Progesterone and Estrogen Regulate Oxidative Metabolism in Brain Mitochondria
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The ovarian hormones progesterone and estrogen have well-established neurotrophic and neuroprotective effects supporting both reproductive function and cognitive health. More recently, it has been recognized that these steroids also regulate metabolic functions sustaining the energetic demands of this neuronal activation. Underlying this metabolic control is an interpretation of signals from diverse environmental sources integrated by receptor-mediated responses converging upon mitochondrial function. In this study, to determine the effects of progesterone (P4) and 17β-estradiol (E2) on metabolic control via mitochondrial function, ovariectomized rats were treated with P4, E2, or E2 plus P4, and whole-brain mitochondria were isolated for functional assessment. Brain mitochondria from hormone-treated rats displayed enhanced functional efficiency and increased metabolic rates. The hormone-treated mitochondria exhibited increased respiratory function coupled to increased expression and activity of the electron transport chain complex IV (cytochrome c oxidase). This increased respiratory activity was coupled with a decreased rate of reactive oxygen leak and reduced lipid peroxidation representing a systematic enhancement of brain mitochondrial efficiency. As such, ovarian hormone replacement induces mitochondrial alterations in the central nervous system supporting efficient and balanced bioenergetics reducing oxidative stress and attenuating endogenous oxidative damage.
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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 [141]
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Mitochondria and neuronal survival
Nicholls, D. G., & Budd, S. L. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.1.315 · Cited by 1,243 · see citing works
Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency
López-Lluch, G., Hunt, N., Jones, B., Zhu, M., Jamieson, H., Hilmer, S., Cascajo, M. V., Allard, J., Ingram, D. K., Navas, P., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510452103 · Cited by 699 · see citing works
Borrás, C., Sastre, J., García-Sala, D., Lloret, A., Pallardó, F. V., & Viña, J. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)01356-4 · Cited by 654 · see citing works
Barja, G. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.07.005 · Cited by 653 · see citing works
17-β Estradiol Protects Neurons from Oxidative Stress-Induced Cell Death in Vitro
Behl, C., Widmann, M., Trapp, T., & Holsboer, F. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2647 · Cited by 608 · see citing works
HAN, D., WILLIAMS, E., & CADENAS, E. (2001) · Biochemical Journal · doi:10.1042/bj3530411 · Cited by 593 · see citing works
Self-citationHan, D., WILLIAMS, E., & Cadenas, E. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3530411 · Cited by 516 · see citing works
Self-citationMitochondrial free radical production and cell signaling
Cadenas, E. (2004) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2004.02.005 · Cited by 430 · see citing works
Self-citationEstrogen, Menopause, and the Aging Brain: How Basic Neuroscience Can Inform Hormone Therapy in Women
Morrison, J. H., Brinton, R. D., Schmidt, P. J., & Gore, A. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3369-06.2006 · Cited by 388 · see citing works
Self-citationNilsen, J., & Brinton, R. D. (2002) · Endocrinology · doi:10.1210/endo.143.1.8582 · Cited by 331 · see citing works
Self-citationEstrogen Increases Mitochondrial Efficiency and Reduces Oxidative Stress in Cerebral Blood Vessels
Stirone, C., Duckles, S. P., Krause, D. N., & Procaccio, V. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.014662 · Cited by 315 · see citing works
Calabrese, V., Scapagnini, G., Giuffrida Stella, A. M., Bates, T. E., & Clark, J. B. (2001) · Neurochemical Research · doi:10.1023/a:1010955807739 · Cited by 263 · see citing works
