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Article: Neuroprotective role for RORA in Parkinson's disease revealed by analysis of post-mortem brain and a dopaminergic cell line.

Al-Zaid, Felwah S / Hurley, Michael J / Dexter, David T / Gillies, Glenda E

2023 Volume 9, Issue 1, Page(s) 119

Abstract: Parkinson's disease (PD) is almost twice as prevalent in men, which has largely been attributed to neuroprotective effect of oestradiol in women. RORA (retinoic acid receptor-related orphan receptor alpha) regulates the transcription of central aromatase, ...

Abstract	Parkinson's disease (PD) is almost twice as prevalent in men, which has largely been attributed to neuroprotective effect of oestradiol in women. RORA (retinoic acid receptor-related orphan receptor alpha) regulates the transcription of central aromatase, the enzyme responsible for local oestradiol synthesis, simultaneously, RORA expression is regulated by sex hormones. Moreover, RORA protects neurones against oxidative stress, a key mechanism contributing to the loss of dopaminergic neurones in PD. Therefore, we hypothesized that there would be sex differences in RORA expression in the substantia nigra pars compacta (SNpc), which could contribute to sex differences observed in PD prevalence and pathogenesis. In a case control study, qPCR and western blot analyses were used to quantify gene and protein expression in the SNpc of post-mortem brains (n = 14 late-stage PD and 11 age and sex matched controls). The neuroprotective properties of a RORA agonist were then investigated directly using a cell culture toxin-based model of PD coupled with measures of viability, mitochondrial function and apoptosis. RORA was expressed at significantly higher levels in the SNpc from control females' brains compared to males. In PD, we found a significant increase in SNpc RORA expression in male PD compared to female PD. Treatment with a RORA agonist showed a significant neuroprotection in our cell culture model of PD and revealed significant effects on intracellular factors involved in neuronal survival and demise. This study is the first to demonstrate a sex specific pattern of RORA protein and gene expression in the SNpc of controls post-mortem human brains, and to show that this is differentially altered in male and female PD subjects, thus supporting a role for RORA in sex-specific aspects of PD. Furthermore, our in vitro PD model indicates mechanisms whereby a RORA agonist exerts its neuroprotective effect, thereby highlighting the translational potential for RORA ligands in PD.
Language	English
Publishing date	2023-07-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	2819218-7
ISSN	2373-8057
ISSN	2373-8057
DOI	10.1038/s41531-023-00563-4
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Article ; Online: Astroglial Plasticity Is Implicated in Hippocampal Remodelling in Adult Rats Exposed to Antenatal Dexamethasone

Vishvesh H. Shende / Simon McArthur / Glenda E. Gillies / Jolanta Opacka-Juffry

Neural Plasticity, Vol

2015 Volume 2015

Keywords	Medicine ; R ; Internal medicine ; RC31-1245 ; Neurosciences. Biological psychiatry. Neuropsychiatry ; RC321-571
Publishing date	2015-01-01T00:00:00Z
Publisher	Hindawi Publishing Corporation
Document type	Article ; Online
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Article ; Online: Sex differences in Parkinson's disease.

Gillies, Glenda E / Pienaar, Ilse S / Vohra, Shiv / Qamhawi, Zahi

Frontiers in neuroendocrinology

2014 Volume 35, Issue 3, Page(s) 370–384

Abstract: Parkinson's disease (PD) displays a greater prevalence and earlier age at onset in men. This review addresses the concept that sex differences in PD are determined, largely, by biological sex differences in the NSDA system which, in turn, arise from ... ...

