Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons

Sonja Y. Grooms, Kyung Min Noh, Roodland Regis, Gary J. Bassell, Monique K. Bryan, Reed C. Carroll, R. Suzanne Zukin

Research output: Contribution to journalArticle

124 Citations (Scopus)

Abstract

Activity-dependent regulation of synaptic AMPA receptor (AMPAR) number is critical to NMDA receptor (NMDAR)-dependent synaptic plasticity. Using quantitative high-resolution in situ hybridization, we show that mRNAs encoding the AMPA-type glutamate receptor subunits (GluRs) 1 and 2 are localized to dendrites of hippocampal neurons and are regulated by paradigms that alter synaptic efficacy. A substantial fraction of synaptic sites contain AMPAR mRNA, consistent with strategic positioning and availability for "on-site" protein synthesis. NMDAR activation depletes dendritic levels of AMPAR mRNAs. The decrease in mRNA occurs via rise in intracellular Ca2+, activation of extracellular signal-regulated kinase/mitogen-activated protein kinase signaling, and transcriptional arrest at the level of the nucleus. The decrease in mRNA is accompanied by a long-lasting reduction in synaptic AMPAR number, consistent with reduced synaptic efficacy. In contrast, group I metabotropic GluR signaling promotes microtubule-based trafficking of existing AMPAR mRNAs from the soma to dendrites. Bidirectional regulation of dendritic mRNA abundance represents a potentially powerful means to effect long-lasting changes in synaptic strength.

Original languageEnglish (US)
Pages (from-to)8339-8351
Number of pages13
JournalJournal of Neuroscience
Volume26
Issue number32
DOIs
StatePublished - Aug 9 2006

Fingerprint

AMPA Receptors
Dendrites
Neurons
Messenger RNA
Neurotransmitter Receptor
N-Methyl-D-Aspartate Receptors
Neuronal Plasticity
Extracellular Signal-Regulated MAP Kinases
Glutamate Receptors
Carisoprodol
Mitogen-Activated Protein Kinases
Microtubules
In Situ Hybridization

Keywords

  • AMPA receptors
  • Dendrites
  • Messenger RNA
  • mRNA trafficking
  • Synaptic plasticity
  • Transcription

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. / Grooms, Sonja Y.; Noh, Kyung Min; Regis, Roodland; Bassell, Gary J.; Bryan, Monique K.; Carroll, Reed C.; Zukin, R. Suzanne.

In: Journal of Neuroscience, Vol. 26, No. 32, 09.08.2006, p. 8339-8351.

Research output: Contribution to journalArticle

Grooms, Sonja Y. ; Noh, Kyung Min ; Regis, Roodland ; Bassell, Gary J. ; Bryan, Monique K. ; Carroll, Reed C. ; Zukin, R. Suzanne. / Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. In: Journal of Neuroscience. 2006 ; Vol. 26, No. 32. pp. 8339-8351.
@article{9334c22ec379401283f5e2c1e68c113d,
title = "Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons",
abstract = "Activity-dependent regulation of synaptic AMPA receptor (AMPAR) number is critical to NMDA receptor (NMDAR)-dependent synaptic plasticity. Using quantitative high-resolution in situ hybridization, we show that mRNAs encoding the AMPA-type glutamate receptor subunits (GluRs) 1 and 2 are localized to dendrites of hippocampal neurons and are regulated by paradigms that alter synaptic efficacy. A substantial fraction of synaptic sites contain AMPAR mRNA, consistent with strategic positioning and availability for {"}on-site{"} protein synthesis. NMDAR activation depletes dendritic levels of AMPAR mRNAs. The decrease in mRNA occurs via rise in intracellular Ca2+, activation of extracellular signal-regulated kinase/mitogen-activated protein kinase signaling, and transcriptional arrest at the level of the nucleus. The decrease in mRNA is accompanied by a long-lasting reduction in synaptic AMPAR number, consistent with reduced synaptic efficacy. In contrast, group I metabotropic GluR signaling promotes microtubule-based trafficking of existing AMPAR mRNAs from the soma to dendrites. Bidirectional regulation of dendritic mRNA abundance represents a potentially powerful means to effect long-lasting changes in synaptic strength.",
keywords = "AMPA receptors, Dendrites, Messenger RNA, mRNA trafficking, Synaptic plasticity, Transcription",
author = "Grooms, {Sonja Y.} and Noh, {Kyung Min} and Roodland Regis and Bassell, {Gary J.} and Bryan, {Monique K.} and Carroll, {Reed C.} and Zukin, {R. Suzanne}",
year = "2006",
month = "8",
day = "9",
doi = "10.1523/JNEUROSCI.0472-06.2006",
language = "English (US)",
volume = "26",
pages = "8339--8351",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "32",

