Effect of Sex Differences on Brain Mitochondrial Function and Its Suppression by Ovariectomy and in Aged Mice

Gaignard, Pauline; Savouroux, Stéphane; Liere, Philippe; Pianos, Antoine; Thérond, Patrice; Schumacher, Michael; Slama, Abdelhamid; Guennoun, Rachida

doi:10.1210/en.2014-1913

Cited by 150Mitochondrial Function and PathologyEstrogen and related hormone effectsReproductive Biology and Fertility

Effect of Sex Differences on Brain Mitochondrial Function and Its Suppression by Ovariectomy and in Aged Mice

Gaignard, Pauline, Savouroux, Stéphane, Liere, Philippe, Pianos, Antoine, Thérond, Patrice, Schumacher, Michael, Slama, Abdelhamid, Guennoun, Rachida·2015·Endocrinology

DOI 10.1210/en.2014-1913

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Abstract

Sex steroids regulate brain function in both normal and pathological states. Mitochondria are an essential target of steroids, as demonstrated by the experimental administration of 17β-estradiol or progesterone (PROG) to ovariectomized female rodents, but the influence of endogenous sex steroids remains understudied. To address this issue, mitochondrial oxidative stress, the oxidative phosphorylation system, and brain steroid levels were analyzed under 3 different experimental sets of endocrine conditions. The first set was designed to study steroid-mediated sex differences in young male and female mice, intact and after gonadectomy. The second set concerned young female mice at 3 time points of the estrous cycle in order to analyze the influence of transient variations in steroid levels. The third set involved the evaluation of the effects of a permanent decrease in gonadal steroids in aged male and female mice. Our results show that young adult females have lower oxidative stress and a higher reduced nicotinamide adenine dinucleotide (NADH)-linked respiration rate, which is related to a higher pyruvate dehydrogenase complex activity as compared with young adult males. This sex difference did not depend on phases of the estrous cycle, was suppressed by ovariectomy but not by orchidectomy, and no longer existed in aged mice. Concomitant analysis of brain steroids showed that pregnenolone and PROG brain levels were higher in females during the reproductive period than in males and decreased with aging in females. These findings suggest that the major male/female differences in brain pregnenolone and PROG levels may contribute to the sex differences observed in brain mitochondrial function.

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Under physiological conditions, sex-specific differences in mitochondrial respiration, bioenergetics, and reactive oxygen species production have been reported in both human and animal studies.
“Under physiological conditions, sex-specific differences in mitochondrial respiration, bioenergetics, and reactive oxygen species production have been reported in both human and animal studies.”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [119]
Mitochondria extracted from brain, liver, and cerebral arteries of female rodents displayed more efficient oxidative phosphorylation than in males.
“mitochondria extracted from brain, liver, and cerebral arteries of female rodents displayed more efficient oxidative phosphorylation than in males”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [119]
Estrogen and progesterone contributed to sex differences in cellular respiration and anti-oxidative functions of brain mitochondria in uninjured female rodents.
“Estrogen and progesterone contributed to sex differences in cellular respiration and anti-oxidative functions of brain mitochondria in uninjured female rodents.”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [119]

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Brain Mitochondrial Metabolism in Males and Females : Endogenous Steroids Influence and Progesterone Effects after Transient Focal Ischemia
Gaignard, P. (2015) · theses.fr (ABES)
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Authors: Gaignard, P., Savouroux, S., Liere, P., Pianos, A., Thérond, P., Schumacher, M., Slama, A., & Guennoun, R.
Affiliations: Université Paris-Sud (FR)
ORCID: Gaignard, Pauline
Pianos, Antoine
Thérond, Patrice
Guennoun, Rachida
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2015-08
Volume: 156
Issue: 8
Pages: 2893-2904
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2014-1913
OpenAlex: W2175348882
Cited by: 150
References: 45
Citations by year: 2026: 8 · 2025: 15 · 2024: 20 · 2023: 23 · 2022: 13 · 2021: 10 · 2020: 9 · 2019: 22 · 2018: 10 · 2017: 14 · 2016: 5 · 2015: 1
FWCI: 4.34
Type: journal article
Language: en
Open access: closed
Locations: Endocrinology (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: Institut National de la Santé et de la Recherche Médicale
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords: sex differences, brain mitochondria, mitochondrial oxidative stress, oxidative phosphorylation, pyruvate dehydrogenase complex, ovariectomy, gonadectomy, estrous cycle, pregnenolone, progesterone, aging, sex steroids
MeSH terms: Aging, Animals, Brain, Estradiol, Flavin-Adenine Dinucleotide, Female, Male, Mice, Inbred C57BL, Mitochondria, NAD, Ovariectomy, Sex Characteristics, Oxidative Stress, Cell Respiration, Mice

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Effect of Sex Differences on Brain Mitochondrial Function and Its Suppression by Ovariectomy and in Aged Mice

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