Progesterone receptors: form and function in brain

Brinton, Roberta Diaz; Thompson, Richard F.; Foy, Michael R.; Baudry, Michel; Wang, JunMing; Finch, Caleb E.; Morgan, Todd E.; Pike, Christian J.; Mack, Wendy J.; Stanczyk, Frank Z.; Nilsen, Jon

doi:10.1016/j.yfrne.2008.02.001

Cited by 675Estrogen and related hormone effectsNeuroscience and Neuropharmacology ResearchNuclear Receptors and Signaling

Progesterone receptors: form and function in brain

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Brinton, Roberta Diaz, Thompson, Richard F., Foy, Michael R., Baudry, Michel, Wang, JunMing, Finch, Caleb E., Morgan, Todd E., Pike, Christian J. +3 more·2008·Frontiers in Neuroendocrinology

DOI 10.1016/j.yfrne.2008.02.001PMC PMC2398769

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Abstract

Emerging data indicate that progesterone has multiple non-reproductive functions in the central nervous system to regulate cognition, mood, inflammation, mitochondrial function, neurogenesis and regeneration, myelination and recovery from traumatic brain injury. Progesterone-regulated neural responses are mediated by an array of progesterone receptors (PR) that include the classic nuclear PRA and PRB receptors and splice variants of each, the seven transmembrane domain 7TMPRbeta and the membrane-associated 25-Dx PR (PGRMC1). These PRs induce classic regulation of gene expression while also transducing signaling cascades that originate at the cell membrane and ultimately activate transcription factors. Remarkably, PRs are broadly expressed throughout the brain and can be detected in every neural cell type. The distribution of PRs beyond hypothalamic borders, suggests a much broader role of progesterone in regulating neural function. Despite the large body of evidence regarding progesterone regulation of reproductive behaviors and estrogen-inducible responses as well as effects of progesterone metabolite neurosteroids, much remains to be discovered regarding the functional outcomes resulting from activation of the complex array of PRs in brain by gonadally and/or glial derived progesterone. Moreover, the impact of clinically used progestogens and developing selective PR modulators for targeted outcomes in brain is a critical avenue of investigation as the non-reproductive functions of PRs have far-reaching implications for hormone therapy to maintain neurological health and function throughout menopausal aging.

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Canonical and non-canonical AR, ER, and PR are expressed on neuronal membranes and in glial cells.
“Canonical and non-canonical AR, ER, and PR, are expressed on neuronal membranes and in glial cells(Almey et al., 2014; Brinton et al., 2008; Foradori et al., 2008; Mermelstein and Micevych, 2008; Petersen et al., 2013).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Brinton et al., 2008

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Allopregnanolone, a progesterone metabolite, enhances behavioral recovery and decreases neuronal loss after traumatic brain injury
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Mitochondrial mechanisms of estrogen neuroprotection
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Self-citation
Dimerization of mammalian progesterone receptors occurs in the absence of DNA and is related to the release of the 90-kDa heat shock protein.
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Disruption of estrogen signaling does not prevent progesterone action in the estrogen receptor α knockout mouse uterus
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Sex differences in the regulation of progesterone receptor isoforms expression in the rat brain
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Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and src/mitogen activated protein kinase pathway
Nilsen, J., Chen, S., & Brinton, R. D. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02254-0 · Cited by 131 · see citing works
Self-citation
Free calcium changes associated with hormone action in amphibian oocytes
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17β-estradiol induces Ca2+ influx, dendritic and nuclear Ca2+ rise and subsequent cyclic AMP response element-binding protein activation in hippocampal neurons: A potential initiation mechanism for estrogen neurotrophism
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Self-citation
Progesterone Neuroprotection in the Wobbler Mouse, a Genetic Model of Spinal Cord Motor Neuron Disease
Deniselle, M. C. G. (2002) · Neurobiology of Disease · doi:10.1006/nbdi.2002.0564 · Cited by 128 · see citing works
17α-estradiol and 17β-estradiol treatments are effective in lowering cerebral amyloid-β levels in AβPPSWE transgenic mice
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Self-citation
Neurogenesis and brain injury: managing a renewable resource for repair
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Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25‐Dx expression in the rat spinal cord
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Specific Progesterone Binding to a Membrane Protein and Related Nongenomic Effects on Ca2+-Fluxes in Sperm
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Impairments in spatial learning and memory: ethanol, allopregnanolone, and the hippocampus
Silvers, J. M., Tokunaga, S., Berry, R. B., White, A. M., & Matthews, D. B. (2003) · Brain Research Reviews · doi:10.1016/j.brainresrev.2003.09.002 · Cited by 121 · see citing works