Abstract	Parkinson's disease (PD) displays a greater prevalence and earlier age at onset in men. This review addresses the concept that sex differences in PD are determined, largely, by biological sex differences in the NSDA system which, in turn, arise from hormonal, genetic and environmental influences. Current therapies for PD rely on dopamine replacement strategies to treat symptoms, and there is an urgent, unmet need for disease modifying agents. As a significant degree of neuroprotection against the early stages of clinical or experimental PD is seen, respectively, in human and rodent females compared with males, a better understanding of brain sex dimorphisms in the intact and injured NSDA system will shed light on mechanisms which have the potential to delay, or even halt, the progression of PD. Available evidence suggests that sex-specific, hormone-based therapeutic agents hold particular promise for developing treatments with optimal efficacy in men and women.
MeSH term(s)	Animals ; Dopamine/therapeutic use ; Gonadal Steroid Hormones/metabolism ; Humans ; Neuroprotective Agents/therapeutic use ; Parkinson Disease/drug therapy ; Sex Characteristics ; Substantia Nigra/drug effects
Chemical Substances	Gonadal Steroid Hormones ; Neuroprotective Agents ; Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2014-03-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	390985-2
ISSN	1095-6808 ; 0532-7466 ; 0091-3022
ISSN (online)	1095-6808
ISSN	0532-7466 ; 0091-3022
DOI	10.1016/j.yfrne.2014.02.002
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Article: Enduring, Sexually Dimorphic Impact of In Utero Exposure to Elevated Levels of Glucocorticoids on Midbrain Dopaminergic Populations.

Gillies, Glenda E / Virdee, Kanwar / Pienaar, Ilse / Al-Zaid, Felwah / Dalley, Jeffrey W

Brain sciences

2016 Volume 7, Issue 1

Abstract: Glucocorticoid hormones (GCs) released from the fetal/maternal glands during late gestation are required for normal development of mammalian organs and tissues. Accordingly, synthetic glucocorticoids have proven to be invaluable in perinatal medicine ... ...

Abstract	Glucocorticoid hormones (GCs) released from the fetal/maternal glands during late gestation are required for normal development of mammalian organs and tissues. Accordingly, synthetic glucocorticoids have proven to be invaluable in perinatal medicine where they are widely used to accelerate fetal lung maturation when there is risk of pre-term birth and to promote infant survival. However, clinical and pre-clinical studies have demonstrated that inappropriate exposure of the developing brain to elevated levels of GCs, either as a result of clinical over-use or after stress-induced activation of the fetal/maternal adrenal cortex, is linked with significant effects on brain structure, neurological function and behaviour in later life. In order to understand the underlying neural processes, particular interest has focused on the midbrain dopaminergic systems, which are critical regulators of normal adaptive behaviours, cognitive and sensorimotor functions. Specifically, using a rodent model of GC exposure in late gestation (approximating human brain development at late second/early third trimester), we demonstrated enduring effects on the shape and volume of the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) (origins of the mesocorticolimbic and nigrostriatal dopaminergic pathways) on the topographical organisation and size of the dopaminergic neuronal populations and astrocytes within these nuclei and on target innervation density and neurochemical markers of dopaminergic transmission (receptors, transporters, basal and amphetamine-stimulated dopamine release at striatal and prefrontal cortical sites) that impact on the adult brain. The effects of antenatal GC treatment (AGT) were both profound and sexually-dimorphic, not only in terms of quantitative change but also qualitatively, with several parameters affected in the opposite direction in males and females. Although such substantial neurobiological changes might presage marked behavioural effects, in utero GC exposure had only a modest or no effect, depending on sex, on a range of conditioned and unconditioned behaviours known to depend on midbrain dopaminergic transmission. Collectively, these findings suggest that apparent behavioural normality in certain tests, but not others, arises from AGT-induced adaptations or compensatory mechanisms within the midbrain dopaminergic systems, which preserve some, but not all functions. Furthermore, the capacities for molecular adaptations to early environmental challenge are different, even opponent, in males and females, which may account for their differential resilience or failure to perform adequately in behavioural tests. Behavioural "normality" is thus achieved by the midbrain dopaminergic network operating outside its normal limits (in a state of allostasis), rendering it at greater risk to malfunction when challenged in later life. Sex-specific neurobiological programming of midbrain dopaminergic systems may, therefore, have psychopathological relevance for the sex bias commonly found in brain disorders associated with these systems, and which have a neurodevelopmental component, including schizophrenia, ADHD (attention/deficit hyperactivity disorders), autism, depression and substance abuse.
Language	English
Publishing date	2016-12-30
Publishing country	Switzerland
Document type	Review ; Journal Article
ZDB-ID	2651993-8
ISSN	2076-3425
ISSN	2076-3425
DOI	10.3390/brainsci7010005
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Article ; Online: Enduring, Sexually Dimorphic Impact of In Utero Exposure to Elevated Levels of Glucocorticoids on Midbrain Dopaminergic Populations

