Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones
Open accessAbstract
Astroglia and steroid hormones such as estrogen and progesterone regulate cell growth, function, and protection in the central nervous system (CNS). It appears that astrocytes and steroids act in concert to promote cell survival under pathological conditions. With respect to the role of mitochondrial fusion and fission in energy metabolism, apoptosis, and proliferation, astrocyte mitochondria resemble a perfect intracellular target for steroids to modulate these processes, thereby promoting cell vitality after damage. We have studied the effects of estrogen and progesterone on cell viability in comparison with mitochondrial fusion and fission gene transcription in primary cortical astrocytes from female and male mouse brains. Estrogen- and progesterone-treated female astrocytes demonstrated an increase in cell number and proliferation marker accompanied by an upregulation of fusion and fission gene transcription, which were apparently balancing pro- and anti-apoptotic processes. On the other hand, male astrocytes exhibited no change in cell number after estrogen treatment, but a decrease after progesterone administration. This could be the consequence of stimulated apoptosis in male astrocytes by both steroids, which was counterbalanced by an increased proliferation in the presence of estrogen, whereas it was strengthened in the presence of progesterone. Supportively, estrogen promoted and progesterone decreased the transcription of fusion and fission genes. We suggest that estrogen and progesterone affect mitochondrial fusion and fission gene transcription in cortical astrocytes in a gender-specific way, thereby influencing mitochondrial function differently in both genders. Thus, interaction of sex steroids with mitochondria may represent one possible cause for gender differences in cellular pathology in the CNS.
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Estrogen and progesterone upregulated transcription of fission and fusion genes in astrocytes of uninjured female mice.
“They upregulated transcription of fission and fusion genes in astrocytes of uninjured female mice”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [142]
Estrogen and progesterone decreased transcription of fission and fusion genes in males.
“but decreased the transcription of these genes in males.”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [142]
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BackgroundGaignard, P., Lière, P., Thérond, P., Schumacher, M., Slama, A., & Guennoun, R. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00406 · Cited by 127 · see citing works
“In contrast, in WT male mice cortical astrocytes, 17β-estradiol enhanced the expression of fission genes and of one fusion gene (MFN2) and decreased the expression of the second fusion gene (MFN1); while progesterone decreased both fission and fusion gene expressions (Arnold et al., 2008).”
ResultRegulation of astroglia by gonadal steroid hormones under physiological and pathological conditions
Acaz‐Fonseca, E., Ávila-Rodriguez, M., García‐Segura, L. M., & Barreto, G. E. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.06.002 · Cited by 126 · see citing works
Johann, S., & Beyer, C. (2012) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2012.11.006 · Cited by 113 · see citing works
Self-citationImpact of sex steroids on neuroinflammatory processes and experimental multiple sclerosis
Kipp, M., & Beyer, C. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.04.004 · Cited by 108 · see citing works
Self-citationLabombarda, F., González, S. L., Lima, A. E., Roig, P., Guennoun, R., Schumacher, M., & Nicola, A. F. D. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.06.001 · Cited by 108 · see citing works
Arnold, S., & Beyer, C. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06133.x · Cited by 95 · see citing works
“In the literature, there are several reports suggesting mitochondria as a putative and promising target for estrogen-mediated cell protection (Araujo et al. 2008; Arnold et al. 2008; Brinton 2008; Klinge 2008; Simpkins and Dykens 2008).”