Nilsen, J., & Brinton, R. D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0438041100 · Cited by 262 · see citing works
Self-citationRodrı́guez-Cuenca, S., Pujol, E., Justo, R., Frontera, M., Oliver, J., Gianotti, M., & Roca, P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207229200 · Cited by 206 · see citing works
Effect of estrogen on global myocardial ischemia-reperfusion injury in female rats
Zhai, P., Eurell, T. E., Cotthaus, R. P., Jeffery, E. H., Bahr, J. M., & Gross, D. R. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.279.6.h2766 · Cited by 180 · see citing works
Nilsen, J., Chen, S., Irwin, R. W., Iwamoto, S. J., & Brinton, R. D. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-74 · Cited by 175 · see citing works
Self-citationMitochondria as Therapeutic Targets of Estrogen Action in the Central Nervous System
Nilsen, J., & Brinton, R. D. (2004) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1568007043337193 · Cited by 166 · see citing works
Self-citationSanz, A., Caro, P., Ibañez, J., Gómez, J., Gredilla, R., & Barja, G. (2005) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-005-4131-0 · Cited by 165 · see citing works
Reddy, P. H. (2006) · BioMed Research International · doi:10.1155/jbb/2006/31372 · Cited by 153 · see citing works
Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis
Justo, R., Boada, J., Frontera, M., Oliver, J., Bermúdez, J., & Gianotti, M. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00035.2005 · Cited by 133 · see citing works
Energy Requirement for Caspase Activation and Neuronal Cell Death
Nicotera, P., Leist, M., Fava, E., Berliocchi, L., & Volbracht, C. (2000) · Brain Pathology · doi:10.1111/j.1750-3639.2000.tb00261.x · Cited by 132 · see citing works
Impact of progestins on estradiol potentiation of the glutamate calcium response
Nilsen, J., & Brinton, R. D. (2002) · Neuroreport · doi:10.1097/00001756-200205070-00018 · Cited by 111 · see citing works
Self-citationZheng, J., & Ramirez, V. D. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00012-6 · Cited by 110 · see citing works
The women's health initiative estrogen replacement therapy is neurotrophic and neuroprotective
Brinton, R. D. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00109-3 · Cited by 109 · see citing works
Self-citationZheng, J., & Ramirez, V. D. (1999) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00161-7 · Cited by 108 · see citing works
Gridley, K. E., Green, P. S., & Simpkins, J. W. (1998) · Molecular Pharmacology · doi:10.1124/mol.54.5.874 · Cited by 100 · see citing works
Estrogen Induction of Cytochrome c Oxidase Subunit III in Rat Hippocampus
Bettini, E., & Maggi, A. C. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb10070.x · Cited by 83 · see citing works
Itallie, C. M. V., & Dannies, P. S. (1988) · Molecular Endocrinology · doi:10.1210/mend-2-4-332 · Cited by 78 · see citing works
Protection of cultured spinal motor neurons by estradiol
Nakamizo, T., Urushitani, M., Inoue, R., Shinohara, A., Sawada, H., Honda, K., Kihara, T., Akaike, A., & Shimohama, S. (2000) · Neuroreport · doi:10.1097/00001756-200011090-00019 · Cited by 73 · see citing works
Oxygen Tolerance and Coupling of Mitochondrial Electron Transport
Campian, J. L., Qian, M., Gao, X., & Eaton, J. W. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406685200 · Cited by 69 · see citing works
Structure of cytochrome c oxidase: a comparison of the bacterial and mitochondrial enzymes
Abramson, J., Svensson-Ek, M., Byrne, B., & Iwata, S. (2001) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/s0167-4838(00)00241-7 · Cited by 55 · see citing works
Gestation confers temporary resistance to peroxidation in the maternal rat brain
Subramanian, M., Pusphendran, C. K., Tarachand, U., & Devasagayam, T. P. A. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90695-h · Cited by 37 · see citing works
Sato, T., Teramoto, T., Tanaka, K., Ohnishi, Y., Irifune, M., & Nishikawa, T. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00010-x · Cited by 35 · see citing works
Acute effects of 17beta-estradiol on oxidative stress in ischemic rat striatum.
