Comparison between basal and apical dendritic spines in estrogen-induced rapid spinogenesis of CA1 principal neurons in the adult hippocampus

Murakami, Gen; Tsurugizawa, Tomokazu; Hatanaka, Yusuke; Komatsuzaki, Yoshimasa; Tanabe, Nari; Mukai, Hideo; Hojo, Yasushi; Kominami, Shiro; Yamazaki, Takeshi; Kimoto, Tsunenobu; Kawato, Suguru

doi:10.1016/j.bbrc.2006.10.066

Cited by 74 publications

(72 citation statements)

References 21 publications

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“…The expression of ERa subtype in other location than the nucleus may indicate that it should act in other functions such as rapid neuronal responses, which are via membranal systems, using second messengers (Yankova et al, 2001;Murakami et al, 2006). This observation is in line with our results in relation with ERa location, which was detected at both nucleus and cytoplasmic level during the different phases of the estrous cycle.…”

Section: Discussionsupporting

confidence: 90%

“…In this brain area, estradiol induces the formation of excitatory synapses, increases dendritic spine density, synaptic plasticity, and prolongs excitatory postsynaptic potentials in CA1 pyramidal cells (Rudick and Woolley, 2001;Murakami et al, 2006;Mukai et al, 2010). Differences in nuclear estradiol uptake was detected in CA1 and CA3, observing a majority of labeled cells in the ventral horn of CA3 .…”

Section: Discussionmentioning

confidence: 96%

“…One of the brain regions sensitive to E2 effects is the hippocampus, which participates in many important functions such as memory consolidation and learning McEwen, 2002;Day and Good, 2005;Zurkovsky et al, 2006;Walf and Frye, 2008;Frick et al, 2010). In this line, it has been recog-nized that estradiol increases the density of dendritic spines and the number of spine synapses in CA1 pyramidal cells of the hippocampus (Murakami et al, 2006). Thus, in adult rats, CA structures in the hippocampus present a robust response to E2 treatment and to fluctuation in ovarian hormone levels along the estrous cycle (Gould et al, 1990;Segal and Murphy, 2001;Znamensky et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Differential Expression of Estrogen Receptors in Two Hippocampal Regions During the Estrous Cycle of the Rat

Mendoza-Garcés

Mendoza-Rodríguez

Jiménez-Trejo

et al. 2011

The Anatomical Record

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In the hippocampus, estrogens increase dendritic arborization, longterm potentiation, neuroprotection, and participate in many functions related with learning, memory, and affective behaviors. The presence of both estrogen receptors alpha (ERa) and beta (ERb) isoforms has been described in the hippocampus where they play different physiological roles. The aim of this study was to investigate, by using both techniques immunohistochemistry and Western Blot, the expression pattern of ERa and ERb in the hippocampus of the rat along the estrous cycle. Western blot analysis was used to confirm the specificity of the antibodies used against ERa and ERb and its relative content in the hippocampus. Results from immunohistochemical studies indicate that ERb expression increased more than the ERa in CA1 and CA3 regions during all phases of the estrous cycle. ERb immunoreactivity was mainly located in the nucleus and predominantly expressed in CA1 during estrous and metestrus, and in CA3 during diestrus. ERa was more abundant during estrous in comparison to other phases of the cycle in CA1 region, while it was more abundant during metestrus in CA3. Interestingly, the immunolocalization of ERa subtype was both cytoplasmic and nuclear. The overall results indicate that there is a differential expression, cellular localization, and distribution of both ER subtypes in CA1 and CA3 regions, suggesting different roles for these two receptors in the hippocampus along the estrous cycle. Anat Rec, 294:1913Rec, 294: -1919Rec, 294: , 2011. V V C 2011 Wiley-Liss, Inc.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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Differential Expression of Estrogen Receptors in Two Hippocampal Regions During the Estrous Cycle of the Rat

Mendoza-Garcés

Mendoza-Rodríguez

Jiménez-Trejo

et al. 2011

The Anatomical Record

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“…al. [295] found that estrogen rapidly increased spine density in CA1 pyramidal neurons in hippocampal slices and this effect was shared by the ER-α selective agonist PPT, and conversely blocked by the estrogen receptor antagonist, ICI182,780. This study showed a very rapid effect on spine density by estrogen, e.g.…”

