Differential Role of Mitogen-Activated Protein Kinase in Three Distinct Phases of Memory for Sensitization in Aplysia

Sharma, Shiv K.; Sherff, Carolyn M.; Shobe, Justin; Bagnall, Martha W.; Sutton, Michael A.; Carew, Thomas J.

doi:10.1523/jneurosci.23-09-03899.2003

Cited by 125Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurobiology and Insect Physiology Research

Differential Role of Mitogen-Activated Protein Kinase in Three Distinct Phases of Memory for Sensitization in Aplysia

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Sharma, Shiv K., Sherff, Carolyn M., Shobe, Justin, Bagnall, Martha W., Sutton, Michael A., Carew, Thomas J.·2003·The Journal of Neuroscience

DOI 10.1523/jneurosci.23-09-03899.2003PMC PMC6742188

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Abstract

The mitogen-activated protein kinase (MAPK) pathway has been implicated recently in synaptic plasticity and memory. Here we used tail shock-induced sensitization of the tail-elicited siphon withdrawal reflex in Aplysia to examine the role of MAPK in three different phases of memory. We show that a specific pattern of serotonin (5-HT) application that produces intermediate-term and long-term synaptic facilitation (ITF and LTF, respectively) of the sensory-motor (SN-MN) synapses in Aplysia leads to sustained activation of extracellular signal-regulated kinase in the ventrocaudal cluster sensory neurons (SNs), which include the tail SNs. Furthermore, repeated tail shocks that induce intermediate-term and long-term memory (ITM and LTM, respectively) for sensitization also lead to sustained MAPK activation in the SNs. Given these results, we next examined the requirement of MAPK activity in (1) SN-MN synaptic facilitation and (2) memory for sensitization in Aplysia, by inhibiting MEK, the upstream kinase that phosphorylates and activates MAPK. In cellular experiments, we show that MAPK activity is required for ITF of tail SN-tail MN synapses, and, in parallel behavioral experiments, we show that ITM requires MAPK activity for its induction but not its expression. In contrast, short-term memory for sensitization does not require MAPK activity. Finally, 5-HT-induced LTF has been shown previously to require MAPK activity. Here we show that LTM for sensitization also requires MAPK activity. These results provide evidence that MAPK plays important roles specifically in long-lasting phases of synaptic plasticity and memory.

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The PKA and ERK cascades are necessary to induce long-term synaptic facilitation (LTF) in Aplysia.
“Two biochemical cascades required for LTF are those that mediate activation of protein kinase A (PKA)12–15 and the MAP kinase isoform termed extracellular signal-regulated kinase (ERK)16–18.”
From Computational design of enhanced learning protocols (2012) · cites this paper as [18]
The delayed 5HT-induced MAPK activation at 45 min requires new protein synthesis but not new gene transcription.
“However, emetine exposure to the CNS for 30 min before 5HT application completely blocked 5HTinduced delayed MAPK activation (n ϭ 19, 5HT: 1.64 Ϯ 0.16 P-MAPK/T-MAPK ratio, 5HT-emetine: 1.19 Ϯ 0.07, p ϭ 0.003 paired t test, Fig. 2b).”
From MAPK Establishes a Molecular Context That Defines Effective Training Patterns for Long-Term Memory Formation (2013) · cites this paper as Sharma et al., 2003
Sustained activation of nuclear MAPK following five repeated spaced training shocks or spaced pulses of 5HT appears to be initiated in the presynaptic terminals of SN-MN synapses and requires the synthesis and local synaptic signaling of the neurotrophin-like peptide sensorin.
“The sustained activation of nuclear MAPK following five repeated spaced training shocks or spaced pulses of 5HT (Sharma et al., 2003) appears to be initiated in the presynaptic terminals of SN-MN synapses and requires the synthesis and local synaptic signaling of the neurotrophin-like peptide sensorin (Hu et al., 2004;Wang et al., 2009).”
From MAPK Establishes a Molecular Context That Defines Effective Training Patterns for Long-Term Memory Formation (2013) · cites this paper as Sharma et al., 2003
Repeated training shocks or 5HT exposures give rise to sustained posttraining MAPK activation in tail sensory neurons.
“Additionally, repeated training shocks or 5HT exposures give rise to sustained posttraining MAPK activation in tail SNs (Sharma et al., 2003).”
From MAPK Establishes a Molecular Context That Defines Effective Training Patterns for Long-Term Memory Formation (2013) · cites this paper as Sharma et al., 2003
Sustained MAPK activation in tail sensory neurons following spaced training is necessary for LTM formation.
“We have previously shown that a sustained (1-3 h) MAPK activation develops in tail SNs following spaced training (4 or 5 spaced training shocks or pulses of 5HT; Sharma et al., 2003) and is necessary for LTM formation (Shobe et al., 2005).”
From MAPK Establishes a Molecular Context That Defines Effective Training Patterns for Long-Term Memory Formation (2013) · cites this paper as Sharma et al., 2003

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Differential roles of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia
Sharma, S. K., Sherff, C. M., Shobe, J., Bagnall, M. W., Sutton, M. A., & Carew, T. J. (2003)
Self-citation
The Roles of MAPK Cascades in Synaptic Plasticity and Memory in Aplysia: Facilitatory Effects and Inhibitory Constraints: Figure 1
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Temporal Phases of Activity-Dependent Plasticity and Memory Are Mediated by Compartmentalized Routing of MAPK Signaling in Aplysia Sensory Neurons
Shobe, J. L., Zhao, Y., Stough, S., Ye, X., Hsuan, V., Martin, K. C., & Carew, T. J. (2009) · Neuron · doi:10.1016/j.neuron.2008.10.049 · Cited by 33 · see citing works
Self-citation
Review The Roles of MAPK Cascades in Synaptic Plasticity and Memory in Aplysia: Facilitatory Effects and Inhibitory Constraints
Sharma, S. K., & Carew, T. J. (2015)
Self-citation
Local synaptic integration of mitogen-activated protein kinase and protein kinase A signaling mediates intermediate-term synaptic facilitation in Aplysia
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Self-citation

Authors: Sharma, S. K., Sherff, C. M., Shobe, J., Bagnall, M. W., Sutton, M. A., & Carew, T. J.
Affiliations: University of California, Irvine (US)
ORCID: Sharma, Shiv K.
Shobe, Justin
Bagnall, Martha W.
Sutton, Michael A.
Carew, Thomas J.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2003-05-01
Volume: 23
Issue: 9
Pages: 3899-3907
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.23-09-03899.2003
PMC: PMC6742188
OpenAlex: W1500995611
Cited by: 125
References: 68
Citations by year: 2025: 2 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 4 · 2017: 7 · 2016: 4 · 2015: 8 · 2014: 4 · 2013: 8 · 2012: 2
FWCI: 5.39
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
PubMed
Funders: National Science Foundation (0049013)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords: mitogen-activated protein kinase, Aplysia, siphon withdrawal reflex, serotonin, extracellular signal-regulated kinase, MEK inhibition, intermediate-term memory, long-term memory, short-term memory, synaptic facilitation, sensory-motor synapses, synaptic plasticity
MeSH terms: Action Potentials, Animals, Aplysia, Electric Stimulation, Enzyme Activation, Enzyme Inhibitors, Memory, Motor Neurons, Neurons, Afferent, Reflex, Serotonin, Stimulation, Chemical, Synapses, Long-Term Potentiation, Excitatory Postsynaptic Potentials, Mitogen-Activated Protein Kinases, In Vitro Techniques

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Differential Role of Mitogen-Activated Protein Kinase in Three Distinct Phases of Memory for Sensitization in Aplysia

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