BackgroundResultSelf-citationAstrocytic response to cerebral ischemia is influenced by sex differences and impaired by aging
Chisholm, N. C., & Sohrabji, F. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.03.028 · Cited by 89 · see citing works
“tors (Azcoitia et al., 1999; Pawlak et al., 2005b; Arnold et al., 2008; Duncan et al., 2013; Kuo et al., 2010b) and estradiol facilitates the syn-”
Multiple sclerosis: Neuroprotective alliance of estrogen–progesterone and gender
Kipp, M., Amor, S., Krauth, R., & Beyer, C. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.01.001 · Cited by 84 · see citing works
Self-citationChowen, J. A., & García‐Segura, L. M. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111473 · Cited by 89 · see citing works
Sex differences in brain mitochondrial metabolism: influence of endogenous steroids and stroke
Gaignard, P., Fréchou, M., Lière, P., Thérond, P., Schumacher, M., Slama, A., & Guennoun, R. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12497 · Cited by 76 · see citing works
Cytochrome c Oxidase and Its Role in Neurodegeneration and Neuroprotection
Arnold, S. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3573-0_13 · Cited by 75 · see citing works
Self-citationZárate, S., Traetta, M. E., Codagnone, M. G., Seilicovich, A., & Reinés, A. G. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00123 · Cited by 70 · see citing works
Sharma, J., Johnston, M. V., & Hossain, M. A. (2014) · BMC Neuroscience · doi:10.1186/1471-2202-15-9 · Cited by 67 · see citing works
“The sequence of primers for mitochondrial fusion and fission used are; Mfn15’- CAGAGAAGAGGGTTTATTCA-3’ (sense) and 5’- ACTCATCAACCAAAACAGAT-3’ (antisense), Mfn 2 5’- TGAATGTTGTGTTCTTTCTG-3’ (sense) and 5’- AA GTGCTCTCTGCTAAATGT-3’ (antisense), Drp1 5’- TTT GCTCGTGTGAAGACTGG-3’ (sense) and 5’- TCCTGG AGCTTCCTTTCTGA-3’…”
BackgroundMethodInfluentialEffects of Estrogen in the Brain: Is it a Neuroprotective Agent in Alzheimers Disease?
Correia, S. C., Santos, R. X., Cardoso, S., Carvalho, C., Santos, M. S., Oliveira, C. R., & Moreira, P. I. (2010) · Current Aging Science · doi:10.2174/1874609811003020113 · Cited by 67 · see citing works
Myatt, L., Muralimanoharan, S., & Maloyan, A. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1031-1_12 · Cited by 62 · see citing works
Estrogen and the regulation of mitochondrial structure and function in the brain
Arnold, S., Victor, M. B., & Beyer, C. (2012) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2012.01.012 · Cited by 57 · see citing works
Self-citationMisiak, M., Beyer, C., & Arnold, S. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.04.009 · Cited by 55 · see citing works
Self-citationLabombarda, F., Jure, I., González, S. L., Lima, A. E., Roig, P., Guennoun, R., Schumacher, M., & Nicola, A. F. D. (2015) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.09.011 · Cited by 48 · see citing works
Mitochondrial function in human brains is affected by pre‐ and post mortem factors
Harish, G., Venkateshappa, C., Mahadevan, A., Pruthi, N., Bharath, M. M. S., & Shankar, S. K. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01285.x · Cited by 45 · see citing works
Boyalla, S. S., Victor, M. B., Roemgens, A., Beyer, C., & Arnold, S. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22669 · Cited by 45 · see citing works
“For sex-specific studies, the sex of the donor was determined by visual inspection of the anogenital distance, which is larger in male than in female mice (Arnold et al., 2008).”
BackgroundMethodSelf-citationMurru, S., Heß, S., Barth, E., Almajan, E.-R., Schatton, D., Hermans, S., Brodesser, S., Langer, T., Kloppenburg, P., & Rugarli, E. I. (2019) · Glia · doi:10.1002/glia.23626 · Cited by 45 · see citing works
“In addition, AFG3L2 can assemble in functional hetero-oligomeric complexes with the homologous subunit SPG7 (also called paraplegin; Banfi et al., 1999; Casari et al., 1998; Koppen, Metodiev, Casari, Rugarli, & Langer, 2007).”
BackgroundOestrogenic Regulation of Mitochondrial Dynamics
Kalkhoran, S. B., & Kararigas, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031118 · Cited by 48 · see citing works
“The reduction of Mfn1 was correlated with a reduction the levels of anti-apoptotic Bcl2 in these cells [159].”