Kii, N., Adachi, N., Liu, K., & Arai, T. (2005) · PubMed · Cited by 26 · see citing works
Jung, M. E., Agarwal, R., & Simpkins, J. W. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.01.065 · Cited by 22 · see citing works
Dose-dependent inhibition of mitochondrial ATP synthase by 17β-estradiol
Massart, F., Paolini, S., Piscitelli, E., Brandi, M. L., & Solaini, G. (2002) · Gynecological Endocrinology · doi:10.1080/gye.16.5.373.377 · Cited by 20 · see citing works
Dose-dependent inhibition of mitochondrial ATP synthase by 17 beta-estradiol.
Massart, F., Paolini, S., Piscitelli, E., Brandi, M. L., & Solaini, G. (2002) · PubMed · Cited by 19 · see citing works
Velier, J. J., Ellison, J. A., Fisher, R. S., & Vinters, H. V. (1997) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19971115)50:4 · Cited by 15 · see citing works
Shea, T. B., & Ortiz, D. (2003) · Journal of Alzheimer s Disease · doi:10.3233/jad-2003-5408 · Cited by 12 · see citing works
Changes in cytochrome oxidase activity in brown adipose tissue during oestrous cycle in the rat
Puerta, M., Rocha, M., González-Covaleda, S., McBennett, S., & Andrews, J. F. (1998) · European Journal of Endocrinology · doi:10.1530/eje.0.1390433 · Cited by 12 · see citing works
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- Keller JN, Germeyer A, Begley JG, Mattson MP 1997 17β-Estradiol attenuates oxidative impairment of synaptic Na+/K+-ATPase activity, glucose transport, and glutamate transport induced by amyloid β-peptide and iron. J Neurosci Res 50:522–530 [DOI] [PubMed] [Google Scholar]
Cited by
Sorted by citations
Yao, J., Irwin, R. W., Zhao, L., Nilsen, J., Hamilton, R. T., & Brinton, R. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903563106 · Cited by 940 · see citing works
Self-citationProgesterone receptors: form and function in brain
Brinton, R. D., Thompson, R. F., Foy, M. R., Baudry, M., Wang, J., Finch, C. E., Morgan, T. E., Pike, C. J., Mack, W. J., Stanczyk, F. Z., et al. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.02.001 · Cited by 675 · see citing works
Self-citationEstrogen: A master regulator of bioenergetic systems in the brain and body
Rettberg, J. R., Yao, J., & Brinton, R. D. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.08.001 · Cited by 534 · see citing works
Self-citationSex Differences in Traumatic Brain Injury: What We Know and What We Should Know
Gupte, R. P., Brooks, W. M., Vukas, R. R., Pierce, J. D., & Harris, J. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6171 · Cited by 533 · see citing works
Protective actions of sex steroid hormones in Alzheimer’s disease
Pike, C. J., Carroll, J. C., Rosario, E. R., & Barron, A. M. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.04.015 · Cited by 524 · see citing works
Estrogenic control of mitochondrial function and biogenesis
Klinge, C. M. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21936 · Cited by 320 · see citing works
Chen, J., Cammarata, P. R., Baines, C. P., & Yager, J. D. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2009.06.001 · Cited by 266 · see citing works
The metabolic face of migraine — from pathophysiology to treatment
Gross, E. C., Martinez, M. L., Fischer, D., Sándor, P. S., & Schoenen, J. E. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0255-4 · Cited by 263 · see citing works
Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration
Spence, R. D., & Voskuhl, R. R. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.12.001 · Cited by 259 · see citing works
Steroid Hormones and Their Action in Women's Brains: The Importance of Hormonal Balance
Río, J. P. D., Alliende, M. I., Molina, N., Serrano, F. G., Molina, S., & Pilar Vigil, P. (2018) · Frontiers in Public Health · doi:10.3389/fpubh.2018.00141 · Cited by 220 · see citing works
Hunter, R. G., Seligsohn, M., Rubin, T. G., Griffiths, B. B., Ozdemir, Y., Pfaff, D. W., Datson, N. A., & McEwen, B. S. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602185113 · Cited by 174 · see citing works
Torres, M. J., Kew, K. A., Ryan, T. E., Pennington, E. R., Lin, C.-T., Buddo, K. A., Fix, A. M., Smith, C. A., Gilliam, L. A., Karvinen, S., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2017.10.003 · Cited by 170 · see citing works
Yao, J., Chen, S., Mao, Z., Cadenas, E., & Brinton, R. D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021788 · Cited by 169 · see citing works
“Mitochondrial Preparation Crude brain mitochondria were isolated from the designated hemisphere following our previously established protocol [59] with minor adaptation.”