Glenda E. Gillies / Kanwar Virdee / Ilse Pienaar / Felwah Al-Zaid / Jeffrey W. Dalley

Brain Sciences, Vol 7, Iss 1, p

2016 Volume 5

Abstract	Glucocorticoid hormones (GCs) released from the fetal/maternal glands during late gestation are required for normal development of mammalian organs and tissues. Accordingly, synthetic glucocorticoids have proven to be invaluable in perinatal medicine where they are widely used to accelerate fetal lung maturation when there is risk of pre-term birth and to promote infant survival. However, clinical and pre-clinical studies have demonstrated that inappropriate exposure of the developing brain to elevated levels of GCs, either as a result of clinical over-use or after stress-induced activation of the fetal/maternal adrenal cortex, is linked with significant effects on brain structure, neurological function and behaviour in later life. In order to understand the underlying neural processes, particular interest has focused on the midbrain dopaminergic systems, which are critical regulators of normal adaptive behaviours, cognitive and sensorimotor functions. Specifically, using a rodent model of GC exposure in late gestation (approximating human brain development at late second/early third trimester), we demonstrated enduring effects on the shape and volume of the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) (origins of the mesocorticolimbic and nigrostriatal dopaminergic pathways) on the topographical organisation and size of the dopaminergic neuronal populations and astrocytes within these nuclei and on target innervation density and neurochemical markers of dopaminergic transmission (receptors, transporters, basal and amphetamine-stimulated dopamine release at striatal and prefrontal cortical sites) that impact on the adult brain. The effects of antenatal GC treatment (AGT) were both profound and sexually-dimorphic, not only in terms of quantitative change but also qualitatively, with several parameters affected in the opposite direction in males and females. Although such substantial neurobiological changes might presage marked behavioural effects, in utero GC exposure had only a modest or no effect, depending on sex, on a range of conditioned and unconditioned behaviours known to depend on midbrain dopaminergic transmission. Collectively, these findings suggest that apparent behavioural normality in certain tests, but not others, arises from AGT-induced adaptations or compensatory mechanisms within the midbrain dopaminergic systems, which preserve some, but not all functions. Furthermore, the capacities for molecular adaptations to early environmental challenge are different, even opponent, in males and females, which may account for their differential resilience or failure to perform adequately in behavioural tests. Behavioural “normality” is thus achieved by the midbrain dopaminergic network operating outside its normal limits (in a state of allostasis), rendering it at greater risk to malfunction when challenged in later life. Sex-specific neurobiological programming of midbrain dopaminergic systems may, therefore, have psychopathological relevance for the sex bias commonly found in brain disorders associated with these systems, and which have a neurodevelopmental component, including schizophrenia, ADHD (attention/deficit hyperactivity disorders), autism, depression and substance abuse.
Keywords	dopaminergic neurones ; astrocytes ; midbrain ; ventral tegmental area ; substantia nigra pars compacta ; antenatal glucocorticoid treatment ; developmental programming ; sex dimorphisms ; Medicine ; R ; Internal medicine ; RC31-1245 ; Neurosciences. Biological psychiatry. Neuropsychiatry ; RC321-571
Subject code	616
Language	English
Publishing date	2016-12-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: Peripheral vs. Central Sex Steroid Hormones in Experimental Parkinson's Disease.

McArthur, Simon / Gillies, Glenda E

Frontiers in endocrinology

2011 Volume 2, Page(s) 82

Abstract: The nigrostriatal dopaminergic (NSDA) pathway degenerates in Parkinson's disease (PD), which occurs with approximately twice the incidence in men than women. Studies of the influence of systemic estrogens in females suggest sex hormones contribute to ... ...

