Estrogen receptor KO mice study on rapid modulation of spines and long-term depression in the hippocampus

Murakami, Gen; Hojo, Yasushi; Ogiue-Ikeda, Mari; Mukai, Hideo; Chambon, Pierre; Nakajima, Kohei; Ooishi, Yuuki; Kimoto, Tsunenobu; Kawato, Suguru

doi:10.1016/j.brainres.2014.12.002

Cited by 36 publications

(26 citation statements)

References 57 publications

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“…In contrast to the in vivo data, however, studies using hippocampal slices from adult male rats report that the density of dendritic spines in CA1 was increased within 2 h of bath application of E 2 (Murakami et al 2006Mukai et al 2007;Ogiue-Ikeda et al 2008;Ooishi et al 2012). This increase was blocked by an inhibitor of ERK phosphorylation (Mukai et al 2007;Murakami et al 2014), linking ERK signaling to E 2 -induced CA1 spinogenesis in males. The spinogenesis in male hippocampal slices appears to be mediated by ERa rather than ERb, as illustrated by findings showing that CA1 spines were increased by bath application of PPT, but not DPN (Mukai et al 2007).…”

Section: Spine Densitymentioning

confidence: 71%

“…Some data support the conclusion that input from the basal forebrain is necessary for estradiol to enhance spines in adult female rats (Leranth et al 2000). However, bathapplied E 2 can increase spines in male hippocampal slices (Mukai et al 2007;Murakami et al 2014;Hasegawa et al 2015) and cultured embryonic hippocampal neurons (Murphy and Segal 1996), suggesting that subcortical input may not be essential, at least in an ex vivo system. Other work shows that two injections of estradiol benzoate spaced 24 h apart failed to increase CA1 spine synapse density in ovariectomized rats trained in the Morris water maze , indicating that stressful behavioral training may interfere with the effects of estradiol on CA1 spinogenesis.…”

Section: Spine Densitymentioning

confidence: 77%

“…These data have been interpreted to suggest that E 2 decreases the threshold for inducing LTD in adult females by activating group I mGlu receptors (Zamani et al 2000;Shiroma et al 2005). Similarly, 30 min of E 2 pretreatment enhanced NMDA-induced LTD in CA1, CA3, and the dentate gyrus of adult male rats (Mukai et al 2007;Murakami et al 2014). In contrast to the important role of ERb in mediating LTP, this effect was mimicked by the ERa agonist PPT, but not by the ERb agonist DPN, indicating a specific involvement of ERa in mediating LTD in the male hippocampus (Mukai et al 2007).…”

Section: Synaptic Plasticitymentioning

confidence: 91%

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Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents

et al. 2015

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Ample evidence has demonstrated that sex steroid hormones, such as the potent estrogen 17b-estradiol (E 2 ), affect hippocampal morphology, plasticity, and memory in male and female rodents. Yet relatively few investigators who work with male subjects consider the effects of these hormones on learning and memory. This review describes the effects of E 2 on hippocampal spinogenesis, neurogenesis, physiology, and memory, with particular attention paid to the effects of E 2 in male rodents. The estrogen receptors, cell-signaling pathways, and epigenetic processes necessary for E 2 to enhance memory in female rodents are also discussed in detail. Finally, practical considerations for working with female rodents are described for those investigators thinking of adding females to their experimental designs.Hormones have long been known to play key roles in regulating learning and memory. Many hormones, including epinephrine, glucocorticoids, and insulin influence learning and memory via inverted U-shaped dose-response relationships in which memory is enhanced by moderate, but not low or high, hormone levels (Roozendaal 2000;Korol and Gold 2007;McNay and Recknagel 2011). Research from the past two decades has demonstrated that sex steroid hormones, particularly the potent estrogen 17b-estradiol (E 2 ), also regulate learning and memory in male and female rodents via an inverted U-shaped dose-response function that is influenced by estrogen receptor expression (Packard and Teather 1997a;Packard 1998;Foster 2012). Yet E 2 has not gained widespread acceptance as a hormonal modulator of memory in both females and males, perhaps because the majority of this research has been conducted in female rodents. Moreover, the common view of E 2 as a "female" hormone may contribute to the misperception that E 2 is not relevant for cognitive function in males. However, considerable evidence supports a vital role for E 2 in mediating neural function and behavior in male rodents. Therefore, it is important for investigators working with males to understand the ways in which E 2 and other sex steroid hormones (e.g., androgens, progestins, and other estrogens) may influence their brain regions and behaviors of interest.Another reason for investigators to be cognizant of sex steroid hormone-induced regulation of learning and memory is that males and females may respond differently to various treatments and environmental factors. A classic example is that of acute stress, which enhances classical conditioning and increases apical CA1 dendritic spine density in male rats, but impairs classical conditioning and decreases CA1 spine density in female rats (Wood and Shors 1998;Shors et al. 2001). Therefore, investigators hoping to comply with National Institutes of Health policies that encourage the inclusion of females in biomedical research must be aware that adding females to a study is not as simple as adding another group. In some ways, females are fundamentally different from males, the most obvious of which is the presence of reproductive...

