Cited by 130Hormonal Regulation and HypertensionEstrogen and related hormone effectsAdrenal Hormones and Disorders

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Agonistic and antagonistic properties of progesterone metabolites at the human mineralocorticoid receptor

Quinkler, M, Meyer, B, Bumke-Vogt, C, Grossmann, C, Gruber, U, Oelkers, W, Diederich, S, Bahr, V·2002·European Journal of Endocrinology

DOI 10.1530/eje.0.1460789

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Abstract

OBJECTIVE: Progesterone binds to the human mineralocorticoid receptor (hMR) with nearly the same affinity as do aldosterone and cortisol, but confers only low agonistic activity. It is still unclear how aldosterone can act as a mineralocorticoid in situations with high progesterone concentrations, e.g. pregnancy. One mechanism could be conversion of progesterone to inactive compounds in hMR target tissues. DESIGN: We analyzed the agonist and antagonist activities of 16 progesterone metabolites by their binding characteristics for hMR as well as functional studies assessing transactivation. METHODS: We studied binding affinity using hMR expressed in a T7-coupled rabbit reticulocyte lysate system. We used co-transfection of an hMR expression vector together with a luciferase reporter gene in CV-1 cells to investigate agonistic and antagonistic properties. RESULTS: Progesterone and 11beta-OH-progesterone (11beta-OH-P) showed a slightly higher binding affinity than cortisol, deoxycorticosterone and aldosterone. 20alpha-dihydro(DH)-P, 5alpha-DH-P and 17alpha-OH-P had a 3- to 10-fold lower binding potency. All other progesterone metabolites showed a weak affinity for hMR. 20alpha-DH-P exhibited the strongest agonistic potency among the metabolites tested, reaching 11.5% of aldosterone transactivation. The agonistic activity of 11beta-OH-P, 11alpha-OH-P and 17alpha-OH-P was 9, 5.1 and 4.1% respectively. At a concentration of 100 nmol/l, progesterone, 17alpha-OH-P and 20alpha-DH-P inhibit nearly 75, 40 and 35% of the transactivation by aldosterone respectively. All other progesterone metabolites tested demonstrate weaker affinity, and agonistic and antagonistic potency. CONCLUSIONS: The binding affinity for hMR and the agonistic and antagonistic activity diminish with increasing reduction of the progesterone molecule at C20, C17 and at ring A. We assume that progesterone metabolism to these compounds is a possible protective mechanism for hMR. 17alpha-OH-P is a strong hMR antagonist and could exacerbate mineralocorticoid deficiency in patients with congenital adrenal hyperplasia.