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Gender differences in Parkinson's disease: Clinical characteristics and cognition
Miller, I. N., & Cronin‐Golomb, A. (2010) · Movement Disorders · doi:10.1002/mds.23388 · Cited by 405 · see citing works
Ovarian hormones and obesity
Leeners, B., Geary, N., Tobler, P. N., & Asarian, L. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmw045 · Cited by 407 · see citing works
Stress, sex hormones, inflammation, and major depressive disorder: Extending Social Signal Transduction Theory of Depression to account for sex differences in mood disorders
Slavich, G. M., & Sacher, J. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05326-9 · Cited by 383 · see citing works
Menstrual cycle influence on cognitive function and emotion processingâ€”from a reproductive perspective
SundstrÃ¶m Poromaa, I., & Gingnell, M. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00380 · Cited by 291 · see citing works
“…estradiol receptors (ERα and ERβ) and the progesterone receptors (PRA and PRB) are highly expressed in brain areas associated with reproduction, cognitive function, and emotional processing such as the hypothalamus and the limbic system (for review, see Gruber et al., 2002; Brinton et al., 2008).”
Background
Minireview: translational animal models of human menopause: challenges and emerging opportunities
Diaz Brinton, R. (2012) · Endocrinology · doi:10.1210/en.2012-1340 · Cited by 272 · see citing works
Hormonal Treatments for Major Depressive Disorder: State of the Art
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Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
Effect of menstrual cycle phase on corticolimbic brain activation by visual food cues
Frank, T. C., Kim, G. L., Krzemien, A., & Van Vugt, D. A. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.071 · Cited by 122 · see citing works
Low levels of estradiol are associated with elevated conditioned responding during fear extinction and with intrusive memories in daily life
Wegerer, M., Kerschbaum, H., Blechert, J., & Wilhelm, F. H. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.10.001 · Cited by 122 · see citing works
Progesterone and Nestorone Facilitate Axon Remyelination: A Role for Progesterone Receptors
Hussain, R., El-Etr, M., Gaci, O., Rakotomamonjy, J., Macklin, W. B., Kumar, N., Sitruk-Ware, R., Schumacher, M., & Ghoumari, A. M. (2011) · Endocrinology · doi:10.1210/en.2011-1219 · Cited by 123 · see citing works
Non-genomic mechanisms of progesterone action in the brain
Singh, M., Su, C., & Ng, S. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00159 · Cited by 117 · see citing works
Identification of a narrow post-ovulatory window of vulnerability to distressing involuntary memories in healthy women
Soni, M., Curran, V. H., & Kamboj, S. K. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.04.003 · Cited by 102 · 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-citation
Neurosteroid withdrawal regulates GABA-A receptor α4-subunit expression and seizure susceptibility by activation of progesterone receptor-independent early growth response factor-3 pathway
Gangisetty, O., & Reddy, D. S. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.07.037 · Cited by 84 · see citing works
Sex Differences in White Matter Abnormalities after Mild Traumatic Brain Injury: Localization and Correlation with Outcome
Fakhran, S., Yaeger, K., Collins, M., & Alhilali, L. (2014) · Radiology · doi:10.1148/radiol.14132512 · Cited by 83 · see citing works
Sex/gender differences in cognitive abilities
Kheloui, S., Jacmin-Park, S., Larocque, O., Kerr, P., Rossi, M., Cartier, L., & Juster, R.-P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105333 · Cited by 78 · see citing works
Female specific risk factors for the development of Alzheimer’s disease neuropathology and cognitive impairment: Call for a precision medicine approach
Udeh-Momoh, C., & Watermeyer, T. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101459 · Cited by 67 · see citing works
Membrane progesterone receptor beta (mPRβ/Paqr8) promotes progesterone-dependent neurite outgrowth in PC12 neuronal cells via non-G protein-coupled receptor (GPCR) signaling
Kasubuchi, M., Watanabe, K., Hirano, K., Inoue, D., Li, X., Terasawa, K., Konishi, M., Itoh, N., & Kimura, I. (2017) · Scientific Reports · doi:10.1038/s41598-017-05423-9 · Cited by 59 · see citing works
Effect of menstrual cycle on thermal perception and autonomic thermoregulatory responses during mild cold exposure
Matsuda-Nakamura, M., Yasuhara, S., & Nagashima, K. (2015) · The Journal of Physiological Sciences · doi:10.1007/s12576-015-0371-x · Cited by 45 · see citing works
Neuroendocrine underpinning of social recognition in males and females
Aspesi, D., & Choleris, E. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13070 · Cited by 41 · see citing works
Autonomic nervous system dysfunction throughout menopausal transition: A potential mechanism underpinning cardiovascular and cognitive alterations during female ageing
Schwarz, K. G., Vicencio, S. C., Inestrosa, N. C., Villaseca, P., & Del Rio, R. (2024) · The Journal of Physiology · doi:10.1113/jp285126 · Cited by 40 · see citing works
Male/female differences in neuroprotection and neuromodulation of brain dopamine
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Early menopause and other gynecologic risk indicators for chronic fatigue syndrome in women
Boneva, R. S., Lin, J.-M. S., & Unger, E. R. (2015) · Menopause · doi:10.1097/gme.0000000000000411 · Cited by 37 · see citing works
Progesterone impairs social recognition in male rats
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“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript 2003;Brinton et al., 2008;Auger and De Vries, 2002).”
Background

