Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons

Hideo Mukai, Tomokazu Tsurugizawa, Gen Murakami, Shiro Kominami, Hirotaka Ishii, Mari Ogiue-Ikeda, Norio Takata, Nobuaki Tanabe, Aizo Furukawa, Yasushi Hojo, Yuuki Ooishi, John Morrison, William G.M. Janssen, John A. Rose, Pierre Chambon, Shigeaki Kato, Shunsuke Izumi, Takeshi Yamazaki, Tetsuya Kimoto, Suguru Kawato

Research output: Contribution to journalArticle

146 Citations (Scopus)

Abstract

Rapid modulation of hippocampal synaptic plasticity by estrogen has long been a hot topic, but analysis of molecular mechanisms via synaptic estrogen receptors has been seriously difficult. Here, two types of independent synaptic plasticity, long-term depression (LTD) and spinogenesis, were investigated, in response to 17β-estradiol and agonists of estrogen receptors using hippocampal slices from adult male rats. Multi-electrode investigations demonstrated that estradiol rapidly enhanced LTD not only in CA1 but also in CA3 and dentate gyrus. Dendritic spine morphology analysis demonstrated that the density of thin type spines was selectively increased in CA1 pyramidal neurons within 2 h after application of 1 nm estradiol. This enhancement of spinogenesis was completely suppressed by mitogen-activated protein (MAP) kinase inhibitor. Only the estrogen receptor (ER) alpha agonist, (propyl-pyrazole-trinyl)tris- phenol (PPT), induced the same enhancing effect as estradiol on both LTD and spinogenesis in the CA1. The ERbeta agonist, (4-hydroxyphenyl)-propionitrile (DPN), suppressed LTD and did not affect spinogenesis. Because the mode of synaptic modulations by estradiol was mostly the same as that by the ERalpha agonist, a search was made for synaptic ERalpha using purified RC-19 antibody qualified using ERalpha knockout (KO) mice. Localization of ERalpha in spines of principal glutamatergic neurons was demonstrated using immunogold electron microscopy and immunohistochemistry. ERalpha was also located in nuclei, cytoplasm and presynapses.

Original languageEnglish (US)
Pages (from-to)950-967
Number of pages18
JournalJournal of Neurochemistry
Volume100
Issue number4
DOIs
StatePublished - Feb 1 2007
Externally publishedYes

Fingerprint

Neurotransmitter Receptor
Estrogen Receptor alpha
Estrogen Receptors
Neurons
Modulation
Estradiol
Estrogens
Neuronal Plasticity
Plasticity
Spine
Estrogen Receptor beta
Dendritic Spines
Pyramidal Cells
Dentate Gyrus
Protein Kinase Inhibitors
Phenol
Mitogen-Activated Protein Kinases
Knockout Mice
Electron microscopy
Rats

Keywords

  • Estrogen
  • Estrogen receptor
  • Hippocampus
  • Neurosteroid
  • Spine
  • Synaptic plasticity

ASJC Scopus subject areas

  • Biochemistry
  • Cellular and Molecular Neuroscience

Cite this

Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. / Mukai, Hideo; Tsurugizawa, Tomokazu; Murakami, Gen; Kominami, Shiro; Ishii, Hirotaka; Ogiue-Ikeda, Mari; Takata, Norio; Tanabe, Nobuaki; Furukawa, Aizo; Hojo, Yasushi; Ooishi, Yuuki; Morrison, John; Janssen, William G.M.; Rose, John A.; Chambon, Pierre; Kato, Shigeaki; Izumi, Shunsuke; Yamazaki, Takeshi; Kimoto, Tetsuya; Kawato, Suguru.

In: Journal of Neurochemistry, Vol. 100, No. 4, 01.02.2007, p. 950-967.

