Cited by 283Stress Responses and CortisolAdrenal Hormones and DisordersNeuropeptides and Animal Physiology

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The Neurosteroid Tetrahydroprogesterone Attenuates the Endocrine Response to Stress and Exerts Glucocorticoid-like Effects on Vasopressin Gene Transcription in the Rat Hypothalamus

Patchev, V·1996·Neuropsychopharmacology

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Abstract

The neurosteroid tetrahydroprogesterone (5 alpha-pregnan-3 alpha-ol-20-one, allopregnanolone, THP), has been previously shown to counteract the anxiogenic effects of corticotropin-releasing hormone (CRH) and to interfere with noradrenergic and corticosteroid-mediated regulation of CRH release and gene transcription. Those observations indicated that, besides its sedative and analgesic activity, THP may also affect the neuroendocrine response to stress in a mode resembling that of corticosteroids. To examine this possibility, we compared the ability of THP, its precursor progesterone (P4), and the glucocorticoids dexamethasone (DEX) and corticosterone (CORT) to influence the pituitary-adrenal response to acute emotional stress and the adrenalectomy-induced increase in the gene transcription of the stress-related peptide arginine vasopressin (AVP) and of corticosteroid receptors (MR and GR) in the brain. Pretreatment of rats with a single dose of THP or P4 (50 micrograms/kg) significantly attenuated the elevation of plasma adrenocorticotropin (ACTH) and serum corticosterone after emotional stress; both steroids were, however, less potent than a similar dose of DEX. Administration of 1 mg of THP, CORT, or P4 to adrenalectomized (ADX) rats attenuated the increase in AVP mRNA levels in the ventromedial subdivision of the hypothalamic paraventricular nucleus (PVN), as compared with vehicle-treated ADX rats. However, whereas CORT and P4 influenced the ADX-induced increase in the transcription of both types of corticosteroid receptors in the hippocampus, these were unaffected by THP. In contrast to the glucocorticoids, THP and P4 failed to decrease plasma ACTH levels in rats deprived of endogenous steroids. These results demonstrate that the neurosteroid THP and its precursor P4 resemble glucocorticoids in their suppression of the pituitary-adrenal response to emotional stress; however, THP influences the transcription of glucocorticoid-responsive genes in brain structures involved in the regulation of the hypothalamo-pituitary-adrenal system in a fashion that is quite distinct from that obtained with glucocorticoids.

