Loss of limbic system-associated membrane protein leads to reduced hippocampal mineralocorticoid receptor expression, impaired synaptic plasticity, and spatial memory deficit

Shenfeng Qiu, Danielle L. Champagne, Melinda Peters, Elizabeth H. Catania, Edwin J. Weeber, Pat Levitt, Aurea F. Pimenta

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Background: The limbic system-associated membrane protein (LAMP) promotes development of neurons of limbic origin. We have previously shown that genetic deletion of LAMP results in heightened reactivity to novelty and reduced anxiety-like behaviors in mice. Here, we demonstrate a critical role of LAMP in hippocampal-dependent synaptic physiology and behavior. Methods: We tested spatial memory performance, hippocampal synaptic plasticity, and stress-related modalities in Lsamp-/- mice and their littermate control mice. Results: Lsamp-/- mice exhibit a pronounced deficit in spatial memory acquisition and poorly sustained CA1 long-term potentiation. We found reduced expression of mineralocorticoid receptor (MR) transcripts in the hippocampus and reduction in the corticosterone-induced, MR-mediated nongenomic modulatory effects on CA1 synaptic transmission. Importantly, the impaired long-term potentiation in Lsamp-/- mice can be rescued by stress-like levels of corticosterone in a MR-dependent manner. Conclusions: Our study reveals a novel functional relationship between a cell adhesion molecule enriched in developing limbic circuits, glucocorticoid receptors, and cognitive functioning.

Original languageEnglish (US)
Pages (from-to)197-204
Number of pages8
JournalBiological Psychiatry
Volume68
Issue number2
DOIs
StatePublished - Jul 15 2010
Externally publishedYes

Fingerprint

Mineralocorticoid Receptors
Neuronal Plasticity
Memory Disorders
Long-Term Potentiation
Corticosterone
Glucocorticoid Receptors
Cell Adhesion Molecules
Synaptic Transmission
Hippocampus
Anxiety
Spatial Memory
limbic system-associated membrane protein
Neurons

Keywords

  • Limbic system-associated membrane protein
  • mineralocorticoid receptor
  • spatial memory
  • stress
  • synaptic plasticity

ASJC Scopus subject areas

  • Biological Psychiatry
  • Medicine(all)

Cite this

Loss of limbic system-associated membrane protein leads to reduced hippocampal mineralocorticoid receptor expression, impaired synaptic plasticity, and spatial memory deficit. / Qiu, Shenfeng; Champagne, Danielle L.; Peters, Melinda; Catania, Elizabeth H.; Weeber, Edwin J.; Levitt, Pat; Pimenta, Aurea F.

In: Biological Psychiatry, Vol. 68, No. 2, 15.07.2010, p. 197-204.

Research output: Contribution to journalArticle

Qiu, Shenfeng ; Champagne, Danielle L. ; Peters, Melinda ; Catania, Elizabeth H. ; Weeber, Edwin J. ; Levitt, Pat ; Pimenta, Aurea F. / Loss of limbic system-associated membrane protein leads to reduced hippocampal mineralocorticoid receptor expression, impaired synaptic plasticity, and spatial memory deficit. In: Biological Psychiatry. 2010 ; Vol. 68, No. 2. pp. 197-204.
@article{ce042223fc07406e944698a9955a3ee9,
title = "Loss of limbic system-associated membrane protein leads to reduced hippocampal mineralocorticoid receptor expression, impaired synaptic plasticity, and spatial memory deficit",
abstract = "Background: The limbic system-associated membrane protein (LAMP) promotes development of neurons of limbic origin. We have previously shown that genetic deletion of LAMP results in heightened reactivity to novelty and reduced anxiety-like behaviors in mice. Here, we demonstrate a critical role of LAMP in hippocampal-dependent synaptic physiology and behavior. Methods: We tested spatial memory performance, hippocampal synaptic plasticity, and stress-related modalities in Lsamp-/- mice and their littermate control mice. Results: Lsamp-/- mice exhibit a pronounced deficit in spatial memory acquisition and poorly sustained CA1 long-term potentiation. We found reduced expression of mineralocorticoid receptor (MR) transcripts in the hippocampus and reduction in the corticosterone-induced, MR-mediated nongenomic modulatory effects on CA1 synaptic transmission. Importantly, the impaired long-term potentiation in Lsamp-/- mice can be rescued by stress-like levels of corticosterone in a MR-dependent manner. Conclusions: Our study reveals a novel functional relationship between a cell adhesion molecule enriched in developing limbic circuits, glucocorticoid receptors, and cognitive functioning.",
keywords = "Limbic system-associated membrane protein, mineralocorticoid receptor, spatial memory, stress, synaptic plasticity",
author = "Shenfeng Qiu and Champagne, {Danielle L.} and Melinda Peters and Catania, {Elizabeth H.} and Weeber, {Edwin J.} and Pat Levitt and Pimenta, {Aurea F.}",
year = "2010",
month = "7",
day = "15",
doi = "10.1016/j.biopsych.2010.02.013",
language = "English (US)",
volume = "68",
pages = "197--204",
journal = "Biological Psychiatry",
issn = "0006-3223",
publisher = "Elsevier USA",
number = "2",