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Section: Spine Densitymentioning

confidence: 71%

Section: Spine Densitymentioning

confidence: 77%

Section: Synaptic Plasticitymentioning

confidence: 91%

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Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents

et al. 2015

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“…For example, inhibitors of ERK, PI3K, PKA, protein kinase C (PKC), and CaMKII phosphorylation block spinogenesis and LTP in hippocampal slices from adult male rats (Hasegawa et al, 2015; Mukai et al, 2007; Murakami et al, 2014). Similarly, inhibition of ERK prevents 17β-estradiol from increasing dendritic spine density in cultured embryonic rat (sex not specified) cortical neurons (Srivastava et al, 2008).…”

Section: Cell-signaling Pathways Involved In 17β-estradiol-inducedmentioning

confidence: 99%

Why estrogens matter for behavior and brain health

Galea

Frick

Hampson

et al. 2017

Neuroscience & Biobehavioral Reviews

138

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The National Institutes of Health (NIH) has required the inclusion of women in clinical studies since 1993, which has enhanced our understanding of how biological sex affects certain medical conditions and allowed the development of sex-specific treatment protocols. However, NIH’s policy did not previously apply to basic research and the NIH recently introduced a new policy requiring all new grant applications to explicitly address sex as a biological variable. The policy itself is grounded in the results of numerous investigations in animals and humans illustrating the existence of sex differences in the brain and behavior, and the importance of sex hormones, particularly estrogens, in regulating physiology and behavior. Here, we review findings from our laboratories and others, demonstrating how estrogens influence brain and behavior in adult females. Research from subjects throughout the adult lifespan on topics ranging from social behavior, learning and memory, to disease risk will be discussed to frame an understanding of why estrogens matter to behavioral neuroscience.

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“…Although the mechanisms by which E 2 regulates synaptic plasticity in CA1 have been extensively studied, less attention has been paid to its effects in other hippocampal areas, such as CA3 or dentate gyrus (DG). Likewise, E 2 modulates different forms of longterm depression (LTD) in hippocampus (Shiroma et al, 2005;Mukai et al, 2007;Murakami et al, 2015), but the underlying mechanism remains largely unknown.…”

Section: Introductionmentioning

confidence: 99%

A novel form of synaptic plasticity in field CA3 of hippocampus requires GPER1 activation and BDNF release

Briz¹,

Liu²,

Zhu³

et al. 2015

J Exp Med

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Estrogen receptor KO mice study on rapid modulation of spines and long-term depression in the hippocampus

Cited by 36 publications

References 57 publications

Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents

Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents

Why estrogens matter for behavior and brain health

A novel form of synaptic plasticity in field CA3 of hippocampus requires GPER1 activation and BDNF release

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