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BackgroundInfluential
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Background
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Background
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Self-citation
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Background
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Background
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Background
The 3β-hydroxysteroid dehydrogenase inhibitor trilostane shows antidepressant properties in mice
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“Likewise, GABAergic neuroactive steroids inhibit CRF production and release, ACTH release, and subsequent corticosterone levels in rodents (Owens et al. 1992; Patchev et al. 1994, 1996).”
Background
3α,5α-THP mediates progestins' effects to protect against adrenalectomy-induced cell death in the dentate gyrus of female and male rats
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“Some of these effects may be due in part to central modulation of 3α,5α-THP which can act in hypothalamus to attenuate neuroendocrine responses to a stressor and restore homeostasis (Patchev et al., 1994, 1996).”
Background
Decreased anticonvulsant efficacy of allopregnanolone during ethanol withdrawal in female Withdrawal Seizure-Prone vs. Withdrawal Seizure-Resistant mice
Beckley, E. H., Fretwell, A. M., Tanchuck, M. A., Gililland, K. R., Crabbe, J. C., & Finn, D. A. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.10.006 · Cited by 23
“…ALLO pre-treatment to decrease plasma corticosterone levels may be due to the anxiolytic effect of this steroid (e.g., Akwa et al., 1999; Bitran et al., 1991, 1999; Finn et al., 1997) and/or the ability of ALLO to decrease the stress-induced increase in HPA axis activation (Patchev et al., 1996).”
Background
Neurosteroids – From Basic Research to Clinical Perspectives
Frye, C. A. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00086-3 · Cited by 24
How is prenatal stress transmitted from the mother to the fetus?
Sze, Y., & Brunton, P. J. (2024) · Journal of Experimental Biology · doi:10.1242/jeb.246073 · Cited by 31
Anxiolytic and Anti-depressive Like Effects of Translocator Protein (18 kDa) Ligand YL-IPA08 in a Rat Model of Postpartum Depression
Ren, P., Ma, L., Wang, J.-Y., Guo, H., Sun, L. J., Gao, M., Liu, Y., Ma, Y., Li, Y., & Guo, W.-Z. (2020) · Neurochemical Research · doi:10.1007/s11064-020-03036-9 · Cited by 25
Giving a good start to a new life via maternal brain allostatic adaptations in pregnancy
Russell, J. A., & Brunton, P. J. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.003 · Cited by 24
5α-Reduced Neurosteroids Sex-Dependently Reverse Central Prenatal Programming of Neuroendocrine Stress Responses in Rats
Brunton, P. J., Donadio, M. V. F., Yao, S. T., Greenwood, M., Seckl, J. R., Murphy, D., & Russell, J. A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5104-13.2015 · Cited by 48
Relationship between omega-3 fatty acids and plasma neuroactive steroids in alcoholism, depression and controls.
Nieminen, L. R., Makino, K. K., Mehta, N., Virkkunen, M., Kim, H.-Y., & Hibbeln, J. R. (2006) · Prostaglandins, Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2006.07.012 · Cited by 23
“3a,5aTHP and THDOC potentiate GABAA receptor inhibition of the central nervous system [8] and have several anxiolytic properties [17,18] including: counteraction of the down regulated GABA receptor function observed in acute stress [19], decreased dopamine metabolism in prefrontal cortex [20], decreased gene expressio…”
Background
The Allopregnanolone Response to Acute Stress in Females: Preclinical and Clinical Studies
Pisu, M. G., Concas, L., Siddi, C., Serra, M., & Porcu, P. (2022) · Biomolecules · doi:10.3390/biom12091262 · Cited by 20
“Such elevations in allopregnanolone levels exert negative feedback upon the HPA axis, thus reducing the neuroendocrine response to stress by inhibiting CRH production and release, ACTH release, and the subsequent corticosterone increase in rats subjected to acute stress [15,16].”
Background
Low doses of prenatal ethanol exposure and maternal separation alter HPA axis function and ethanol consumption in adult male rats
Biggio, F., Talani, G., Locci, V., Pisu, M. G., Boero, G., Ciarlo, B., Grayson, D. R., & Serra, M. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.12.005 · Cited by 20
“, 1995), exerts a potent inhibitory action on HPA axis activity attenuating the increase of plasma ACTH and corticosterone elicited by stress (Bali and Jaggi, 2014; Biggio et al., 2004a; Rupprecht and Holsboer, 1999; Patchev et al. 1996).”
Progesterone reduces hyperactivity of female and male dopamine transporter knockout mice
Frye, C. A., & Sora, I. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.01.015 · Cited by 21
The role of neuroactive steroids in ethanol/stress interactions: proceedings of symposium VII at the Volterra conference on alcohol and stress, May 2008
Morrow, A. L., Biggio, G., Serra, M., Becker, H. C., Lopez, M. F., Porcu, P., Alward, S. E., & O’Buckley, T. K. (2009) · Alcohol · doi:10.1016/j.alcohol.2009.04.002 · Cited by 21
“Likewise, GABAergic neuroactive steroids inhibit CRF production, release, ACTH release and subsequent corticosterone levels in rodents (Owens et al., 1992; Patchev et al., 1996; Patchev et al., 1994).”
Neurosteroids and Traumatic Brain Injury: Translating Biomarkers to Therapeutics; Overview and Pilot Investigations in Iraq and Afghanistan Era Veterans
Marx, C., Naylor, J., Kilts, J., Dunn, C. E., Tupler, L. A., Szabo, S., Capehart, B., Morey, R., Shampine, L. J., & Acheson, S. (2016) · doi:10.1201/b18959-8 · Cited by 21
Progesterone Treatment of Adult Male Rats Suppresses Arginine Vasopressin Expression in the Bed Nucleus of the Stria Terminalis and the Centromedial Amygdala
Auger, C. J., & Vanzo, R. J. (2005) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2005.01400.x · Cited by 21
Neurosteroids for a successful pregnancy
Frye, C. A., Hirst, J. J., Brunton, P. J., & Russell, J. A. (2010) · Stress · doi:10.3109/10253890.2010.540050 · Cited by 19
“As such, neurosteroids like allopregnanolone have important benzodiazepine-like actions that are associated with reductions in stress responding and restoration of HPA homeostasis (Patchev et al. 1996; Barbaccia et al. 2001).”
Background
Cognitive impairment and increased brain neurosteroids in adult rats perinatally exposed to low millimolar blood alcohol concentrations
Barbaccia, M. L., Scaccianoce, S., Bianco, P. D., Campolongo, P., Trezza, V., Tattoli, M., Cuomo, V., & Steardo, L. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.06.013 · Cited by 19
