Cytoplasmic Polyadenylation Element Binding Protein-Dependent Protein Synthesis Is Regulated by Calcium/Calmodulin-Dependent Protein Kinase II

Atkins, Coleen M.; Nozaki, Naohito; Shigeri, Yasushi; Soderling, Thomas R.

doi:10.1523/jneurosci.0854-04.2004

Cited by 137 publications

(135 citation statements)

References 54 publications

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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%

“…Increasing or decreasing CaMKII activity affects synaptic plasticity and dendritic-arbor development of neurons in the X. laevis optic tectum (32) and mammalian systems, where it is also required for learning and memory (40). CaMKII phosphorylates CPEB1 in response to NMDA receptor activity (19) and its own synthesis increases following plasticity-inducing stimuli (41), NMDA receptor activation, and CPEB1 activation (18). 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).…”

Section: Discussionmentioning

confidence: 99%

“…This activity-dependent dendritic growth operates by an NMDA receptordependent mechanism (21). Although NMDA receptor signaling and downstream kinase activity increased CPEB-dependent mRNA polyadenylation and protein synthesis in the rodent visual system (18,25) and hippocampal neurons (17,19), CPEB1 has not yet been implicated in experience-dependent structural plasticity.…”

Section: Delcpeb and Rbdcpeb Expression Blocks Experience-dependentmentioning

confidence: 99%

“…Originally discovered in Xenopus laevis oocytes, CPEB1 binds CPE-containing mRNAs, regulates their microtubule-dependent dendritic trafficking, and represses their translation (13). Unlike vertebrate CPEB3 and 4, ApCPEB in Aplysia (14,15), or Drosophila Orb2 (16), translational repression by CPEB1 is relieved by phosphorylation by either aurora kinase (17,18) or calcium/calmodulin-dependent kinase II (CaMKII) (19), following stimulation by progesterone in oocytes or glutamatergic synaptic activity in neurons. Phosphorylation of CPEB1 initiates a biochemical cascade that culminates in polyadenylation of the CPEB1-bound mRNAs and their translational derepression (13).…”

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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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: Delcpeb and Rbdcpeb Expression Blocks Experience-dependentmentioning

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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“…In these cells, transcripts are sequestered in a complex that prevents them from associating with translation initiation factors. CaMKII phosphorylates a member of the complex, allowing the transcript to be polyadenylated and translated (Atkins et al, 2004;reviewed in Jones, 2007). In Drosophila, polyadenylation and translation of bicoid does not occur in activated eggs of flies mutant for sra, the CaN regulator (see above; Horner et al, 2006).…”

Section: Maternal Transcript Translationmentioning

confidence: 99%

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

Horner

Wolfner

2008

Developmental Dynamics

181

177

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The transition from mature oocyte to developing embryo requires a coordinated series of events, collectively known as egg activation. Egg activation includes changes to egg coverings to prevent polyspermy, release of oocyte meiotic arrest, generation of haploid female and male pronuclei, changes in maternal mRNAs and protein populations, and cytoskeletal rearrangements. In many animals, egg activation is triggered by fertilization, which increases intracellular calcium within the oocyte and thereby regulates molecular events of egg activation. In other animals, fertilization-independent external signals, including mechanical stimulation of eggs and/or changes in ionic milieu, trigger activation. Recent studies have clarified the upstream portion of pathways leading to eggshell changes and cell cycle resumption and have identified activation-induced changes in maternal mRNA and protein profiles that can identify molecular players in the downstream events of egg activation. We review signals that trigger activation and how they link to subsequent molecular events of egg activation. Developmental Dynamics 237:527-544, 2008.

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RNA transport and localized protein synthesis in neurological disorders and neural repair

Wang

Niekerk

Willis

et al. 2007

Developmental Neurobiology

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Neural cells are able to finely tune gene expression through post-transcriptional mechanisms. Localization of mRNAs to subcellular regions has been detected in neurons, oligodendrocytes, and astrocytes providing these domains with a locally renewable source of proteins. Protein synthesis in dendrites has most frequently been associated with synaptic plasticity, while axonally synthesized proteins appear to facilitate pathfinding and injury responses. For oligodendrocytes, mRNAs encoding several proteins for myelin formation are locally generated suggesting that this mechanism assists in myelination. Astrocytic processes have not been well studied but localization of GFAP mRNA has been demonstrated. Both RNA transport and localized translation are regulated processes. RNA transport appears to be highly selective and, at least in part, the destiny of individual mRNAs is determined in the nucleus. RNA-protein and protein-protein interactions determine which mRNAs are targeted to subcellular regions. Several RNA binding proteins that drive mRNA localization have also been shown to repress translation during transport. Activity of the translational machinery is also regulated in distal neural cell processes. Clinically, disruption of mRNA localization and/or localized mRNA translation may contribute to pathophysiology of fragile X mental retardation and spinal muscular atrophy. Axonal injury has been shown to activate localized protein synthesis, providing both a means to initiate regeneration and retrogradely signal injury to the cell body. Decreased capacity to transport mRNAs and translational machinery into distal processes could jeopardize the ability to respond to injury or local stimuli within axons and dendrites.

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Cytoplasmic Polyadenylation Element Binding Protein-Dependent Protein Synthesis Is Regulated by Calcium/Calmodulin-Dependent Protein Kinase II

Cited by 137 publications

References 54 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

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

RNA transport and localized protein synthesis in neurological disorders and neural repair

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