BackgroundMitochondrial Polymorphisms Impact Outcomes after Severe Traumatic Brain Injury
Conley, Y. P., Okonkwo, D. O., Deslouches, S., Alexander, S. A., Puccio, A. M., Beers, S. R., & Ren, D. (2013) · Journal of Neurotrauma · doi:10.1089/neu.2013.2855 · Cited by 38 · see citing works
Combined effects of rat Schwann cells and 17β-estradiol in a spinal cord injury model
Namjoo, Z., Moradi, F., Aryanpour, R., Piryaei, A., Joghataei, M. T., Abbasi, Y., Hosseini, A., Hassanzadeh, S., Taklimie, F. R., Beyer, C., et al. (2018) · Metabolic Brain Disease · doi:10.1007/s11011-018-0220-8 · Cited by 34 · see citing works
Self-citationBian, C., Zhu, K., Guo, Q., Xiong, Y., Cai, W., & Zhang, J. (2011) · Steroids · doi:10.1016/j.steroids.2011.11.002 · Cited by 30 · see citing works
“P0 was defined as within 24 h after birth, the sex was determined by visual inspection of the anogenital distance, which is larger in male than in female mice [40].”
BackgroundPossible roles of astrocytes in estrogen neuroprotection during cerebral ischemia
Wang, C., Jie, C., & Dai, X. (2014) · Reviews in the Neurosciences · doi:10.1515/revneuro-2013-0055 · Cited by 28 · see citing works
Cheng, W., Yang, S., Li, X., Liang, F., Zhou, R., Wang, H., Feng, Y., & Wang, Y. (2019) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2019.114850 · Cited by 29 · see citing works
Axonal transport in a peripheral diabetic neuropathy model: sex-dimorphic features
Pesaresi, M., Giatti, S., Spezzano, R., Romano, S., Diviccaro, S., Borsello, T., Mitro, N., Caruso, D., García‐Segura, L. M., & Melcangi, R. C. (2018) · Biology of Sex Differences · doi:10.1186/s13293-018-0164-z · Cited by 25 · see citing works
“Estradiol and progesterone are also able to modulate mitochondrial fusion and fission genes, stimulating MFN1 and MFN2 expression [67].”
BackgroundEffect of sex and gonadectomy on brain MPTP toxicity and response to dutasteride treatment in mice
Isenbrandt, A., Morissette, M., Bourque, M., Lamontagne‐Proulx, J., Coulombe, K., Soulet, D., & Paolo, T. D. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108784 · Cited by 23 · see citing works
Sex differences and the role of estrogens in the immunological underpinnings of Alzheimer's disease
Price, B. R., Walker, K. A., Eissman, J. M., Suryadevara, V., Sime, L. N., Hohman, T. J., & Gordon, M. N. (2025) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.70139 · Cited by 23 · see citing works
Age-related ultrastructural neurovascular changes in the female mouse cortex and hippocampus
Frías-Anaya, E., Gromnicova, R., Kraev, I., Rogachevsky, V. V., Male, D. K., Crea, F., Hawkes, C. A., & Romero, I. A. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.12.008 · Cited by 19 · see citing works
“Indeed, sex-dependent increase in astrocyte number, in addition to the above-mentioned astrocyte increased viability due to higher levels of mitochondrial fusion (Arnold et al., 2008), might attenuate the ageing effect on astrocytic end-feet coverage in the female BBB.”
BackgroundMisiak, M., Singh, S., Drewlo, S., Beyer, C., & Arnold, S. (2010) · Cell and Tissue Research · doi:10.1007/s00441-010-0995-3 · Cited by 19 · see citing works
“Astroglial cultures were prepared from postnatal day 1 BALB/c mice as previously documented (Arnold et al. 2008).”
MethodSelf-citationShaw, R. L., Norton, C. E., & Segal, S. S. (2021) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00956.2020 · Cited by 18 · see citing works
Stanley, J. A., Aruldhas, M. M., Yuvaraju, P. B., Banu, S. K., Jaganathan, A., Neelamohan, R., Annapoorna, K., & Jayaraman, G. (2010) · Steroids · doi:10.1016/j.steroids.2010.06.009 · Cited by 17 · see citing works
Siddiqui, N., Sharma, A. K., Kesharwani, A., Anurag, & Parihar, V. K. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102282 · Cited by 16 · see citing works
Sex-Specific Effects of Estradiol and Progesterone in Ischemic Kidney Injury
Andrianova, N. V., Brezgunova, A. A., Buyan, M. I., Makievskaya, C. I., Buyan, A., Cherkesova, K. S., Pevzner, I. B., Zorova, L. D., Zorov, D. B., Plotnikov, E. Y., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25063155 · Cited by 15 · see citing works
MicroRNA as biomarkers of mitochondrial toxicity
Baumgart, B. R., Gray, K. L., Woicke, J., Bunch, R. T., Sanderson, T. P., & Vleet, T. R. V. (2015) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2015.10.007 · Cited by 14 · see citing works
Sex differences and altered mitophagy in experimental pulmonary hypertension
Bazan, I. S., Kim, S., Ardito, T. A., Zhang, Y., Shan, P., Sauler, M., & Lee, P. J. (2022) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00019.2020 · Cited by 14 · see citing works
Potential use of adult bovine serum obtained during the slaughtering process as a biological reagent
Yu, J. E., Kim, M., Pokharel, S., Kim, J., Choi, I., Choe, N., & Nahm, S. (2013) · Animal Cells and Systems · doi:10.1080/19768354.2013.772073 · Cited by 13 · see citing works
“Previous results showed that only astrocytes derived from female mice, but not from male mice, exhibited enhanced proliferation with female serum supplementation (Arnold et al. 2008).”