Early postnatal stimulation alters pregnane neurosteroids in the hippocampus
Frye, C., Rhodes, M. E., Raol, Y. H., & Brooks-Kayal, A. (2006) · Psychopharmacology · doi:10.1007/s00213-005-0253-7 · Cited by 20
“…attribute causal effects of altered 3α,5α-THP levels on corticosterone levels from the present data, previous reports show that the administration of 3α,5α-THP significantly attenuates elevation of plasma ACTH and serum corticosterone following exposure to emotional stress (Patchev et al. 1996).”
ResultInfluential
Palatable Food Affects HPA Axis Responsivity and Forebrain Neurocircuitry in an Estrous Cycle-specific Manner in Female Rats
Egan, A. E., Thompson, A. M. K., Buesing, D., Fourman, S. M., Packard, A. E. B., Terefe, T., Li, D., Wang, X., Song, S., Solomon, M. B., et al. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.05.030 · Cited by 19
Ethnic differences in allopregnanolone concentrations in women during rest and following mental stress
Girdler, S. S., Mechlin, B., Light, K. C., & Morrow, A. L. (2006) · Psychophysiology · doi:10.1111/j.1469-8986.2006.00410.x · Cited by 18
Stress and cytokine effects on learning: What does sex have to do with it?
Beck, K. D., & Servatius, R. J. (2003) · Integrative Psychological and Behavioral Science · doi:10.1007/bf02688852 · Cited by 16
Die Neuroendokrinologie von Stress und die Pathophysiologie und Therapie von Depression und Angst
Ströhle, A. (2003) · Der Nervenarzt · doi:10.1007/s00115-002-1444-7 · Cited by 18
Microbiota modulates the steroid response to acute immune stress in male mice
Vagnerová, K., Gazárková, T., Vodička, M., Ergang, P., Klusoňová, P., Hudcovic, T., Šrůtková, D., Hermanová, P. P., Nováková, L., & Pácha, J. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1330094 · Cited by 18
Women recovering from social rejection: The effect of the person and the situation on a hormonal mechanism of affiliation
Duffy, K. A., Harris, L. T., Chartrand, T. L., & Stanton, S. J. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.11.017 · Cited by 18
“…of progesterone into allopregnanolone, a powerful anxiolytic that reduces stress in two ways: (1) by acting on GABA receptors in the brain and (2) by downregulating gene transcription for corticotrophin-releasing hormone in the HPA axis (Bitran et al., 1995, 1993; Patchev et al., 1996, 1994).”
Background
Differential hypothalamic–pituitary–adrenal activation of the neuroactive steroids pregnenolone sulfate and deoxycorticosterone in healthy controls and alcohol-dependent subjects
Porcu, P., O’Buckley, T. K., Morrow, A. L., & Adinoff, B. H. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.11.003 · Cited by 20
“Likewise, the GABAergic neuroactive steroids inhibit CRH production, ACTH release and corticosterone increase in rodents (Owens et al., 1992; Patchev et al., 1994; Patchev et al., 1996).”
Background
Intergenerational Perioperative Neurocognitive Disorder
Ju, L.-S., Morey, T. E., Seubert, C. N., & Martynyuk, A. E. (2023) · Biology · doi:10.3390/biology12040567 · Cited by 18
“GABA type A receptor (GABAAR)-mediated control of the CRH-releasing PVN neurons is another important mechanism regulating the HPA axis [83,104,105].”
Background
Prenatal Stress Alters Progestogens to Mediate Susceptibility to Sex-Typical, Stress-Sensitive Disorders, such as Drug Abuse: A Review
Frye, C. A., Paris, J. J., Osborne, D. M., Campbell, J. C., & Kippin, T. E. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00052 · Cited by 18
Ovarian Steroid Treatment Decreases Corticotropin-Releasing Hormone (CRH) mRNA and Protein in the Hypothalamic Paraventricular Nucleus of Ovariectomized Monkeys
Bethea, C. L., & Centeno, M. L. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301442 · Cited by 17
“In rodents, allopregnanolone attenuated endocrine responses to stress (Patchev et al, 1996) and progesterone, via conversion into allopregnanalone, attenuated CRH-enhanced startle (Toufexis et al, 2004).”
Background
Effects of neurosteroids on glucocorticoid receptor-mediated gene transcription in LMCAT cells—A possible interaction with psychotropic drugs
Basta‐Kaim, A., Budziszewska, B., Jaworska-Feil, L., Leśkiewicz, M., Tetich, M., Otczyk, M., Kubera, M., & Lasoń, W. (2006) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2006.02.004 · Cited by 18
Maternal Brain Adaptations in Pregnancy
Brunton, P. J., & Russell, J. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00044-2 · Cited by 18
Estrogen is necessary for 5α-pregnan-3α-ol-20-one (3α,5α-THP) infusion to the ventral tegmental area to facilitate social and sexual, but neither exploratory nor affective behavior of ovariectomized rats
Frye, C. A., Paris, J. J., & Rhodes, M. E. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.08.018 · Cited by 16
“In support, administration of systemic 3α,5α-THP reduces ACTH levels in response to intermittent air-puff exposure (Patchev et al., 1996).”
Background
Microarray profiling of gene expression patterns in adult male rat brain following acute progesterone treatment
Auger, C. J., Jessen, H. M., & Auger, A. P. (2005) · Brain Research · doi:10.1016/j.brainres.2005.10.033 · Cited by 14
The role of neuroactive steroids in tic disorders
Branca, C., & Bortolato, M. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105637 · Cited by 21
(3α,5α)3-hydroxypregnan-20-one (3α,5α-THP) regulation of hypothalamic and extrahypothalamic corticotropin releasing factor (CRF): Sexual dimorphism and brain region specificity in Sprague Dawley rats
Boero, G., Tyler, R. E., Todd, C. A., O’Buckley, T. K., Balan, I. S., Besheer, J., & Morrow, A. L. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108463 · Cited by 16
Effects of prenatal stress on neuroactive steroid responses to acute stress in adult male and female rats
Sze, Y., & Brunton, P. J. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12916 · Cited by 18
Sex differences in neurosteroid and hormonal responses to metyrapone in posttraumatic stress disorder
Inslicht, S. S., Richards, A. L., Madden, E., Rao, M. N., O’Donovan, A., Talbot, L. S., Rucker, E., Metzler, T. J., Hauger, R. L., & Neylan, T. C. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3621-3 · Cited by 17
3α5β-Pregnanolone glutamate, a use-dependent NMDA antagonist, reversed spatial learning deficit in an animal model of schizophrenia.
Valeš, K., Rambousek, L., Holubová, K., Svoboda, J., Bubeníková-Valešová, V., Chodounská, H., Vyklický, L., & Stuchlík, A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.07.020 · Cited by 15
Role of progestins with partial antiandrogenic effects
Sitruk-Ware, R. L., Husmann, F., Thijssen, J. H. H., Skouby, S. O., Fruzzetti, F., Hanker, J. P., Huber, J., & Druckmann, R. A. (2004) · Climacteric · doi:10.1080/13697130400001307 · Cited by 15