Research output: Contribution to journalArticle

Mukai, H, Tsurugizawa, T, Murakami, G, Kominami, S, Ishii, H, Ogiue-Ikeda, M, Takata, N, Tanabe, N, Furukawa, A, Hojo, Y, Ooishi, Y, Morrison, J, Janssen, WGM, Rose, JA, Chambon, P, Kato, S, Izumi, S, Yamazaki, T, Kimoto, T & Kawato, S 2007, 'Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons', Journal of Neurochemistry, vol. 100, no. 4, pp. 950-967. https://doi.org/10.1111/j.1471-4159.2006.04264.x
Mukai, Hideo ; Tsurugizawa, Tomokazu ; Murakami, Gen ; Kominami, Shiro ; Ishii, Hirotaka ; Ogiue-Ikeda, Mari ; Takata, Norio ; Tanabe, Nobuaki ; Furukawa, Aizo ; Hojo, Yasushi ; Ooishi, Yuuki ; Morrison, John ; Janssen, William G.M. ; Rose, John A. ; Chambon, Pierre ; Kato, Shigeaki ; Izumi, Shunsuke ; Yamazaki, Takeshi ; Kimoto, Tetsuya ; Kawato, Suguru. / Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. In: Journal of Neurochemistry. 2007 ; Vol. 100, No. 4. pp. 950-967.
@article{23fa4c6dcfcf41dd952a27e1821575f1,
title = "Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons",
abstract = "Rapid modulation of hippocampal synaptic plasticity by estrogen has long been a hot topic, but analysis of molecular mechanisms via synaptic estrogen receptors has been seriously difficult. Here, two types of independent synaptic plasticity, long-term depression (LTD) and spinogenesis, were investigated, in response to 17β-estradiol and agonists of estrogen receptors using hippocampal slices from adult male rats. Multi-electrode investigations demonstrated that estradiol rapidly enhanced LTD not only in CA1 but also in CA3 and dentate gyrus. Dendritic spine morphology analysis demonstrated that the density of thin type spines was selectively increased in CA1 pyramidal neurons within 2 h after application of 1 nm estradiol. This enhancement of spinogenesis was completely suppressed by mitogen-activated protein (MAP) kinase inhibitor. Only the estrogen receptor (ER) alpha agonist, (propyl-pyrazole-trinyl)tris- phenol (PPT), induced the same enhancing effect as estradiol on both LTD and spinogenesis in the CA1. The ERbeta agonist, (4-hydroxyphenyl)-propionitrile (DPN), suppressed LTD and did not affect spinogenesis. Because the mode of synaptic modulations by estradiol was mostly the same as that by the ERalpha agonist, a search was made for synaptic ERalpha using purified RC-19 antibody qualified using ERalpha knockout (KO) mice. Localization of ERalpha in spines of principal glutamatergic neurons was demonstrated using immunogold electron microscopy and immunohistochemistry. ERalpha was also located in nuclei, cytoplasm and presynapses.",
keywords = "Estrogen, Estrogen receptor, Hippocampus, Neurosteroid, Spine, Synaptic plasticity",
author = "Hideo Mukai and Tomokazu Tsurugizawa and Gen Murakami and Shiro Kominami and Hirotaka Ishii and Mari Ogiue-Ikeda and Norio Takata and Nobuaki Tanabe and Aizo Furukawa and Yasushi Hojo and Yuuki Ooishi and John Morrison and Janssen, {William G.M.} and Rose, {John A.} and Pierre Chambon and Shigeaki Kato and Shunsuke Izumi and Takeshi Yamazaki and Tetsuya Kimoto and Suguru Kawato",
year = "2007",
month = "2",
day = "1",
doi = "10.1111/j.1471-4159.2006.04264.x",
language = "English (US)",
volume = "100",
pages = "950--967",
journal = "Journal of Neurochemistry",
issn = "0022-3042",
publisher = "Wiley-Blackwell",
number = "4",

}

TY - JOUR

T1 - Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons

AU - Mukai, Hideo

AU - Tsurugizawa, Tomokazu

AU - Murakami, Gen

AU - Kominami, Shiro

AU - Ishii, Hirotaka

AU - Ogiue-Ikeda, Mari

AU - Takata, Norio

AU - Tanabe, Nobuaki

AU - Furukawa, Aizo

AU - Hojo, Yasushi

AU - Ooishi, Yuuki

AU - Morrison, John

AU - Janssen, William G.M.