}

TY - JOUR

T1 - Loss of limbic system-associated membrane protein leads to reduced hippocampal mineralocorticoid receptor expression, impaired synaptic plasticity, and spatial memory deficit

AU - Qiu, Shenfeng

AU - Champagne, Danielle L.

AU - Peters, Melinda

AU - Catania, Elizabeth H.

AU - Weeber, Edwin J.

AU - Levitt, Pat

AU - Pimenta, Aurea F.

PY - 2010/7/15

Y1 - 2010/7/15

N2 - Background: The limbic system-associated membrane protein (LAMP) promotes development of neurons of limbic origin. We have previously shown that genetic deletion of LAMP results in heightened reactivity to novelty and reduced anxiety-like behaviors in mice. Here, we demonstrate a critical role of LAMP in hippocampal-dependent synaptic physiology and behavior. Methods: We tested spatial memory performance, hippocampal synaptic plasticity, and stress-related modalities in Lsamp-/- mice and their littermate control mice. Results: Lsamp-/- mice exhibit a pronounced deficit in spatial memory acquisition and poorly sustained CA1 long-term potentiation. We found reduced expression of mineralocorticoid receptor (MR) transcripts in the hippocampus and reduction in the corticosterone-induced, MR-mediated nongenomic modulatory effects on CA1 synaptic transmission. Importantly, the impaired long-term potentiation in Lsamp-/- mice can be rescued by stress-like levels of corticosterone in a MR-dependent manner. Conclusions: Our study reveals a novel functional relationship between a cell adhesion molecule enriched in developing limbic circuits, glucocorticoid receptors, and cognitive functioning.

AB - Background: The limbic system-associated membrane protein (LAMP) promotes development of neurons of limbic origin. We have previously shown that genetic deletion of LAMP results in heightened reactivity to novelty and reduced anxiety-like behaviors in mice. Here, we demonstrate a critical role of LAMP in hippocampal-dependent synaptic physiology and behavior. Methods: We tested spatial memory performance, hippocampal synaptic plasticity, and stress-related modalities in Lsamp-/- mice and their littermate control mice. Results: Lsamp-/- mice exhibit a pronounced deficit in spatial memory acquisition and poorly sustained CA1 long-term potentiation. We found reduced expression of mineralocorticoid receptor (MR) transcripts in the hippocampus and reduction in the corticosterone-induced, MR-mediated nongenomic modulatory effects on CA1 synaptic transmission. Importantly, the impaired long-term potentiation in Lsamp-/- mice can be rescued by stress-like levels of corticosterone in a MR-dependent manner. Conclusions: Our study reveals a novel functional relationship between a cell adhesion molecule enriched in developing limbic circuits, glucocorticoid receptors, and cognitive functioning.

KW - Limbic system-associated membrane protein

KW - mineralocorticoid receptor

KW - spatial memory

KW - stress

KW - synaptic plasticity

UR - http://www.scopus.com/inward/record.url?scp=77954212930&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77954212930&partnerID=8YFLogxK

U2 - 10.1016/j.biopsych.2010.02.013

DO - 10.1016/j.biopsych.2010.02.013

M3 - Article

VL - 68

SP - 197

EP - 204

JO - Biological Psychiatry

JF - Biological Psychiatry

SN - 0006-3223

IS - 2

ER -