Influence of gonadal steroids on the glial fibrillary acidic protein‐immunoreactive astrocyte population in young rat hippocampus

Conejo, Nélida M.; González-Pardo, Héctor; Cimadevilla, José Manuel; Argüelles, Juan; Díaz, Francisca; Vallejo, Guillermo; Árias, Jorge L.

doi:10.1002/jnr.20372

Cited by 35 publications

(20 citation statements)

References 48 publications

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“…Our data from 21-day-old rats support those of Catalani et al [42] who showed that GFAP was higher in 11-day-old females than in males, but it increased more in males until it exceeded that in females by day 30 [43]. The only previous study that measured S100B in whole hippocampal homogenates of 1-day-old male and female rats did not detect a sex difference either [66].…”

Section: Discussionsupporting

confidence: 79%

“…They also participate in the synthesis of neurosteroids and the metabolism of sex hormones which can regulate the expression of glial fibrillary acid protein (GFAP) through their glucocorticoid and estrogen receptors [40,41]. GFAP immunoreactivity is age and sex dependent [42] and can be reduced in males by chemical castration and increased in females by testosterone [43]. The astrocyte-specific Ca 2+ -binding protein S100B simulates glial cell proliferation [44], neuronal survival and induces neurite outgrowth [45].…”

Section: Introductionmentioning

confidence: 99%

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Sex-Specific Effects of Prenatal Stress on Memory and Markers of Neuronal Activity in Juvenile Rats

Barbie-Shoshani

Shoham²,

Bejar³

et al. 2016

Dev Neurosci

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Stress during pregnancy can increase the incidence of emotional problems, learning and language difficulties in human infants and pre-adolescents. Most preclinical studies in rats that attempted to find experimental support for these observations were performed in adult male offspring, but the results are inconsistent. The aim of the current study was to examine the effect of prenatal stress on novel object recognition (NOR) and spatial learning and memory in the Morris water maze (MWM) of juvenile rats of both sexes. By the use of fluorescence immunohistochemistry and protein measurements by Western blot, we measured the expression of markers of neurogenesis (doublecortin, DCX) and neuronal activity that are important for synaptic plasticity and learning (c-fos, GluR1, nNOS). Since neuronal activity in the developing and adult brain can be regulated by astrocytes, we also measured the number of astrocytes and the expression of two astroglial proteins (GFAP and S100B) in the stress-responsive hippocampal dentate gyrus (DG). Experiments were performed on littermates of rats in which its effects on behavior were measured. We found for the first time that juvenile females performed better than males in the NOR and MWM tests. They also had higher densities of DCX and c-fos in the DG, together with the expression of nNOS and GluR1 in the subgranular zone (SGZ) of the DG. There were no sex differences in the expression of GFAP and S100B in astrocytes. Prenatal stress did not affect NOR in females, but improved it in males, together with an increase in DCX+ and c-fos, the number of GFAP-expressing astrocytes and the intensity of GFAP and S100B immunofluorescence in the DG. Staining intensity of GluR1 and nNOS in the hilus and SGZ of the DG, and protein expression in the whole DG, was unchanged in prenatally stressed males. Thus, prenatal stress changed the behavior and expression of key proteins in the DG to resemble that in females. A reduction in plasma testosterone, which although not attaining statistical significance was associated with that in anogenital distance, may contribute to the effect of prenatal stress in males. In females, prenatal stress had no effect on c-fos, DCX or the number of astrocytes but reduced the staining intensity of GluR1 and nNOS. Protein expression of nNOS was also significantly lower than that in prenatally stressed males. The differential effects of prenatal stress on hippocampal neuronal and glial markers may help to explain the sex-dependent effect on spatial learning in prepubertal rats.

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Section: Discussionsupporting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Sex-Specific Effects of Prenatal Stress on Memory and Markers of Neuronal Activity in Juvenile Rats

Barbie-Shoshani

Shoham²,

Bejar³

et al. 2016

Dev Neurosci

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show abstract

“…Males were found to have more doublecortin positive cells [47]. During development, sex steroids are also able to modulate astrocytes [110] and a higher number of hippocampal astrocytes in females was found in some [111], [112], but not all [113] studies. In summary, our data indicate that sex-differences in dentate gyrus structure and neurogenesis are already present before sexual maturity is reached.…”

