcripts. Thus, understanding the connection between binding to specific sites and active regulation of the whole transcript is essential. Many immunoprecipitation techniques have been developed that identify either whole transcripts or binding sites of RBPs on each transcript using cell lysates. However, none of these methods simultaneously measures the strength of each binding site and quantifies binding to whole transcripts. In this study, we compare current procedures and present digestion optimized (DO)-RIP-seq, a simple method that locates and quantifies RBP binding sites using a continuous metric. We have used the RBP HuR/ELAVL1 to demonstrate that DO-RIP-seq can quantify HuR binding sites with high coverage across the entire human transcriptome, thereby generating metrics of relative RNA binding strength. We demonstrate that this quantitative enrichment of binding sites is proportional to the relative in vitro binding strength for these sites. In addition, we used DO-RIP-seq to quantify and compare HuR's binding to whole transcripts, thus allowing for seamless integration of binding site data with whole-transcript measurements. Finally, we demonstrate that DO-RIP-seq is useful for identifying functional mRNA target sets and binding sites where combinatorial interactions between HuR and AGOmicroRNAs regulate the fate of the transcripts. Our data indicate that DO-RIP-seq will be useful for quantifying RBP binding events that regulate dynamic biological processes.

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IGF2BP3 Modulates the Interaction of Invasion-Associated Transcripts with RISC

Cited by 69 publications

References 44 publications

IMPs: an RNA-binding protein family that provides a link between stem cell maintenance in normal development and cancer

IMPs: an RNA-binding protein family that provides a link between stem cell maintenance in normal development and cancer

DNA methylation and chromatin dynamics during postnatal cardiomyocyte maturation

Quantifying RNA binding sites transcriptome-wide using DO-RIP-seq

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