Spatial arrangement of an RNA zipcode identifies mRNAs under post-transcriptional control

Patel, Vivek; Mitra, Subhasish; Harris, Richard; Buxbaum, Adina R.; Lionnet, Timothée; Brenowitz, Michael; Girvin, Mark E.; Levy, Matthew; Almo, Steven C.; Singer, Robert H.; Chao, Jeffrey A.

doi:10.1101/gad.177428.111

Cited by 138 publications

(216 citation statements)

References 57 publications

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“…Understanding b-actin mRNA spatial regulation through ZBP1 has enabled a greater understanding of how mRNA localization can elicit significant control over cell dynamics. Whether other mRNA targets of ZBP1 act in a way similar to b-actin mRNA has yet to be fully determined, although there is recent evidence to support a conserved mechanism (Patel et al 2012). ZBP1 expression has implications for cancer prognosis (Wang et al 2004;Vainer et al 2008), neural regulation (Donnelly et al 2011;Welshhans and Bassell 2011), and development (Hansen et al 2004).…”

Section: B-actin Mrna Compartmentalizationmentioning

confidence: 99%

β-Actin mRNA compartmentalization enhances focal adhesion stability and directs cell migration

Wells²,

et al. 2012

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Directed cell motility is at the basis of biological phenomena such as development, wound healing, and metastasis. It has been shown that substrate attachments mediate motility by coupling the cell's cytoskeleton with force generation. However, it has been unclear how the persistence of cell directionality is facilitated. We show that mRNA localization plays an important role in this process, but the mechanism of action is still unknown. In this study, we show that the zipcode-binding protein 1 transports b-actin mRNA to the focal adhesion compartment, where it dwells for minutes, suggesting a means for associating its localization with motility through the formation of stable connections between adhesions and newly synthesized actin filaments. In order to demonstrate this, we developed an approach for assessing the functional consequences of b-actin mRNA and protein localization by tethering the mRNA to a specific location-in this case, the focal adhesion complex. This approach will have a significant impact on cell biology because it is now possible to forcibly direct any mRNA and its cognate protein to specific locations in the cell. This will reveal the importance of localized protein translation on various cellular processes.

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Section: B-actin Mrna Compartmentalizationmentioning

confidence: 99%

β-Actin mRNA compartmentalization enhances focal adhesion stability and directs cell migration

Wells²,

et al. 2012

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“…Cis-acting elements are typically in the 3 0 untranslated region (UTR), where hindrance with translation is unlikely, and generally form secondary structures including stem loops, hairpins and bulges. [43][44][45][46] Alternative splicing of the mRNA in the nucleus can adjust these elements, resulting in unique RNP compositions and ultimately different outcomes for the mRNA. 47,48 The prevailing model of localization suggests that newly formed RNPs are recognized by other factors, such as proteins linking cargo to molecular motors in the case of transport, and become localized.…”

Section: Mechanisms Of Mrna Localizationmentioning

confidence: 99%

mRNA localization in theDrosophilagermline

Weil

2014

RNA Biology

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“…Although the molecular mechanisms underlying specific recognition of zipcodes by RNA-binding proteins have long been elusive, recent structural studies have revealed requirements for highly specific motifs and/or structures. For example, a 54-nt sequence required for the targeting of -actin mRNA in fibroblasts has been shown to contain a bipartite element comprising two RNA motifs recognized by the RNA-binding protein Zbp1 (Chao et al, 2010;Patel et al, 2012). The RNA binding protein Egalitarian, by contrast, does not recognize a specific sequence, but rather the atypical AЈ-form helices formed by the 44-nt localization element of Drosophila fs(1)K10 transcripts .…”

Section: Cis-regulatory Elements and Trans-acting Factorsmentioning

confidence: 99%

Principles and roles of mRNA localization in animal development

2012

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SummaryIntracellular targeting of mRNAs has long been recognized as a means to produce proteins locally, but has only recently emerged as a prevalent mechanism used by a wide variety of polarized cell types. Localization of mRNA molecules within the cytoplasm provides a basis for cell polarization, thus underlying developmental processes such as asymmetric cell division, cell migration, neuronal maturation and embryonic patterning. In this review, we describe and discuss recent advances in our understanding of both the regulation and functions of RNA localization during animal development.Key words: RNA localization, RNA transport, Local translation, Cell polarity, Post-transcriptional gene regulation Introduction Establishment of cell polarity is crucial for the execution of developmental programmes governing key processes, including specification of cell fates, individual or collective cell movements and specialization of somatic cell types. Cell polarization depends on the asymmetric segregation of organelles and various molecules within the cell. Polarized accumulation of RNA molecules was first visualized nearly 30 years ago, when -actin mRNA was found to be asymmetrically localized within ascidian eggs and embryos (Jeffery et al., 1983). Following this, the discovery of the first localized maternal mRNAs in Xenopus (Rebagliati et al., 1985) and Drosophila oocytes (Frigerio et al., 1986;Berleth et al., 1988) provided evidence for the earlier proposal that localized RNA determinants could be responsible for early embryonic patterning (Kandler-Singer and Kalthoff, 1976). mRNAs were soon found to be asymmetrically distributed within differentiated somatic cells, such as fibroblasts (Lawrence and Singer, 1986), oligodendrocytes (Trapp et al., 1987) and neurons (Garner et al., 1988), and to colocalize with their encoded proteins, establishing intracellular transport of mRNAs as a potential mechanism used to target the production of selected proteins to discrete sites.Significant improvements in RNA detection methods led to the identification of a growing number of localized mRNAs. Still, in the early 2000s, the set of described targeted mRNAs was limited to ~100 (reviewed by Bashirullah et al., 1998;Palacios and St Johnston, 2001) and the process of mRNA localization was thought to be restricted to specific cell types. However, recent genome-wide analyses (see Table 1) have changed this view dramatically, and strongly suggest that subcellular targeting of mRNAs is a prevalent mechanism used by polarized cells to establish functionally distinct compartments (Fig. 1). Particularly striking was the discovery that >70% of the 2314 expressed transcripts analysed in a highresolution in situ hybridization screen were subcellularly localized in Drosophila embryos (Lécuyer et al., 2007). Moreover, hundreds to thousands of mRNAs have been detected in cellular compartments as diverse as the mitotic apparatus (Blower et al., 2007;Sharp et al., 2011), pseudopodia (Mili et al., 2008), dendrites (Moccia et al., 2003;Poon et a...

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Spatial arrangement of an RNA zipcode identifies mRNAs under post-transcriptional control

Cited by 138 publications

References 57 publications

β-Actin mRNA compartmentalization enhances focal adhesion stability and directs cell migration

β-Actin mRNA compartmentalization enhances focal adhesion stability and directs cell migration

mRNA localization in theDrosophilagermline

Principles and roles of mRNA localization in animal development

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