MethodSelf-citationSong, Y., Li, S.-R., Li, X., Chen, X., Wei, Z., Liu, Q., & Cheng, Y. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00157 · Cited by 171 · see citing works
Klosinski, L. P., Yao, J., Yin, F., Fonteh, A. N., Harrington, M. G., Christensen, T. A., Trushina, E. V., & Brinton, R. D. (2015) · EBioMedicine · doi:10.1016/j.ebiom.2015.11.002 · Cited by 160 · see citing works
Self-citationProgesterone neuroprotection in traumatic CNS injury and motoneuron degeneration
Nicola, A. F. D., Labombarda, F., Deniselle, M. C. G., González, S. L., Garay, L. I., Meyer, M., Gargiulo, G., Guennoun, R., & Schumacher, M. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.001 · Cited by 161 · see citing works
Cognition, Mood and Sleep in Menopausal Transition: The Role of Menopause Hormone Therapy
Gava, G., Orsili, I., Alvisi, S., Mancini, I., Seracchioli, R., & Meriggiola, M. C. (2019) · Medicina · doi:10.3390/medicina55100668 · Cited by 168 · see citing works
Estrogen actions on mitochondria—Physiological and pathological implications
Simpkins, J. W., Yang, S., Sarkar, S. N., & Pearce, V. P. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.04.013 · Cited by 158 · see citing works
Gaignard, P., Savouroux, S., Liere, P., Pianos, A., Thérond, P., Schumacher, M., Slama, A., & Guennoun, R. (2015) · Endocrinology · doi:10.1210/en.2014-1913 · Cited by 150 · see citing works
Yao, J., Hamilton, R. T., Cadenas, E., & Brinton, R. D. (2010) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2010.06.002 · Cited by 152 · see citing works
Self-citationPrognostic factors in paediatric anaplastic large cell lymphoma role of ALK
Woessmann, W. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/434 · Cited by 166 · see citing works
Roles of sigma-1 receptors on mitochondrial functions relevant to neurodegenerative diseases
Weng, T.-Y., Tsai, S., & Su, T. (2017) · Journal of Biomedical Science · doi:10.1186/s12929-017-0380-6 · Cited by 139 · see citing works
Yin, F., Yao, J., Sancheti, H., Feng, T., Melcangi, R. C., Morgan, T. E., Finch, C. E., Pike, C. J., Mack, W. J., Cadenas, E., et al. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.03.013 · Cited by 137 · see citing works
Self-citationOvarian hormone loss induces bioenergetic deficits and mitochondrial β-amyloid
Yao, J., Irwin, R. W., Chen, S., Hamilton, R., Cadenas, E., & Brinton, R. D. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.03.001 · Cited by 133 · see citing works
Self-citationGaignard, 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
Contributions of sex to cerebrovascular function and pathology
Robison, L. S., Gannon, O. J., Salinero, A. E., & Zuloaga, K. L. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.030 · Cited by 124 · see citing works
Cognitive impairment after cancer treatment: mechanisms, clinical characterization, and management
Fleming, B., Edison, P., & Kenny, L. M. (2023) · BMJ · doi:10.1136/bmj-2022-071726 · Cited by 120 · see citing works
Grimm, A., Schmitt, K., Lang, U. E., Mensah‐Nyagan, A. G., & Eckert, A. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.09.013 · Cited by 113 · 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
Reyngoudt, H., Paemeleire, K., Descamps, B., Deene, Y. D., & Achten, E. (2011) · Cephalalgia · doi:10.1177/0333102410394675 · Cited by 110 · see citing works
