Activation of a Tyrosine Kinase-MAPK Cascade Enhances the Induction of Long-Term Synaptic Facilitation and Long-Term Memory in Aplysia

Purcell, Angela L.; Sharma, Shiv K.; Bagnall, Martha W.; Sutton, Michael A.; Carew, Thomas

doi:10.1016/s0896-6273(03)00030-8

Cited by 116 publications

(114 citation statements)

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“…Interestingly, the defect in capture of LTP was more pronounced in these mutant mice than in another strain in which the ablation of BDNF was restricted only to CA1 pyramidal cells . Based on these results we proposed that the presynaptic release of BDNF into the synaptic cleft after tetanic stimulation may participate in the post-synaptic tagging of the synapse through activation of TrkB receptors , perhaps by promoting local protein synthesis (Aakalu et al, 2001;Purcell et al, 2003). This idea, which could be indeed considered a specific mechanisms of the general view of regulation of local protein synthesis as substrate for synaptic tagging proposed above, has been further developed by Lu and colleagues in a recent review (Lu et al, 2007).…”

Section: Accepted Manuscriptmentioning

confidence: 89%

Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later

Barco

Armentia

Alarcón

2008

Neuroscience & Biobehavioral Reviews

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Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited ten years later, Neuroscience and Biobehavioral Reviews (2008Reviews ( ), doi:10.1016Reviews ( /j.neubiorev.2008 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.A c c e p t e d m a n u s c r i p t A c c e p t e d m a n u s c r i p tThe STC hypothesis revisited 2 Abstract A decade ago, the synaptic tagging hypothesis was proposed to explain how newly synthesized plasticity products can be specifically targeted to active synapses. A growing number of studies have validated the seminal findings that gave rise to this model, as well as contributed to unveil and expand the range of mechanisms underlying late-associativity and neuronal computation.Here, we will review what it was learnt during this past decade regarding the cellular and molecular mechanisms underlying synaptic tagging and synaptic capture. The accumulated experimental evidence has widened the theoretical framework set by the synaptic tagging and capture (STC) model and introduced concepts that were originally considered part of alternative models for explaining synapse-specific LTP. As a result, we believe that the STC model, now improved and expanded with these new ideas and concepts, still represents the most compelling hypothesis to explain late-associativity in synapse-specific plasticity processes. We will also discuss the impact of this model in our view of the integrative capability of neurons and associative learning. wordsKeywords: synaptic plasticity; LTP; associative learning; neuronal computation; synaptic tagging; synaptic capture; metaplasticity A c c e p t e d m a n u s c r i p tThe STC hypothesis revisited 3 Contents

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Section: Accepted Manuscriptmentioning

confidence: 89%

Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later

Barco

Armentia

Alarcón

2008

Neuroscience & Biobehavioral Reviews

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“…Newly released sensorin after tetanus plus 5-HT activates and translocates MAPK Phosphorylation (activation) and translocation of p42/44 MAPK into the nuclei of sensory neurons is critical for nonassociative LTF Purcell et al, 2003;Hu et al, 2004aHu et al, , 2006Sharma et al, 2006). The release of the newly synthesized sensorin after five applications of 5-HT binds to autoreceptors, leading to the activation and translocation of the MAPK (Hu et al, 2004a(Hu et al, , 2006.…”

Section: Both Pka and Pkc Activities Regulate The Secretion Of Newly mentioning

confidence: 99%

“…LTF accompanied by structural plasticity requires new gene and protein expression (Bailey et al, 1992) mediated by the timely activation of phosphoinosotide 3-kinase (PI3K), protein kinase A (PKA), and mitogen-activated protein kinase (MAPK) in sensory neurons (Greenberg et al, 1987;Sweatt and Kandel, 1989;Nazif et al, 1991;Schacher et al, 1993;Martin et al, 1997;Michael et al, 1998;Muller and Carew, 1998;Purcell et al, 2003;Udo et al, 2005;Hu et al, 2006). The kinases phosphorylate both local cytoplasmic substrates (Schuster et al, 1985;Bailey et al, 1997;Martin et al, 1997;Michael et al, 1998;Angers et al, 2002;Liu et al, 2004) and transcription factors in the sensory neurons (Dash et al, 1990;Bacskai et al, 1993;Alberini et al, 1994;Martin et al, 1997;Bartsch et al, 1998;Yamamoto et al, 1999;Purcell et al, 2003). Protein kinase C (PKC) activity is enhanced by 5-HT (Sacktor and Schwartz, 1990;Sossin and Schwartz, 1992) and participates in both short-and intermediate-term facilitation (ITF) (Sugita et al, 1992(Sugita et al, , 1997Wu et al, 1995;Sutton and Carew, 2000;Manseau et al, 2001;Sutton et al, 2004), but its role in nonassociative LTF is not clear (Sossin et al, 1994;Wu et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