Expression profiling of genes controlled by estradiol (E2) and/or nuclear estrogen receptors ER α and ER β
Lana, A. (2009)
Estrogen-induced downregulation of TASK-1 expression through estrogen receptor β in N2A cells
Qiu, X.-Y., & Li, X. (2021) · Molecular Biology Reports · doi:10.1007/s11033-021-06852-6 · Cited by 1 · see citing works
Effects of estrogen on estrogen receptors in myocardium of ovariectomized female rats
Li, Q. (2008) · Zhongguo linchuang yaolixue yu zhiliaoxue
Anticonvulsant Activity of Progesterone and Neurosteroids in Progesterone Receptor Knockout Mice
Reddy, D. S., Castaneda, D. C., O’Malley, B. W., & Rogawski, M. A. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.065268 · Cited by 181 · see citing works
Estrogen Up-regulates ATBF1 Transcription but Causes Its Protein Degradation in Estrogen Receptor-α-positive Breast Cancer Cells
Dong, X., Guo, P., Sun, X., Li, Q., & Dong, J. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.187849 · Cited by 29 · see citing works

Authors: 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., & Nilsen, J.
Affiliations: University of Southern California (US)
Loyola Marymount University (US)
ORCID: Baudry, Michel
Finch, Caleb E.
Morgan, Todd E.
Pike, Christian J.
Mack, Wendy J.
Stanczyk, Frank Z.
Nilsen, Jon
Venue: Frontiers in Neuroendocrinology
Publisher: Elsevier BV
Published: 2008-05
Volume: 29
Issue: 2
Pages: 313-339
ISSN: 0091-3022 (ISSN-L)
DOI: 10.1016/j.yfrne.2008.02.001
PMC: PMC2398769
OpenAlex: W2113179569
Cited by: 675
References: 324
Citations by year: 2026: 30 · 2025: 30 · 2024: 54 · 2023: 49 · 2022: 41 · 2021: 40 · 2020: 39 · 2019: 29 · 2018: 37 · 2017: 32 · 2016: 36 · 2015: 28 · 2014: 30 · 2013: 40 · 2012: 35
FWCI: 3.87
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Frontiers in Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (P01AG026572)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
Keywords: progesterone receptor, progesterone, brain, PGRMC1, neurosteroids, cognition, mood, neuroinflammation, mitochondrial function, neurogenesis, myelination, traumatic brain injury, progestogens, selective progesterone receptor modulators, menopause, hormone therapy
MeSH terms: Alzheimer Disease, Animals, Brain, Brain Chemistry, Female, Humans, Male, Meiosis, Memory, Mitosis, Neuroglia, Neuronal Plasticity, Receptors, Progesterone, Neuroprotective Agents, Protein Isoforms, Cell Proliferation

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Progesterone receptors: form and function in brain

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