Abstract	The nigrostriatal dopaminergic (NSDA) pathway degenerates in Parkinson's disease (PD), which occurs with approximately twice the incidence in men than women. Studies of the influence of systemic estrogens in females suggest sex hormones contribute to these differences. In this review we analyze the evidence revealing great complexity in the response of the healthy and injured NSDA system to hormonal influences, and emphasize the importance of centrally generated estrogens. At physiological levels, circulating estrogen (in females) or estrogen precursors (testosterone in males, aromatized to estrogen centrally) have negligible effects on dopaminergic neuron survival in experimental PD, but can modify striatal dopamine levels via actions on the activity or adaptive responses of surviving cells. However, these effects are sexually dimorphic. In females, estradiol promotes adaptive responses in the partially injured NSDA pathway, preserving striatal dopamine, whereas in males gonadal steroids and exogenous estradiol have a negligible or even suppressive effect, effectively exacerbating dopamine loss. On balance, the different effects of gonadal factors in males and females contribute to sex differences in experimental PD. Fundamental sex differences in brain organization, including the sexually dimorphic networks regulating NSDA activity are likely to underpin these responses. In contrast, estrogen generated locally appears to preserve striatal dopamine in both sexes. The available data therefore highlight the need to understand the biological basis of sex-specific responses of the NSDA system to peripheral hormones, so as to realize the potential for sex-specific, hormone-based therapies in PD. Furthermore, they suggest that targeting central steroid generation could be equally effective in preserving striatal dopamine in both sexes. Clarification of the relative roles of peripheral and central sex steroid hormones is thus an important challenge for future studies.
Language	English
Publishing date	2011-11-30
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2592084-4
ISSN	1664-2392 ; 1664-2392
ISSN (online)	1664-2392
ISSN	1664-2392
DOI	10.3389/fendo.2011.00082
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Article ; Online: Astroglial Plasticity Is Implicated in Hippocampal Remodelling in Adult Rats Exposed to Antenatal Dexamethasone.

Shende, Vishvesh H / McArthur, Simon / Gillies, Glenda E / Opacka-Juffry, Jolanta

Neural plasticity

2015 Volume 2015, Page(s) 694347

Abstract: The long-term effects of antenatal dexamethasone treatment on brain remodelling in 3-month-old male Sprague Dawley rats whose mothers had been treated with dexamethasone were investigated in the present study. Dorsal hippocampus, basolateral amygdala and ...

Abstract	The long-term effects of antenatal dexamethasone treatment on brain remodelling in 3-month-old male Sprague Dawley rats whose mothers had been treated with dexamethasone were investigated in the present study. Dorsal hippocampus, basolateral amygdala and nucleus accumbens volume, cell numbers, and GFAP-immunoreactive astroglial cell morphology were analysed using stereology. Total brain volume as assessed by micro-CT was not affected by the treatment. The relative volume of the dorsal hippocampus (% of total brain volume) showed a moderate, by 8%, but significant reduction in dexamethasone-treated versus control animals. Dexamethasone had no effect on the total and GFAP-positive cell numbers in the hippocampal subregions, basolateral amygdala, and nucleus accumbens. Morphological analysis indicated that numbers of astroglial primary processes were not affected in any of the hippocampal subregions analysed but significant reductions in the total primary process length were observed in CA1 by 32%, CA3 by 50%, and DG by 25%. Mean primary process length values were also significantly decreased in CA1 by 25%, CA3 by 45%, and DG by 25%. No significant astroglial morphological changes were found in basolateral amygdala and nucleus accumbens. We propose that the dexamethasone-dependent impoverishment of hippocampal astroglial morphology is the case of maladaptive glial plasticity induced prenatally.
MeSH term(s)	Animals ; Astrocytes/drug effects ; Astrocytes/ultrastructure ; CA1 Region, Hippocampal/drug effects ; CA1 Region, Hippocampal/pathology ; CA3 Region, Hippocampal/drug effects ; CA3 Region, Hippocampal/pathology ; Cell Count ; Dexamethasone/pharmacology ; Female ; Glial Fibrillary Acidic Protein/metabolism ; Hippocampus/cytology ; Hippocampus/drug effects ; Immunohistochemistry ; Male ; Neuroglia/drug effects ; Neuroglia/ultrastructure ; Neuronal Plasticity/drug effects ; Organ Size/drug effects ; Pregnancy ; Prenatal Exposure Delayed Effects/pathology ; Rats ; Rats, Sprague-Dawley
Chemical Substances	Glial Fibrillary Acidic Protein ; Dexamethasone (7S5I7G3JQL)
Language	English
Publishing date	2015
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1454938-4
ISSN	1687-5443 ; 2090-5904 ; 0792-8483
ISSN (online)	1687-5443
ISSN	2090-5904 ; 0792-8483
DOI	10.1155/2015/694347
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Article ; Online: Novel ontogenetic patterns of sexual differentiation in arcuate nucleus GHRH neurons revealed in GHRH-enhanced green fluorescent protein transgenic mice.

