Activity-dependent polyadenylation in neurons

Du, Ling; Richter, Joel D.

doi:10.1261/rna.2870505

Cited by 84 publications

(97 citation statements)

References 34 publications

(49 reference statements)

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“…Whole-cell recordings of visual responses and spontaneous bursting activity in tectal neurons in the intact animal demonstrate that CPEB1 function is required for the integration of neurons into the visual circuit. The results support a model in which synaptic activity leads to phosphorylation of CPEB and translational derepression of target mRNAs (18,19,24,35). The newly translated proteins then act as effectors to control experience-dependent modifications of dendritic arbor structure, synaptic connectivity, and ultimately the function and plasticity of the developing circuit.…”

Section: Discussionsupporting

confidence: 80%

“…About 7% of brain mRNAs are estimated to be targets of CPEB1, although only a relatively small number have been confirmed experimentally (24). Potential mRNA targets include key plasticity genes, such as ␣CaMKII (18,25), BDNF (24), tPA (37), engrailed1 (38), Homer (18), and insulin-receptor substrate p53 (11).…”

Section: Discussionmentioning

confidence: 99%

“…Potential mRNA targets include key plasticity genes, such as ␣CaMKII (18,25), BDNF (24), tPA (37), engrailed1 (38), Homer (18), and insulin-receptor substrate p53 (11). Proteins from these mRNAs, plus many identified in a recent screen of CPE-containing mRNAs (24), are capable of altering synaptic strength and neuronal structure. Nevertheless, it is unlikely that the effects of CPEB1 manipulations that we document here can be attributed to misregulation of a single CPEB mRNA target.…”

Section: Discussionmentioning

confidence: 99%

“…Because ␣CaMKII both activates CPEB1 and is also a downstream product of CPEB1 activity, ␣CaMKII may act in a feedback loop where synaptic input that activates ␣CaMKII can also derepress CPEB-mediated inhibition of ␣CaMKII synthesis (35). Therefore CPEB1-mediated control of ␣CaMKII synthesis alone is likely to have both immediate and long-lasting effects on functional and structural plasticity, as well as subsequent regulation of CPEB1, which likely work in concert with the other CPEB1 target mRNAs that are associated with synaptic and morphological plasticity (24).…”

Section: Discussionmentioning

confidence: 99%

“…The development of the dendritic arbor structure and maturation of tectal cell synaptic physiology progress coordinately and are governed by molecular pathways that include numerous proteins, such as ␣CaMKII (22) and brain-derived neurotrophic factor (BDNF) (23). Interestingly, the mRNA of both ␣CaMKII and BDNF are targets of CPEB1 (18,24,25), suggesting that CPEB may mediate aspects of activity-dependent visual system development. Indeed, studies in vivo have demonstrated that brief light exposure delivered to dark-reared rats produced CPEBdependent increases in ␣CaMKII mRNA polyadenylation and protein synthesis that required NMDA receptor signaling (18,25).…”

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confidence: 99%

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The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo

Bestman

Cline

2008

Proc. Natl. Acad. Sci. U.S.A.

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Visual system development requires experience-dependent mechanisms that regulate neuronal structure and function, including dendritic arbor growth, synapse formation, and stabilization. Although RNA binding proteins have been shown to affect some forms of synaptic plasticity in adult animals, their role in the development of neuronal structure and functional circuitry is not clear. Using two-photon time-lapse in vivo imaging and electrophysiology combined with morpholino-mediated knockdown and expression of functional deletion mutants, we demonstrate that the mRNA binding protein, cytoplasmic polyadenylation element binding protein1 (CPEB1), affects experience-dependent neuronal development and circuit formation in the visual system of Xenopus laevis. These data indicate that sensory experience controls circuit development by regulating translational activity of mRNAs.circuit integration ͉ experience-dependent plasticity ͉ in vivo imaging ͉ visual system ͉ whole-cell recording D uring CNS development, neuronal structure, synaptic connections, and circuit functions change in response to sensory input. Although the regulation of mRNA translation and new protein synthesis have been implicated in some forms of neuronal plasticity in adult animals (1, 2), their role in experience-dependent sensory system plasticity has not been addressed (3). In the brain, the translation of many mRNAs is regulated by their association with ribonucleoprotein (RNP) granules, which are composed of core RNA binding proteins, translational machinery, and mRNAs (4). RNA binding proteins package specific mRNAs within RNP granules, regulate their transport into dendrites, and in principle, could temporally and spatially govern their translation in response to synaptic activity (4). Because of these features, mRNA binding proteins are in a unique position to control developmental events through the coordinated translation of a functionally related cohort of mRNAs (5, 6). Indeed, local protein synthesis affords neurons the ability to stabilize changes in synaptic connections and alter neuronal output (7). Recent studies indicate that cytoplasmic polyadenylation element binding protein 1 (CPEB1) is among a handful of RNA binding proteins that regulate dendritic protein synthesis and synaptic plasticity in vitro (8). Although studies in mutant mice implicate CPEB1 in some forms of synaptic and spine plasticity and in memory extinction (9-11), no studies have examined the potential role of CPEB1 in dendritic arbor development, experience-dependent structural plasticity, or the integration of neurons into a functional circuit in an intact animal.CPEB1 (Orb in D. melanogaster) is a member of an evolutionarily conserved family of RNA binding proteins that is expressed in the brain (in vertebrates, CPEB1-4). While all members are defined by the presence of RNA recognition motifs in their carboxy-terminals, CPEB1 is the only member that targets mRNAs containing cytoplasmic polyadenylation elements (CPEs) in their 3Ј untranslated regions (12). Origina...