Protein Kinase C Regulates Local Synthesis and Secretion of a Neuropeptide Required for Activity-Dependent Long-Term Synaptic Plasticity

Chen²,

Schacher³

2007

J. Neurosci.

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Long-term facilitation (LTF) of sensory neuron synapses inAplysia is produced by either nonassociative or associative stimuli. Nonassociative LTF can be produced by five spaced applications of serotonin (5-HT) and requires a phosphoinosotide 3-kinase (PI3K)-dependent and rapamycin-sensitive increase in the local synthesis of the sensory neuron neuropeptide sensorin and a protein kinase A (PKA)-dependent increase in the secretion of the newly synthesized sensorin. We report here that associative LTF produced by a single pairing of a brief tetanus with one application of 5-HT requires a rapid protein kinase C (PKC)-dependent and rapamycin-sensitive increase in local sensorin synthesis. This rapid increase in sensorin synthesis does not require PI3K activity or the presence of the sensory neuron cell body but does require the presence of the motor neuron. The secretion of newly synthesized sensorin by 2 h after stimulation requires both PKA and PKC activities to produce associative LTF because incubation with exogenous anti-sensorin antibody or the kinase inhibitors after tetanus plus 5-HT blocked LTF. The secreted sensorin leads to phosphorylation and translocation of p42/44 mitogenactivated protein kinase (MAPK) into the nuclei of the sensory neurons. Thus, different stimuli activating different signaling pathways converge by regulating the synthesis and release of a neuropeptide to produce long-term synaptic plasticity.

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“…Alternatively, the CREBdependent memory might also be generated independently. Intriguingly, it has been proposed that CREB can be activated independent of STM in long-term synaptic facilitation in Aplysia (Emptage and Carew, 1993;Casadio et al, 1999;Purcell et al, 2003). In addition, although memory performance becomes undetectable in 3 h, the requirement of CREB activity suggests neural mechanisms that are in part shared with LTM in the adult fly.…”

Section: Requirement For Amn In Larval Learning and Memorymentioning

confidence: 99%

Induction of cAMP Response Element-Binding Protein-Dependent Medium-Term Memory by Appetitive Gustatory Reinforcement inDrosophilaLarvae

Honjo¹,

Furukubo-Tokunaga²

2005

J. Neurosci.

118

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The fruit fly Drosophila melanogaster has been successfully used as a model animal for the study of the genetic and molecular mechanisms of learning and memory. Although most of the Drosophila learning studies have used the adult fly, the relative complexity of its neural network hinders cellular and molecular studies at high resolution. In contrast, the Drosophila larva has a simple brain with uniquely identifiable neural networks, providing an opportunity of an attractive alternative system for elucidation of underlying mechanisms involved in learning and memory. In this paper, we describe a novel paradigm of larval associative learning with a single odor and a positive gustatory reinforcer, sucrose. Mutant analyses have suggested importance of cAMP signaling and potassium channel activities in larval learning as has been demonstrated with the adult fly. Intriguingly, larval memory produced by the appetitive conditioning lasts medium term and depends on both amnesiac and cAMP response element-binding protein (CREB). A significant part of memory was disrupted at very early phase by CREB blockade without affecting immediate learning performance. Moreover, we also show that synaptic output of larval mushroom body neurons is required for retrieval but not for acquisition and retention of the larval memory, including the CREB-dependent component.

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Activation of a Tyrosine Kinase-MAPK Cascade Enhances the Induction of Long-Term Synaptic Facilitation and Long-Term Memory in Aplysia

Cited by 116 publications

References 53 publications

Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later

Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later

Protein Kinase C Regulates Local Synthesis and Secretion of a Neuropeptide Required for Activity-Dependent Long-Term Synaptic Plasticity

Induction of cAMP Response Element-Binding Protein-Dependent Medium-Term Memory by Appetitive Gustatory Reinforcement inDrosophilaLarvae

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