McArthur, Simon / Robinson, Iain C / Gillies, Glenda E

Endocrinology

2011 Volume 152, Issue 2, Page(s) 607–617

Abstract: GH secretion and growth rates are developmentally regulated and sexually dimorphic, but the neuroregulatory mechanisms between birth and puberty are unclear. Using the GHRH-enhanced green fluorescent protein (eGFP) transgenic mouse, in which eGFP ... ...

Abstract	GH secretion and growth rates are developmentally regulated and sexually dimorphic, but the neuroregulatory mechanisms between birth and puberty are unclear. Using the GHRH-enhanced green fluorescent protein (eGFP) transgenic mouse, in which eGFP provides a strong surrogate signal for identifying GHRH neurons, we showed that numbers in the male arcuate nucleus were double those seen in females at x postnatal day (P)1 and P10, during which time numbers increased 2- to 3-fold. Thereafter (P20, P30, P60, P365) there was a significant trend for numbers to decrease in males and increase in females, such that sex differences were, surprisingly, absent in young and late adulthood. Conversely, we identified the emergence of male-dominant sex differences in the number of processes extended per GHRH perikarya across puberty. Intriguingly, prepubertal gonadectomy (P28), unlike adult gonadectomy, caused a dramatic 40% loss of GHRH cells in both sexes in adulthood and a significant (30%) increase in processes emanating from cell bodies only in females. These findings establish a novel ontogenetic profile for GHRH neurons and suggest previously undiscovered roles for peripubertal gonadal factors in establishing population size in both sexes. They also provide the first demonstration of emergent sex-specific GHRH architecture, which may signal the onset of sex-dependent regulation of activity reported for adult GHRH-eGFP neurons, and its differential regulation by gonadal factors in males and females. This information adds to our knowledge of processes that underpin the emergence of sex-specific GH secretory dynamics and hence biological activity of this pleiotropic hormone.
MeSH term(s)	Animals ; Arcuate Nucleus of Hypothalamus/metabolism ; Female ; Green Fluorescent Proteins/genetics ; Green Fluorescent Proteins/metabolism ; Growth Hormone-Releasing Hormone/metabolism ; Immunohistochemistry ; Male ; Mice ; Mice, Transgenic ; Sex Differentiation/physiology
Chemical Substances	enhanced green fluorescent protein ; Green Fluorescent Proteins (147336-22-9) ; Growth Hormone-Releasing Hormone (9034-39-3)
Language	English
Publishing date	2011-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	427856-2
ISSN	1945-7170 ; 0013-7227
ISSN (online)	1945-7170
ISSN	0013-7227
DOI	10.1210/en.2010-0798
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Article ; Online: Sex-specific disruption of murine midbrain astrocytic and dopaminergic developmental trajectories following antenatal GC treatment.

McArthur, Simon / Pienaar, Ilse S / Siddiqi, Sindhu M / Gillies, Glenda E

Brain structure & function

2015 Volume 221, Issue 5, Page(s) 2459–2475

Abstract: The mammalian midbrain dopaminergic systems arising in the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA) are critical for coping behaviours and are implicated in neuropsychiatric disorders where early life challenges comprise ... ...