Liu, L., Wang, J., Zhao, L., Nilsen, J., McClure, K., Wong, K., & Brinton, R. D. (2009) · Endocrinology · doi:10.1210/en.2008-1447 · Cited by 108 · see citing works
Self-citationAlzheimer, mitochondria and gender
Grimm, A., Mensah‐Nyagan, A. G., & Eckert, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.04.012 · Cited by 107 · see citing works
Estrogen down-regulates uncoupling proteins and increases oxidative stress in breast cancer
Sastre‐Serra, J., Valle, A., Garau, I., Oliver, J., & Roca, P. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.11.025 · Cited by 104 · see citing works
Grimm, A., Biliouris, E. E., Lang, U. E., Götz, J., Mensah‐Nyagan, A. G., & Eckert, A. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1988-x · Cited by 104 · see citing works
Nutrition in Menopausal Women: A Narrative Review
Silva, T. R., Oppermann, K., dos Reis, F. M., & Spritzer, P. M. (2021) · Nutrients · doi:10.3390/nu13072149 · Cited by 97 · see citing works
Mitochondrial and sex steroid hormone crosstalk during aging
Velarde, M. C. (2014) · Longevity & Healthspan · doi:10.1186/2046-2395-3-2 · Cited by 96 · see citing works
Duclot, F., & Kabbaj, M. (2015) · Genome biology · doi:10.1186/s13059-015-0815-x · Cited by 95 · 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
Estrogen Regulation of Mitochondrial Bioenergetics
Yao, J., & Brinton, R. D. (2012) · Advances in pharmacology · doi:10.1016/b978-0-12-394816-8.00010-6 · Cited by 97 · see citing works
Self-citationMa, C., Wu, X., Shen, X., Yang, Y., Chen, Z., Sun, X., & Wang, Z. (2019) · Chinese Neurosurgical Journal · doi:10.1186/s41016-019-0173-8 · Cited by 93 · see citing works
Selective Oestrogen Receptor Modulators Differentially Potentiate Brain Mitochondrial Function
Irwin, R. W., Yao, J., To, J., Hamilton, R. T., Cadenas, E., & Brinton, R. D. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02251.x · Cited by 92 · see citing works
Self-citationRole of hormones in sarcopenia
Priego, T., Martı́n, A. I., González‐Hedström, D., Granado, M., & López‐Calderón, A. (2021) · Vitamins and hormones · doi:10.1016/bs.vh.2020.12.021 · Cited by 97 · see citing works
Liu, L., Zhao, L., She, H., Chen, S., Wang, J. M., Wong, C., McClure, K., Sitruk-Ware, R. L., & Brinton, R. D. (2010) · Endocrinology · doi:10.1210/en.2010-0005 · Cited by 90 · see citing works
Self-citationGuo, J., Krause, D. N., Horne, J. N., Weiss, J. H., Li, X.-J., & DUCKLES, S. P. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.226 · Cited by 89 · see citing works
Seal, S., Puigvert, J. C., Trapotsi, M., Yang, H., Spjuth, O., & Bender, A. (2022) · Communications Biology · doi:10.1038/s42003-022-03763-5 · Cited by 83 · see citing works
Progesterone and progestins: neuroprotection and myelin repair
Schumacher, M., Sitruk-Ware, R. L., & Nicola, A. F. D. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.10.002 · Cited by 89 · see citing works
Significant role of estrogen in maintaining cardiac mitochondrial functions
Rattanasopa, C., Phungphong, S., Wattanapermpool, J., & Bupha‐Intr, T. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.11.009 · Cited by 88 · see citing works
The importance of estradiol for body weight regulation in women