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“the MR-dependent activity of a gene-reporter in transiently transfected cell lines (Grassi et al., 1997; Agarwal and Mirashi, 2000; Piwien-Pilipuk et al., 2002a; Quinkler et al., 2002), which evidences the enormous differences that can be obtained by working with an integrated biological effect under in vivo condition…”
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“Aldosterone binding characteristics were determined as previously described ( 22 ).”
Background
Immunohistochemical Demonstration of the Mineralocorticoid Receptor, 11β-Hydroxysteroid Dehydrogenase-1 and −2, and Hexose-6-phosphate Dehydrogenase in Rat Ovary
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Sex and Gender Related Differences in Diabetic Kidney Disease
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“…local inactivation of the progesterone pre-receptor by the enzyme 20-alpha-hydroxysteroid-dehydrogenase (AKR1C1), which converts progesterone to inactive 20-hydroxy-progesterone [58], exhibits reduced affinity for the human mineralocorticoid receptor (Ki 10.8 nM and IC50 282.5 nM) [51,59,60] (Fig.”
BackgroundInfluential
Low potassium level during the first half of pregnancy is associated with lower risk for the development of gestational diabetes mellitus and severe pre-eclampsia
Wolak, T., Sergienko, R., Wiznitzer, A., Shlush, L. B., Paran, E., & Sheiner, E. (2010) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767050903544736 · Cited by 21
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Background
Sex-dependent association of mineralocorticoid receptor gene (NR3C2) DNA methylation and schizophrenia.
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“In addition, based on the reported affinity of deoxycorticosterone for the mineralocorticoid receptor [47] and on the very low aldosterone synthase mRNA level in fetal lungs ([22] and data not shown), one would suggest that this steroid could have also mineralocorticoid effects in the lung.”
Background
Modified-release hydrocortisone is associated with lower plasma renin activity in patients with salt-wasting congenital adrenal hyperplasia
Tschaidse, L., Reisch, N., Arlt, W., de la Perrière, A. B., Hirschberg, A. L., Juul, A., Mallappa, A., Merke, D. P., Newell-Price, J. D. C., Perry, C. G., et al. (2023) · European Journal of Endocrinology · doi:10.1093/ejendo/lvac006 · Cited by 15
“13 These studies revealed that 17OHP binds well to the hMR (Ki = 16.5 nmol L –1 ), possesses only a weak agonistic effect (ED 50 > 1000 nmol L –1 ), but a strong antagonistic effect with an IC 50 of 135 nmol L –1 .”
BackgroundInfluential
Mineralocorticoid replacement during infancy for salt wasting congenital adrenal hyperplasia due to 21-hydroxylase deficiency
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“Additionally, in 21OHD patients, the accumulated androgen precursors, progesterone and 17OH-progesterone (17OHP) inhibit mineralocorticoid receptor transactivation by aldosterone (20).”
Background
Luteal Lipid Droplets: A Novel Platform for Steroid Synthesis
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“Furthermore, progesterone metabolites have weak affinity for human mineralocorticoid receptors and can demonstrate either agonistic or antagonistic effects, although the main role of progesterone metabolism in the kidney, especially during pregnancy, is the protection of the mineralocorticoid receptor against high pro…”
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Maternal Adaptation to Pregnancy
Thornburg, K. L. R., Bagby, S. P., & Giraud, G. D. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50059-2 · Cited by 12
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“0 nmol/L) using CV-1 cells transfected with hMR and the luciferase reporter gene [28].”
Method
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“Contributing factors to this altered fluid homeostasis include vasodilatation from uteroplacental derived prostaglandins which inhibit the effect of increased angiotensin II [48], and progesterone’s action as a mineralocorticoid receptor antagonist [49].”
Background
Case report of severe Cushing’s syndrome in medullary thyroid cancer complicated by functional diabetes insipidus, aortic dissection, jejunal intussusception, and paraneoplastic dysautonomia: remission with sorafenib without reduction in cortisol concentration
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“Progesterone exhibits the same affinity as aldosterone for the human mineralocorticoid receptor, acting as antagonist [16].”
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Does Stress Elicit Depression? Evidence From Clinical and Preclinical Studies
Sickmann, H. M., Li, Y., Mørk, A., Sánchez, C., & Gulinello, M. E. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_292 · Cited by 10
“Progestins can also bind to both the MR and the GR (Myles and Funder 1996; Quinkler et al. 2002).”
Renal tubular acidosis type 4 in pregnancy
Jakes, A. D., Baynes, K., & Nelson‐Piercy, C. (2016) · BMJ Case Reports · doi:10.1136/bcr-2016-214798 · Cited by 10
11α-Hydroxyprogesterone, a potent 11β-hydroxysteroid dehydrogenase inhibitor, is metabolised by steroid-5α-reductase and cytochrome P450 17α-hydroxylase/17,20-lyase to produce C11α-derivatives of 21-deoxycortisol and 11-hydroxyandrostenedione in vitro
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The metabolic fate and receptor interaction of 16α-hydroxyprogesterone and its 5α-reduced metabolite, 16α-hydroxy-dihydroprogesterone
van Rooyen, D., du Toit, T., Toit, R. L.-D., Africander, D., Swart, P., & Swart, A. C. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.09.025 · Cited by 9
Unraveling the steroid hormone response in male marathon runners: Correlation of running time with aldosterone and progesterone
Bae, Y. J., Kratzsch, J., Zeidler, R. B., Fikenzer, S., Werner, C., Herm, J., Jungehulsing, G. J., Endres, M., Hæusler, K. G., Thiery, J., et al. (2019) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2019.105473 · Cited by 8
The Physiological Roles of the Renin-Angiotensin Aldosterone System and Vasopressin in Human Pregnancy
Lumbers, E. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-814823-5.00010-6 · Cited by 9
Mineralocorticoid replacement therapy in salt‐wasting congenital adrenal hyperplasia
Lang, K., Quinkler, M. O., & Kienitz, T. (2023) · Clinical Endocrinology · doi:10.1111/cen.14959 · Cited by 7
“17 In terms of intrinsic activity, judged by induction of gene expression, aldosterone was demonstrated to be the most potent MR agonist.”
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Androgen levels are associated with blood pressure in pregnant women after term
Carlsen, S. M., & Heimstad, R. (2011) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/j.1600-0412.2011.01280.x · Cited by 7
“However, progesterone binds to the human mineralocorticoid receptor and exerts both agonistic and antagonistic effects (23).”
Background
Decreased renal expression of PAQR5 is associated with the absence of a nephroprotective effect of progesterone in a rat UUO model
Abramicheva, P. A., Semenovich, D. S., Zorova, L. D., Pevzner, I. B., Sokolov, I. A., Popkov, V. A., Kazakov, E. P., Zorov, D. B., & Plotnikov, E. Y. (2023) · Scientific Reports · doi:10.1038/s41598-023-39848-2 · Cited by 6
“Progesterone was long believed to exert its effects in the kidney by binding to high-affinity mineralocorticoid receptors 27–29 , until identification of progesterone receptors that are predominantly expressed in kidney tissue, namely the membrane receptors PAQR5 and the nuclear receptors nPR-A and…”
Biological activity and ligand binding mode to the progesterone receptor of A-homo analogues of progesterone
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Association of Elevated Serum Aldosterone Concentrations in Pregnancy with Hypertension
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Background
Evidence of the Role of Inflammation and the Hormonal Environment in the Pathogenesis of Adrenal Myelolipomas in Congenital Adrenal Hyperplasia
Kolli, V., Frucci, E., da Cunha, I. W., Iben, J., Kim, S. A., Mallappa, A., Li, T., Faucz, F. R., Kebebew, E., Nilubol, N., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25052543 · Cited by 3
Polycystic Ovary Syndrome Accompanied by Hyperandrogenemia or Metabolic Syndrome Triggers Glomerular Podocyte Injury
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Relationship between levels of sex hormones and response to cardiac resynchronisation therapy in men
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“В экспериментальных работах были показаны кардиопротективные эффекты PGN: иммуносупрессивный [41, 42], антиминералокортикоидный [43, 44], антиапоптотический [45].”
Histone deacetylase inhibition, but not a mineralocorticoid receptor antagonist spironolactone, attenuates atypical transcription by an activating mutant MR ( MRS 810L)
Kang, S., Lee, H., Lee, E., Kim, M., & Kim, I. (2016) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12614 · Cited by 3
The Autonomic Nervous System and Its Functions
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Association of sex hormone dynamics with 10-year survival in men with implanted cardiac resynchronization therapy devices
Enina, T. N., Евгеньевич, Ш. Н., & Petelina, T. I. (2022) · Journal of Arrhythmology · doi:10.35336/va-2022-2-01 · Cited by 2