Authors: Patchev, V
Affiliations: Max Planck Institute of Psychiatry (DE)
Corresponding author: Patchev, V
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 1996-12
Volume: 15
Issue: 6
Pages: 533-540
ISSN: 0893-133X (ISSN-L)
DOI: 10.1016/s0893-133x(96)00096-6
OpenAlex: W2072990514
Cited by: 283
References: 0
Citations by year: 2026: 3 · 2025: 4 · 2024: 10 · 2023: 5 · 2022: 5 · 2021: 9 · 2020: 8 · 2019: 11 · 2018: 10 · 2017: 3 · 2016: 10 · 2015: 6 · 2014: 16 · 2013: 12 · 2012: 11
FWCI: 3.47
Type: journal article
Language: en
Open access: closed
Locations: Neuropsychopharmacology (publishedVersion)
PubMed (publishedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: Deutsche Forschungsgemeinschaft
Max-Planck-Gesellschaft
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: tetrahydroprogesterone, allopregnanolone, neurosteroids, progesterone, pituitary-adrenal response, emotional stress, vasopressin, paraventricular nucleus, corticosteroid receptors, mineralocorticoid receptor, glucocorticoid receptor, ACTH, corticosterone, dexamethasone, adrenalectomy, hypothalamus
MeSH terms: Adrenocorticotropic Hormone, Animals, Anti-Inflammatory Agents, Arginine Vasopressin, Corticosterone, Dexamethasone, Glucocorticoids, Hypothalamus, Male, Pregnanolone, Progesterone, Receptors, Steroid, Stress, Psychological, Anti-Anxiety Agents, Transcription, Genetic, Rats, Wistar, Neuroprotective Agents, Rats

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The Neurosteroid Tetrahydroprogesterone Attenuates the Endocrine Response to Stress and Exerts Glucocorticoid-like Effects on Vasopressin Gene Transcription in the Rat Hypothalamus

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