ResultBrain Volume Loss, Astrocyte Reduction, and Inflammation in Anorexia Nervosa
Seitz, J., Trinh, S., Kogel, V., & Beyer, C. (2021) · Advances in neurobiology · doi:10.1007/978-3-030-77375-5_12 · Cited by 14 · see citing works
Self-citationOestrogen Regulates Mitochondrial Respiratory Chain Enzyme Transcription in the Mouse Spinal Cord
Johann, S., Dahm, M., Kipp, M., Beyer, C., & Arnold, S. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02006.x · Cited by 12 · see citing works
Self-citationEffect of estrogens on base excision repair in brain and liver mitochondria of aged female rats
Leclère, R., Torregrosa-Muñumer, R., Kireev, R., García, C., Vara, E., Tresguerres, J. A. F., & Gredilla, R. (2013) · Biogerontology · doi:10.1007/s10522-013-9431-x · Cited by 11 · see citing works
“Keywords Mitochondria Estrogens DNA Base excision repair AP endonuclease Aging”
BackgroundMethodHassanzadeh, S., Sabetvand, M., Sardar, R., Aryanpour, R., & Namjoo, Z. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03710-3 · Cited by 11 · see citing works
“…the mitochondrial networks are highly orchestrated in some cells, it is not unexpected that the morphology of mitochondria can significantly affect their function due to their functional characteristics in the respiratory chain and regulation of nuclear and mitochondrial gene expression [10, 11].”
Moradi, F., Fiocchetti, M., Marino, M., Moffatt, C., & Stuart, J. A. (2021) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00080.2021 · Cited by 11 · see citing works
Sex-Specific Properties of Astrocytes: From Development to Evolutionary Insights
Bortolanza, M., Gobbo, D., Fang, L., Scheller, A., Bai, X., & Kirchhoff, F. (2025) · Neurochemical Research · doi:10.1007/s11064-025-04512-w · Cited by 10 · see citing works
“These species-dependent features highlight the impor - tance of primate models for translational aging research.”
Wyse, Â. T. D. S., Siebert, C., Bobermin, L. D., dos Santos, T. M., & Quincozes‐Santos, A. (2019) · Neurotoxicity Research · doi:10.1007/s12640-019-00128-5 · Cited by 9 · see citing works
de Assis, D. R., Szabó, A., Osete, J. R., Puppo, F., O’Connell, K. S., Akkouh, I. A., Hughes, T., Frei, E., Andreassen, O. A., & Djurovic, S. (2021) · Cells · doi:10.3390/cells10020209 · Cited by 10 · see citing works
Mechanisms Underlying Treatment‐Resistant Depression: Exploring Sex‐Based Biological Differences
da Silva, F. E. R., Yücel, A., Menezes, A. P. M., Ruiz, A. C., Tamez, M. C. C., Barichello, T., Scaini, G., & Quevedo, J. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70215 · Cited by 11 · see citing works
“…estrogen receptor beta (ERβ) mediates critical protective effects, influencing mitochondrial dynamics and biogenesis through PGC-1α, NRF1 signaling, and proteins involved in mitochondrial fusion/fission, such as Drp1 and MFN2 (Arnold et al. 2008; Kalkhoran and Kararigas 2022; Yang et al. 2009).”