Pilar Vigil, P., Meléndez, J., Petkovic, G., & Río, J. P. D. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.951186 · Cited by 82 · 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
Baassiri, M. G. E., Raouf, Z., Badin, S., Escobosa, A., Sodhi, C., & Nasr, I. W. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03118-3 · Cited by 74 · see citing works
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Arnold, S. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3573-0_13 · Cited by 74 · see citing works
Kim, J., Kim, T.-Y., Cho, K.-S., Kim, H., & Koh, J. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.07.011 · Cited by 74 · see citing works
Strom, J. O., Theodorsson, A., & Theodorsson, E. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12031533 · Cited by 76 · see citing works
Frey, B. N., & Dias, R. D. S. (2013) · Bipolar Disorders · doi:10.1111/bdi.12151 · Cited by 76 · see citing works
Cameron, R. B., Beeson, C. C., & Schnellmann, R. G. (2016) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b00669 · Cited by 74 · see citing works
Kasote, D. M., Hegde, M. V., & Katyare, S. S. (2013) · BioFactors · doi:10.1002/biof.1093 · Cited by 71 · see citing works
Potential biological contributers to the sex difference in multiple sclerosis progression
Álvarez‐Sánchez, N., & Dunn, S. E. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1175874 · Cited by 71 · see citing works
López-Grueso, R., Gambini, J., Abdelaziz, K. M., Monleón, D., Díaz, A., Alami, M. E., Bonet-Costa, V., Borrás, C., & Viña, J. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.5112 · Cited by 69 · see citing works
Effects 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
Medroxyprogesterone Acetate Antagonizes Estrogen Up-Regulation of Brain Mitochondrial Function
Irwin, R. W., Yao, J., Ahmed, S. S., Hamilton, R. T., Cadenas, E., & Brinton, R. D. (2010) · Endocrinology · doi:10.1210/en.2010-1061 · Cited by 66 · see citing works
Self-citationDu, J., Ma, M., Zhao, Q., Fang, L., Chang, J., Wang, Y., Fei, R., & Song, X. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.062 · Cited by 66 · see citing works
Role of Uncoupling Proteins in Cancer
Valle, A., Oliver, J., & Roca, P. (2010) · Cancers · doi:10.3390/cancers2020567 · Cited by 67 · see citing works
Arnold, S., de Araújo, G. W., & Beyer, C. (2008) · Journal of Molecular Endocrinology · doi:10.1677/jme-08-0085 · Cited by 65 · see citing works
Systemic distribution of progesterone receptor subtypes in human tissues
Asavasupreechar, T., Saito, R., Miki, Y., Edwards, D. P., Boonyaratanakornkit, V., & Sasano, H. (2020) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2020.105599 · Cited by 65 · see citing works
Effects of hormone therapy on cognition and mood
Fischer, B. L., Gleason, C. E., & Asthana, S. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.02.025 · Cited by 64 · see citing works
Steroids and Alzheimer’s Disease: Changes Associated with Pathology and Therapeutic Potential
Akwa, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134812 · Cited by 63 · see citing works
Neuroprotective Effects of 17β-Estradiol Rely on Estrogen Receptor Membrane Initiated Signals
Fiocchetti, M., Ascenzi, P., & Marino, M. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00073 · Cited by 65 · see citing works
Is Progesterone a Candidate Neuroprotective Factor for Treatment following Ischemic Stroke?