Authors: Quinkler, M., Meyer, B., Bumke-Vogt, C., Grossmann, C., Gruber, U., Oelkers, W., Diederich, S., & Bahr, V
Affiliations: Freie Universität Berlin (DE)
Corresponding author: Quinkler, M
ORCID: Quinkler, M
Grossmann, C
Diederich, S
Venue: European Journal of Endocrinology
Publisher: Oxford University Press (OUP)
Published: 2002-06-01
Volume: 146
Issue: 6
Pages: 789-799
ISSN: 0804-4643 (ISSN-L)
1479-683X
DOI: 10.1530/eje.0.1460789
OpenAlex: W2165755939
Cited by: 130
References: 59
Citations by year: 2026: 4 · 2025: 3 · 2024: 8 · 2023: 8 · 2022: 6 · 2021: 7 · 2020: 8 · 2019: 7 · 2018: 3 · 2017: 7 · 2016: 8 · 2015: 5 · 2014: 10 · 2013: 3 · 2012: 3
FWCI: 1.73
Type: journal article
Language: en
Open access: closed
Locations: European Journal of Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: Deutsche Forschungsgemeinschaft
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal Regulation and Hypertension
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
Keywords: progesterone metabolites, receptor binding affinity, agonist activity, antagonist activity, 17-hydroxyprogesterone, 20alpha-dihydroprogesterone, 11β-hydroxyprogesterone, aldosterone, mineralocorticoid deficiency, congenital adrenal hyperplasia, pregnancy, transcriptional activation
MeSH terms: Aldosterone, Mineralocorticoid Receptor Antagonists, Animals, Desoxycorticosterone, Humans, Hydrocortisone, Luciferases, Progesterone, Rabbits, Reticulocytes, Transcription, Genetic, Transfection, Protein Biosynthesis, Transcriptional Activation, Receptors, Mineralocorticoid

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Agonistic and antagonistic properties of progesterone metabolites at the human mineralocorticoid receptor

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