Estrogen and Mitochondrial Function in Disease
Mooga, V. P., White, C. R., & Giordano‐Mooga, S. (2018) · InTech eBooks · doi:10.5772/intechopen.73015 · Cited by 8 · see citing works
“In the myocardium of ischemia reperfusion injury rodents, OVX rodents display an increase in mitochondrial fusion after injury, which is reversed by estrogen treatment [41] Work in isolated cortical astrocytes from male and female postnatal day 1 mice shows that estrogen regulates fission and fusion genes in a gender-…”
BackgroundEpiAlign: an alignment-based bioinformatic tool for comparing chromatin state sequences
Ge, X., Zhang, H., Xie, L., Li, W. V., Kwon, S. B., & Li, J. J. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz287 · Cited by 7 · see citing works
“For example, MFF that controls mitochondrial fission has been reported to have to have sex-specific regulation [29].”
BackgroundZhou, G., Zhao, Q., Luo, C., Liu, H., Li, P., Cui, Y., Yu, X., Chen, J., Liu, L., Zhang, S., et al. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.147330 · Cited by 7 · see citing works
Preveza, N. J., Setenet, G., Gwin, P., Bae, Y., Patrick, M. B., Cummings, A., Abraham, J. R., Ray, W. K., Helm, R. F., & Jarome, T. J. (2024) · Hippocampus · doi:10.1002/hipo.23650 · Cited by 4 · see citing works
“…however, previous studies have shown that injections of estrogen and progesterone effect the transcription of mitochondrial fusion and fission genes differently in the astrocytes across the entire brain of female and male mice (Arnold, de Araujo, and Beyer 2008; Demarest and McCarthy 2015).”
Lyon, A., Agius, T., MacArthur, M. R., Kiesworo, K., Stavart, L., Allagnat, F., Mitchell, S. J., Riella, L. V., Uygun, K., Yeh, H., et al. (2024) · iScience · doi:10.1016/j.isci.2024.111256 · Cited by 2 · see citing works
Sima, Y., Shi, S., Min, Z., Chen, Y., Lu, Y., Sha, H., & Liu, S. (2025) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-025-03431-7 · Cited by 1 · see citing works
Robb, E. L. (2013) · Brock University Digital Repository (Brock University) · Cited by 1 · see citing works
EpiAlign: an alignment-based bioinformatic tool for comparing chromatin state sequencesPreprint
Ge, X., Zhang, H., Xie, L., Li, W. V., Kwon, S. B., & Li, J. J. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/566299 · Cited by 1 · see citing works
Misiak, M., & Arnold, S. (2010) · RWTH Publications (RWTH Aachen)
Self-citationMiRNA as Biomarkers of Mitochondrial Toxicity
Vleet, T. R. V., & Mahalingaiah, P. K. S. (2018) · Wiley eBooks · doi:10.1002/9781119329725.ch22
- Authors
- Arnold, S., de Araújo, G. W., & Beyer, C.
- Affiliations
- RWTH Aachen University (DE)
- Venue
- Journal of Molecular Endocrinology
- Publisher
- Bioscientifica
- Published
- 2008-08-27
- Volume
- 41
- Issue
- 5
- Pages
- 289-300
- ISSN
- 0952-5041 (ISSN-L)
- 1479-6813
- OpenAlex
- W2100458662
- Cited by
- 65
- References
- 89
- Citations by year
- 2025: 4 · 2024: 4 · 2023: 1 · 2022: 2 · 2021: 7 · 2020: 1 · 2019: 7 · 2018: 4 · 2017: 4 · 2016: 1 · 2015: 4 · 2014: 6 · 2013: 4 · 2012: 5
- FWCI
- 1.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Molecular Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- RWTH Aachen University
- Medizinische Fakultät, RWTH Aachen University
- 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 › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- cortical astrocytes, mitochondrial fusion, mitochondrial fission, estrogen, progesterone, sex steroids, sex differences, gene transcription, apoptosis, cell proliferation, astrocyte viability, mitochondrial function, brain energy metabolism
- MeSH terms
- Animals, Astrocytes, Cell Survival, Cerebral Cortex, Estrogens, Female, Male, Mice, Inbred BALB C, Mitochondria, Progesterone, Sex Factors, Transcription, Genetic, Mice
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