Gibson, C. L., Coomber, B., & Rathbone, J. (2009) · The Neuroscientist · doi:10.1177/1073858409333069 · Cited by 63 · see citing works
Alzheimer's Disease, Oestrogen and Mitochondria: an Ambiguous Relationship
Grimm, A., Lim, Y.-A., Mensah‐Nyagan, A. G., Götz, J., & Eckert, A. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8281-x · Cited by 64 · see citing works
Acupuncture reversed hippocampal mitochondrial dysfunction in vascular dementia rats
Li, H., Liu, Y., Lin, L.-T., Wang, X., Du, S., Yan, C.-Q., He, T., Yang, J., & Liu, C. (2015) · Neurochemistry International · doi:10.1016/j.neuint.2015.12.001 · Cited by 61 · see citing works
Zhu, J., Zhou, Y., Jin, B., & Shu, J. (2023) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/20420188231199359 · Cited by 70 · see citing works
Huang, Y., & Zhang, Q. (2010) · British Journal Of Nutrition · doi:10.1017/s0007114510002291 · Cited by 61 · see citing works
Progestogens and brain: An update
Pluchino, N., Cubeddu, A., Giannini, A., Merlini, S., Cela, V., Angioni, S. L., & Genazzani, A. R. (2009) · Maturitas · doi:10.1016/j.maturitas.2008.11.023 · Cited by 61 · see citing works
Yao, J., Zhao, L.-Q., Mao, Z.-S., Chen, S.-H., Wong, K., To, J., & Brinton, R. (2013) · Brain Research · doi:10.1016/j.brainres.2013.02.021 · Cited by 61 · see citing works
Self-citationRepurposing sex steroids and related drugs as potential treatment for Parkinson's disease
Bourque, M., Morissette, M., & Paolo, T. D. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.04.005 · Cited by 61 · see citing works
Zhao, L., Morgan, T. E., Mao, Z., Lin, S., Cadenas, E., Finch, C. E., Pike, C. J., Mack, W. J., & Brinton, R. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031267 · Cited by 58 · see citing works
Self-citationThe other side of progestins: effects in the brain.
Giatti, S., Melcangi, R., & Pesaresi, M. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0061 · Cited by 53 · 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
Actions of 17β-estradiol and testosterone in the mitochondria and their implications in aging
Vasconsuelo, A., Milanesi, L., & Boland, R. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.09.001 · Cited by 55 · see citing works
Misiak, 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
Lazarus, R. C., Buonora, J. E., Jacobowitz, D. M., & Mueller, G. P. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.10.507 · Cited by 53 · see citing works
Zakaria, A., Hamdi, N., & Abdel-Kader, R. M. (2016) · Molecular Neurobiology · doi:10.1007/s12035-014-9088-8 · Cited by 53 · see citing works
Yu, H., Fei, J., Chen, X.-S., Cai, Q., Liu, H., Liu, G., & Yao, Z. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.03.079 · Cited by 53 · see citing works
Borrás, C., Ferrando, M., Inglés, M., Gambini, J., López-Grueso, R., Edo, R., Mas‐Bargues, C., Pellicer, A., & Viña, J. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8101615 · Cited by 52 · see citing works
Nadal‐Serrano, M., Sastre‐Serra, J., Pons, D. G., Miró, A. M., Oliver, J., & Roca, P. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24192 · Cited by 52 · see citing works
The Interaction Between NF-κB and Estrogen in Alzheimer’s Disease
Mishra, P., Davies, D. A., & Albensi, B. C. (2023) · Molecular Neurobiology · doi:10.1007/s12035-022-03152-3 · Cited by 51 · see citing works
Progestogen-Mediated Neuroprotection in Central Nervous System Disorders
Bassani, T. B., Bartolomeo, C. S., Oliveira, R. B., & Ureshino, R. P. (2022) · Neuroendocrinology · doi:10.1159/000525677 · Cited by 50 · see citing works
Progesterone Prevents Nerve Injury-Induced Allodynia and Spinal NMDA Receptor Upregulation in Rats
Coronel, M. F., Labombarda, F., Roig, P., Villar, M. J., Nicola, A. F. D., & González, S. L. (2011) · Pain Medicine · doi:10.1111/j.1526-4637.2011.01178.x · Cited by 49 · see citing works
Sex-Specific Differences in Redox Homeostasis in Brain Norm and Disease