Abstract	The mammalian midbrain dopaminergic systems arising in the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA) are critical for coping behaviours and are implicated in neuropsychiatric disorders where early life challenges comprise significant risk factors. Here, we aimed to advance our hypothesis that glucocorticoids (GCs), recognised key players in neurobiological programming, target development within these systems, with a novel focus on the astrocytic population. Mice received antenatal GC treatment (AGT) by including the synthetic GC, dexamethasone, in the mothers' drinking water on gestational days 16-19; controls received normal drinking water. Analyses of regional shapes and volumes of the adult SNc and VTA demonstrated that AGT induced long-term, dose-dependent, structural changes that were accompanied by profound effects on astrocytes (doubling/tripling of numbers and/or density). Additionally, AGT induced long-term changes in the population size and distribution of SNc/VTA dopaminergic neurons, confirming and extending our previous observations made in rats. Furthermore, glial/neuronal structural remodelling was sexually dimorphic and depended on the AGT dose and sub-region of the SNc/VTA. Investigations within the neonatal brain revealed that these long-term organisational effects of AGT depend, at least in part, on targeting perinatal processes that determine astrocyte density and programmed cell death in dopaminergic neurons. Collectively, our characterisation of enduring, AGT-induced, sex-specific cytoarchitectural disturbances suggests novel mechanistic links for the strong association between early environmental challenge (inappropriate exposure to excess GCs) and vulnerability to developing aberrant behaviours in later life, with translational implications for dopamine-associated disorders (such as schizophrenia, ADHD, autism, depression), which typically show a sex bias.
MeSH term(s)	Animals ; Apoptosis/drug effects ; Astrocytes/drug effects ; Astrocytes/physiology ; Cell Count ; Dexamethasone/administration & dosage ; Dopaminergic Neurons/drug effects ; Dopaminergic Neurons/physiology ; Female ; Glucocorticoids/administration & dosage ; Male ; Mice ; Mice, Inbred C57BL ; Pars Compacta/drug effects ; Pars Compacta/growth & development ; Pars Compacta/metabolism ; Pregnancy ; Prenatal Exposure Delayed Effects/physiopathology ; Sex Characteristics ; Tyrosine 3-Monooxygenase/metabolism ; Ventral Tegmental Area/drug effects ; Ventral Tegmental Area/growth & development ; Ventral Tegmental Area/metabolism
Chemical Substances	Glucocorticoids ; Dexamethasone (7S5I7G3JQL) ; Tyrosine 3-Monooxygenase (EC 1.14.16.2)
Language	English
Publishing date	2015-05-06
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2273162-3
ISSN	1863-2661 ; 1863-2653
ISSN (online)	1863-2661
ISSN	1863-2653
DOI	10.1007/s00429-015-1049-0
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Article ; Online: Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines.

Gillies, Glenda E / McArthur, Simon

Pharmacological reviews

2010 Volume 62, Issue 2, Page(s) 155–198

Abstract: The classic view of estrogen actions in the brain was confined to regulation of ovulation and reproductive behavior in the female of all mammalian species studied, including humans. Burgeoning evidence now documents profound effects of estrogens on ... ...

Abstract	The classic view of estrogen actions in the brain was confined to regulation of ovulation and reproductive behavior in the female of all mammalian species studied, including humans. Burgeoning evidence now documents profound effects of estrogens on learning, memory, and mood as well as neurodevelopmental and neurodegenerative processes. Most data derive from studies in females, but there is mounting recognition that estrogens play important roles in the male brain, where they can be generated from circulating testosterone by local aromatase enzymes or synthesized de novo by neurons and glia. Estrogen-based therapy therefore holds considerable promise for brain disorders that affect both men and women. However, as investigations are beginning to consider the role of estrogens in the male brain more carefully, it emerges that they have different, even opposite, effects as well as similar effects in male and female brains. This review focuses on these differences, including sex dimorphisms in the ability of estradiol to influence synaptic plasticity, neurotransmission, neurodegeneration, and cognition, which, we argue, are due in a large part to sex differences in the organization of the underlying circuitry. There are notable sex differences in the incidence and manifestations of virtually all central nervous system disorders, including neurodegenerative disease (Parkinson's and Alzheimer's), drug abuse, anxiety, and depression. Understanding the cellular and molecular basis of sex differences in brain physiology and responses to estrogen and estrogen mimics is, therefore, vitally important for understanding the nature and origins of sex-specific pathological conditions and for designing novel hormone-based therapeutic agents that will have optimal effectiveness in men or women.
MeSH term(s)	Alzheimer Disease/metabolism ; Animals ; Brain/drug effects ; Brain Diseases/etiology ; Brain Diseases/metabolism ; Estrogens/metabolism ; Estrogens/pharmacology ; Female ; Humans ; Hypothalamus/drug effects ; Hypothalamus/metabolism ; Learning/drug effects ; Male ; Memory/drug effects ; Parkinson Disease/metabolism ; Rats ; Sex Factors
Chemical Substances	Estrogens
Language	English
Publishing date	2010-04-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	209898-2
ISSN	1521-0081 ; 0031-6997
ISSN (online)	1521-0081
ISSN	0031-6997
DOI	10.1124/pr.109.002071
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