AU - Rose, John A.

AU - Chambon, Pierre

AU - Kato, Shigeaki

AU - Izumi, Shunsuke

AU - Yamazaki, Takeshi

AU - Kimoto, Tetsuya

AU - Kawato, Suguru

PY - 2007/2/1

Y1 - 2007/2/1

N2 - Rapid modulation of hippocampal synaptic plasticity by estrogen has long been a hot topic, but analysis of molecular mechanisms via synaptic estrogen receptors has been seriously difficult. Here, two types of independent synaptic plasticity, long-term depression (LTD) and spinogenesis, were investigated, in response to 17β-estradiol and agonists of estrogen receptors using hippocampal slices from adult male rats. Multi-electrode investigations demonstrated that estradiol rapidly enhanced LTD not only in CA1 but also in CA3 and dentate gyrus. Dendritic spine morphology analysis demonstrated that the density of thin type spines was selectively increased in CA1 pyramidal neurons within 2 h after application of 1 nm estradiol. This enhancement of spinogenesis was completely suppressed by mitogen-activated protein (MAP) kinase inhibitor. Only the estrogen receptor (ER) alpha agonist, (propyl-pyrazole-trinyl)tris- phenol (PPT), induced the same enhancing effect as estradiol on both LTD and spinogenesis in the CA1. The ERbeta agonist, (4-hydroxyphenyl)-propionitrile (DPN), suppressed LTD and did not affect spinogenesis. Because the mode of synaptic modulations by estradiol was mostly the same as that by the ERalpha agonist, a search was made for synaptic ERalpha using purified RC-19 antibody qualified using ERalpha knockout (KO) mice. Localization of ERalpha in spines of principal glutamatergic neurons was demonstrated using immunogold electron microscopy and immunohistochemistry. ERalpha was also located in nuclei, cytoplasm and presynapses.

AB - Rapid modulation of hippocampal synaptic plasticity by estrogen has long been a hot topic, but analysis of molecular mechanisms via synaptic estrogen receptors has been seriously difficult. Here, two types of independent synaptic plasticity, long-term depression (LTD) and spinogenesis, were investigated, in response to 17β-estradiol and agonists of estrogen receptors using hippocampal slices from adult male rats. Multi-electrode investigations demonstrated that estradiol rapidly enhanced LTD not only in CA1 but also in CA3 and dentate gyrus. Dendritic spine morphology analysis demonstrated that the density of thin type spines was selectively increased in CA1 pyramidal neurons within 2 h after application of 1 nm estradiol. This enhancement of spinogenesis was completely suppressed by mitogen-activated protein (MAP) kinase inhibitor. Only the estrogen receptor (ER) alpha agonist, (propyl-pyrazole-trinyl)tris- phenol (PPT), induced the same enhancing effect as estradiol on both LTD and spinogenesis in the CA1. The ERbeta agonist, (4-hydroxyphenyl)-propionitrile (DPN), suppressed LTD and did not affect spinogenesis. Because the mode of synaptic modulations by estradiol was mostly the same as that by the ERalpha agonist, a search was made for synaptic ERalpha using purified RC-19 antibody qualified using ERalpha knockout (KO) mice. Localization of ERalpha in spines of principal glutamatergic neurons was demonstrated using immunogold electron microscopy and immunohistochemistry. ERalpha was also located in nuclei, cytoplasm and presynapses.

KW - Estrogen

KW - Estrogen receptor

KW - Hippocampus

KW - Neurosteroid

KW - Spine

KW - Synaptic plasticity

UR - http://www.scopus.com/inward/record.url?scp=33846807827&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33846807827&partnerID=8YFLogxK

U2 - 10.1111/j.1471-4159.2006.04264.x

DO - 10.1111/j.1471-4159.2006.04264.x

M3 - Article

C2 - 17266735

AN - SCOPUS:33846807827

VL - 100

SP - 950

EP - 967

JO - Journal of Neurochemistry

JF - Journal of Neurochemistry

SN - 0022-3042

IS - 4

ER -