Section: Mechanisms Of Estrogen Regulation Of Synaptic Plasticitymentioning

confidence: 95%

Neurotrophic and neuroprotective actions of estrogen: Basic mechanisms and clinical implications

et al. 2007

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Estrogen is an important hormone signal that regulates multiple tissues and functions in the body. This review focuses on the neurotrophic and neuroprotective actions of estrogen in the brain, with particular emphasis on estrogen actions in the hippocampus, cerebral cortex and striatum. Sex differences in the risk, onset and severity of neurodegenerative disease such as Alzheimer's disease, Parkinson's disease and stroke are well known, and the potential role of estrogen as a neuroprotective factor is discussed in this context. The review assimilates a complex literature that spans research in humans, non-human primates and rodent animal models and attempts to contrast and compare the findings across species where possible. Current controversies regarding the WHI (Women's Health Initiative) study, its ramifications, concerns and the new studies needed to address these concerns are also addressed. Signaling mechanisms underlying estrogen-induced neuroprotection and synaptic plasticity are reviewed, including the important concepts of genomic versus nongenomic mechanisms, types of estrogen receptor involved and their subcellular targeting, and implicated downstream signaling pathways and mediators. Finally, a multicellular mode of estrogen action in the regulation of neuronal survival and neurotrophism is discussed, as are potential future directions for the field.

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“…immature synapse | short-term memory | structural plasticity | synaptic plasticity | signal-to-noise ratio E stradiol rapidly and dramatically increases hippocampal dendritic spine and synapse density within minutes of application (1)(2)(3)(4). There is a strong correlative association between estrogeninduced spinogenesis and improvements in cognition (5); however, the relationship of these structural changes to estrogen-induced alterations in hippocampal function is unclear.…”

mentioning

confidence: 99%

Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

Phan

Suschkov

Molinaro

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

129

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Dramatic increases in hippocampal spine synapse density are known to occur within minutes of estrogen exposure. Until now, it has been assumed that enhanced spinogenesis increased excitatory input received by the CA1 pyramidal neurons, but how this facilitated learning and memory was unclear. Delivery of 17β-estradiol or an estrogen receptor (ER)-α (but not ER-β) agonist into the dorsal hippocampus rapidly improved general discrimination learning in female mice. The same treatments increased CA1 dendritic spines in hippocampal sections over a time course consistent with the learning acquisition phase. Surprisingly, estrogen-activated spinogenesis was associated with a decrease in CA1 hippocampal excitatory input, rapidly and transiently reducing CA1 AMPA activity via a mechanism likely reflecting AMPA receptor internalization and creation of silent or immature synapses. We propose that estrogens promote hippocampally mediated learning via a mechanism resembling some of the broad features of normal development, an initial overproduction of functionally immature connections being subsequently "pruned" by experience.immature synapse | short-term memory | structural plasticity | synaptic plasticity | signal-to-noise ratio E stradiol rapidly and dramatically increases hippocampal dendritic spine and synapse density within minutes of application (1-4). There is a strong correlative association between estrogeninduced spinogenesis and improvements in cognition (5); however, the relationship of these structural changes to estrogen-induced alterations in hippocampal function is unclear. Our laboratory recently reported that the density of hippocampal CA1 pyramidal dendritic spines increases very rapidly after systemic treatment with 17β-estradiol or estrogen receptor (ER) -selective agonists in ovariectomized female mice, changes that are paralleled by learning enhancements (2, 3). Estrogen-induced rapid structural changes are substantial, increasing spine density by 30-50% within 15-40 min of hormone application (1-3, 6). As a result, adult rodents can experience the addition of thousands of CA1 synapses within a span of minutes after exposure to estradiol. These effects of estrogens reproduce the changes occurring during the 4-d estrous cycle of female rodents, which include the induction of CA1 spines (7).How these processes contribute to the behavioral changes observed after estradiol treatment is not understood. Estradiol enhances excitatory neurotransmission throughout the hippocampus (8-10), and activates BDNF signaling in the mossy fiber system (11). Dendritic spines turn over more rapidly in the hippocampus than in the neocortex (12), particularly in the case of estradiol-induced spines (13). Such rapid, transient, and apparently indiscriminate increases in excitatory synapse formation would seem, at first sight, to be more likely to interfere with preexisting brain circuits and impair normal information processing than to enhance cognitive function.How then, does enhancement of spine formation lead to improved ...

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Comparison between basal and apical dendritic spines in estrogen-induced rapid spinogenesis of CA1 principal neurons in the adult hippocampus

Cited by 74 publications

References 21 publications

Differential Expression of Estrogen Receptors in Two Hippocampal Regions During the Estrous Cycle of the Rat

Differential Expression of Estrogen Receptors in Two Hippocampal Regions During the Estrous Cycle of the Rat

Neurotrophic and neuroprotective actions of estrogen: Basic mechanisms and clinical implications

Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

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