Section: Discussionmentioning

confidence: 94%

Opposite Effects of Early Maternal Deprivation on Neurogenesis in Male versus Female Rats

et al. 2009

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BackgroundMajor depression is more prevalent in women than in men. The underlying neurobiological mechanisms are not well understood, but recent data shows that hippocampal volume reductions in depressed women occur only when depression is preceded by an early life stressor. This underlines the potential importance of early life stress, at least in women, for the vulnerability to develop depression. Perinatal stress exposure in rodents affects critical periods of brain development that persistently alter structural, emotional and neuroendocrine parameters in adult offspring. Moreover, stress inhibits adult hippocampal neurogenesis, a form of structural plasticity that has been implicated a.o. in antidepressant action and is highly abundant early postnatally. We here tested the hypothesis that early life stress differentially affects hippocampal structural plasticity in female versus male offspring.Principal FindingsWe show that 24 h of maternal deprivation (MD) at PND3 affects hippocampal structural plasticity at PND21 in a sex-dependent manner. Neurogenesis was significantly increased in male but decreased in female offspring after MD. Since no other structural changes were found in granule cell layer volume, newborn cell survival or proliferation rate, astrocyte number or gliogenesis, this indicates that MD elicits specific changes in subsets of differentiating cells and differentially affects immature neurons. The MD induced sex-specific effects on neurogenesis cannot be explained by differences in maternal care.ConclusionsOur data shows that early environment has a critical influence on establishing sex differences in neural plasticity and supports the concept that the setpoint for neurogenesis may be determined during perinatal life. It is tempting to speculate that a reduced level of neurogenesis, secondary to early stress exposure, may contribute to maladaptation of the HPA axis and possibly to the increased vulnerability of women to stress-related disorders.

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“…In the hippocampus, astrocyte volume fluctuates with the estrous cycle (Klintsova et al, 1995). Estradiol treatment brings about alterations in the number of astrocytes (Lei et al, 2003;Conejo et al, 2005), reduction in the density of glial processes (Lam and Leranth, 2003), and changes in the expression of glial fibrillary acidic protein (GFAP) (Day et al, 1993). In cultured astrocytes, estradiol was shown to affect astrocyte morphology Del Cerro et al, 1995) and repress GFAP expression (Rozovsky et al, 2002).…”

Section: Introductionmentioning

confidence: 98%

Astrocytes in 17β-estradiol treated mixed hippocampal cultures show attenuated calcium response to neuronal activity

Rao

Sikdar

2006

Glia

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Glial cells in the brain are capable of responding to hormonal signals. The ovarian steroid hormone 17beta-estradiol, in addition to its actions on neurons, can directly affect glial cells. Estrogen receptors have been described on both neurons and astrocytes, suggesting a complex interplay between these two in mediating the effects of the hormone. Astrocytes sense and respond to neuronal activity with a rise in intracellular calcium concentration ([Ca(2+)](i)). Using simultaneous electrophysiology and calcium imaging techniques, we monitored neuronal activity evoked astrocyte ([Ca(2+)](i)) changes in mixed hippocampal cultures loaded with fluo-3 AM. Action potential firing in neurons, elicited by injecting depolarizing current pulses, was associated with ([Ca(2+)](i)) elevations in astrocytes, which could be blocked by 200 microM MCPG and also 1 microM TTX. We compared astrocytic ([Ca(2+)](i)) transients in control and 24-hour estradiol treated cultures. The amplitude of the ([Ca(2+)](i)) transient, the number of responsive astrocytes, and the ([Ca(2+)](i)) wave velocity were all significantly reduced in estradiol treated cultures. ([Ca(2+)](i)) rise in astrocytes in response to local application of the metabotropic glutamate receptor (mGluR) agonist t-ACPD was attenuated in estradiol treated cultures, suggesting functional changes in the astrocyte mGluR following 24-h treatment with estradiol. Since astrocytes can modulate synaptic transmission by release of glutamate, the attenuated ([Ca(2+)](i)) response seen following estradiol treatment could have functional consequences on astrocyte-neuron signaling.

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Influence of gonadal steroids on the glial fibrillary acidic protein‐immunoreactive astrocyte population in young rat hippocampus

Cited by 35 publications

References 48 publications

Sex-Specific Effects of Prenatal Stress on Memory and Markers of Neuronal Activity in Juvenile Rats

Sex-Specific Effects of Prenatal Stress on Memory and Markers of Neuronal Activity in Juvenile Rats

Opposite Effects of Early Maternal Deprivation on Neurogenesis in Male versus Female Rats

Astrocytes in 17β-estradiol treated mixed hippocampal cultures show attenuated calcium response to neuronal activity

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