Ruszkiewicz, J. A., Miranda‐Vizuete, A., Tinkov, A. A., Геннадиевна, С. М., Skalny, A. V., Tsatsakis, A. M., & Aschner, M. (2019) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1241-9 · Cited by 47 · see citing works
Dilek, M., Nazıroğlu, M., Oral, H. B., Övey, İ. S., Küçükayaz, M., Mungan, M. T., Kara, H. Y., & Sütçü, R. (2010) · The Journal of Membrane Biology · doi:10.1007/s00232-010-9233-x · Cited by 47 · see citing works
Sandhir, R., Sethi, N., Aggarwal, A., & Khera, A. (2014) · Neurochemistry International · doi:10.1016/j.neuint.2014.04.011 · Cited by 46 · see citing works
Ishihara, Y., Takemoto, T., Ishida, A., & Yamazaki, T. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/343706 · Cited by 45 · see citing works
Nadal-Casellas, A., Proenza, A. M., Lladó, I., & Gianotti, M. (2011) · Steroids · doi:10.1016/j.steroids.2011.04.009 · Cited by 45 · see citing works
Sárvári, M., Kalló, I., Hrabovszky, E., Solymosi, N., Rodolosse, A., & Liposits, Z. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00149 · Cited by 44 · see citing works
Yao, J., Chen, S., Cadenas, E., & Brinton, R. D. (2010) · Brain Research · doi:10.1016/j.brainres.2010.11.090 · Cited by 43 · see citing works
Self-citationDuffy, Á., Schaner, M. J., Wu, S. H., Staniszewski, A., Kumar, A. R., Arévalo, J. C., Arancio, O., Chao, M. V., & Scharfman, H. E. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.03.008 · Cited by 43 · see citing works
Estrogen Protects against Oxidative Multiorgan Damage in Rats with Chronic Renal Failure
Kasımay, Ö., Şener, G., Çakır, B., Yüksel, M., Çetinel, Ş., Contuk, G., & Yeğen, B. (2009) · Renal Failure · doi:10.3109/08860220903134563 · Cited by 41 · see citing works
TSPO PIGA Ligands Promote Neurosteroidogenesis and Human Astrocyte Well-Being
Pozzo, E. D., Giacomelli, C., Costa, B., Cavallini, C., Taliani, S., Barresi, E., Settimo, F. D., & Martini, C. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17071028 · Cited by 44 · see citing works
Neuroprotective Effect of Progesterone in MPTP-Treated Male Mice
Bourque, M., Morissette, M., Al-Sweidi, S., Caruso, D., Melcangi, R. C., & Paolo, T. D. (2015) · Neuroendocrinology · doi:10.1159/000438789 · Cited by 42 · see citing works
Kipp, M., Berger, K., Clarner, T., Dang, J., & Beyer, C. (2012) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.2011.02163.x · Cited by 41 · see citing works
- Authors
- Irwin, R. W., Yao, J., Hamilton, R. T., Cadenas, E., Brinton, R. D., & Nilsen, J.
- Affiliations
- University of Southern California (US)
- Department of Pharmacology and Pharmaceutical Sciences (R.W.I., J.Y., R.T.H., E.C., R.D.B., J.N.), University of Southern California, Pharmaceutical Sciences Center, University of Southern California, Los Angeles, California, 90033
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2008-02-21
- Volume
- 149
- Issue
- 6
- Pages
- 3167-3175
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC2408802
- OpenAlex
- W2069825814
- Cited by
- 289
- References
- 39
- Citations by year
- 2026: 14 · 2025: 8 · 2024: 17 · 2023: 27 · 2022: 10 · 2021: 17 · 2020: 12 · 2019: 15 · 2018: 19 · 2017: 14 · 2016: 15 · 2015: 18 · 2014: 13 · 2013: 14 · 2012: 21
- FWCI
- 7.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Endocrinology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (T32AG000093, T32-AG000093-24/25, P01AG026572)
- National Institute of Mental Health (R01MH067159, 1R01 MH67159-01)
- 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
- progesterone, estradiol, ovarian hormones, brain mitochondria, mitochondrial respiration, cytochrome c oxidase, electron transport chain, reactive oxygen species, lipid peroxidation, oxidative stress, brain energy metabolism, hormone replacement therapy, ovariectomy
- MeSH terms
- Animals, Brain, Electron Transport Complex IV, Estradiol, Female, Free Radicals, Hydrogen Peroxide, Mitochondria, Ovariectomy, Oxygen Consumption, Progesterone, Lipid Peroxidation, Rats, Sprague-Dawley, Reverse Transcriptase Polymerase Chain Reaction, Rats
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