}

TY - JOUR

T1 - Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons

AU - Grooms, Sonja Y.

AU - Noh, Kyung Min

AU - Regis, Roodland

AU - Bassell, Gary J.

AU - Bryan, Monique K.

AU - Carroll, Reed C.

AU - Zukin, R. Suzanne

PY - 2006/8/9

Y1 - 2006/8/9

N2 - Activity-dependent regulation of synaptic AMPA receptor (AMPAR) number is critical to NMDA receptor (NMDAR)-dependent synaptic plasticity. Using quantitative high-resolution in situ hybridization, we show that mRNAs encoding the AMPA-type glutamate receptor subunits (GluRs) 1 and 2 are localized to dendrites of hippocampal neurons and are regulated by paradigms that alter synaptic efficacy. A substantial fraction of synaptic sites contain AMPAR mRNA, consistent with strategic positioning and availability for "on-site" protein synthesis. NMDAR activation depletes dendritic levels of AMPAR mRNAs. The decrease in mRNA occurs via rise in intracellular Ca2+, activation of extracellular signal-regulated kinase/mitogen-activated protein kinase signaling, and transcriptional arrest at the level of the nucleus. The decrease in mRNA is accompanied by a long-lasting reduction in synaptic AMPAR number, consistent with reduced synaptic efficacy. In contrast, group I metabotropic GluR signaling promotes microtubule-based trafficking of existing AMPAR mRNAs from the soma to dendrites. Bidirectional regulation of dendritic mRNA abundance represents a potentially powerful means to effect long-lasting changes in synaptic strength.

AB - Activity-dependent regulation of synaptic AMPA receptor (AMPAR) number is critical to NMDA receptor (NMDAR)-dependent synaptic plasticity. Using quantitative high-resolution in situ hybridization, we show that mRNAs encoding the AMPA-type glutamate receptor subunits (GluRs) 1 and 2 are localized to dendrites of hippocampal neurons and are regulated by paradigms that alter synaptic efficacy. A substantial fraction of synaptic sites contain AMPAR mRNA, consistent with strategic positioning and availability for "on-site" protein synthesis. NMDAR activation depletes dendritic levels of AMPAR mRNAs. The decrease in mRNA occurs via rise in intracellular Ca2+, activation of extracellular signal-regulated kinase/mitogen-activated protein kinase signaling, and transcriptional arrest at the level of the nucleus. The decrease in mRNA is accompanied by a long-lasting reduction in synaptic AMPAR number, consistent with reduced synaptic efficacy. In contrast, group I metabotropic GluR signaling promotes microtubule-based trafficking of existing AMPAR mRNAs from the soma to dendrites. Bidirectional regulation of dendritic mRNA abundance represents a potentially powerful means to effect long-lasting changes in synaptic strength.

KW - AMPA receptors

KW - Dendrites

KW - Messenger RNA

KW - mRNA trafficking

KW - Synaptic plasticity

KW - Transcription

UR - http://www.scopus.com/inward/record.url?scp=33748133059&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33748133059&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0472-06.2006

DO - 10.1523/JNEUROSCI.0472-06.2006

M3 - Article

VL - 26

SP - 8339

EP - 8351

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 32

ER -