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Section: Discussionsupporting

confidence: 80%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo

Bestman

Cline

2008

Proc. Natl. Acad. Sci. U.S.A.

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Specificity factors in cytoplasmic polyadenylation

2013

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Poly(A) tail elongation after export of an messenger RNA (mRNA) to the cytoplasm is called cytoplasmic polyadenylation. It was first discovered in oocytes and embryos, where it has roles in meiosis and development. In recent years, however, has been implicated in many other processes, including synaptic plasticity and mitosis. This review aims to introduce cytoplasmic polyadenylation with an emphasis on the factors and elements mediating this process for different mRNAs and in different animal species. We will discuss the RNA sequence elements mediating cytoplasmic polyadenylation in the 3′ untranslated regions of mRNAs, including the CPE, MBE, TCS, eCPE, and C-CPE. In addition to describing the role of general polyadenylation factors, we discuss the specific RNA binding protein families associated with cytoplasmic polyadenylation elements, including CPEB (CPEB1, CPEB2, CPEB3, and CPEB4), Pumilio (PUM2), Musashi (MSI1, MSI2), zygote arrest (ZAR2), ELAV like proteins (ELAVL1, HuR), poly(C) binding proteins (PCBP2, αCP2, hnRNP-E2), and Bicaudal C (BICC1). Some emerging themes in cytoplasmic polyadenylation will be highlighted. To facilitate understanding for those working in different organisms and fields, particularly those who are analyzing high throughput data, HUGO gene nomenclature for the human orthologs is used throughout. Where human orthologs have not been clearly identified, reference is made to protein families identified in man. © 2013 John Wiley & Sons, Ltd.

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Tales around the clock: Poly(A) tails in circadian gene expression

Beta

Balatsos

2018

WIREs RNA

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Circadian rhythms are ubiquitous time-keeping processes in eukaryotes with a period of ~24 hr. Light is perhaps the main environmental cue (zeitgeber) that affects several aspects of physiology and behaviour, such as sleep/wake cycles, orientation of birds and bees, and leaf movements in plants. Temperature can serve as the main zeitgeber in the absence of light cycles, even though it does not lead to rhythmicity through the same mechanism as light. Additional cues include feeding patterns, humidity, and social rhythms. At the molecular level, a master oscillator orchestrates circadian rhythms and organizes molecular clocks located in most cells. The generation of the 24 hr molecular clock is based on transcriptional regulation, as it drives intrinsic rhythmic changes based on interlocked transcription/translation feedback loops that synchronize expression of genes. Thus, processes and factors that determine rhythmic gene expression are important to understand circadian rhythms. Among these, the poly(A) tails of RNAs play key roles in their stability, translational efficiency and degradation. In this article, we summarize current knowledge and discuss perspectives on the role and significance of poly(A) tails and associating factors in the context of the circadian clock. This article is categorized under: RNA Turnover and Surveillance > Regulation of RNA Stability RNA Processing > 3' End Processing.

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Activity-dependent polyadenylation in neurons

Cited by 84 publications

References 34 publications

The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo

The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo

Specificity factors in cytoplasmic polyadenylation

Tales around the clock: Poly(A) tails in circadian gene expression

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