Structure, function and tissue-specific gene expression of 3β-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase enzymes in classical and peripheral intracrine steroidogenic tissues.

Labrie, Fernand; Simard, Jacques; Van Luu-The; Bélanger, Alain; Pelletier, Georges

doi:10.1016/0960-0760(92)90308-6

Cited by 132Adrenal Hormones and DisordersEstrogen and related hormone effectsSexual Differentiation and Disorders

Structure, function and tissue-specific gene expression of 3β-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase enzymes in classical and peripheral intracrine steroidogenic tissues.

Labrie, Fernand, Simard, Jacques, Van Luu-The, Bélanger, Alain, Pelletier, Georges·1992·The Journal of Steroid Biochemistry and Molecular Biology

DOI 10.1016/0960-0760(92)90308-6

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Abstract

The membrane-bound enzyme 3β-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase (3β-HSD) catalyses an essential step in the transformation of all 5-pregnen-3β-ol and 5-androsten-3β-ol steroids into the corresponding 3-keto-4-ene-steroids, namely progesterone as well as all the precursors of androgens, estrogens, glucocorticoids and mineralocorticoids. We have recently characterized two types of human 3β-HSD cDNA clones and the corresponding genes which encode type I and II 3β-HSD isoenzymes of 372 and 371 amino acids, respectively, and share 93.5% homology. The human 3β-HSD genes containing 4 exons were assigned by in situ hybridization to the p11-p13 region of the short arm of chromosome 1. Human type I 3β-HSD is the almost exclusive mRNA species present in the placenta and skin while the human type II is the predominant mRNA species in the adrenals, ovaries and testes. The type I protein possesses higher 3β-HSD activity than type II. We elucidated the structures of three types of rat 3β-HSD cDNAs as well that of one type of 3β-HSD from bovine and macaque ovary λgt11 cDNA libraries, which all encode a 372 amino acid protein. The rat type I and II 3β-HSD proteins expressed in the adrenals, gonads and adipose tissue share 93.8% homology. Transient expression of human type I and II as well as rat type I and II 3β-HSD cDNAs in HeLa human cervical carcinoma cells reveals that 3β-ol dehydrogenase and 5-ene-4-ene isomerase activities reside within a single protein. These expressed 3β-HSD proteins convert 3β-hydroxy-5-ene-steroids into 3-keto-4-ene derivatives and catalyze the interconversion of 3β-hydroxy and 3-keto-5α-androstane steroids. By site-directed mutagenesis, we demonstrated that the lower activity of expressed rat type II compared to rat type I 3β-HSD is due to a change of four residues probably involved in a membrane-spanning domain. When homogenates from cells transfected with a plasmid vector containing rat type I 3β-HSD is incubated in the presence of dihydrotestosterone (DHT) using NAD⁺ as co-factor, 5α-androstanedione was formed (A-dione), indicating an intrinsic androgenic 17β-hydroxysteroid dehydrogenase (17β-HSD) activity of this 3β-HSD. We cloned a third type of rat cDNA encoding a predicted type III 3β-HSD specifically expressed in the rat liver, which shares 80% similarity with the two other isoenzymes. Transient expression in human HeLa cells reveals that the type III isoenzyme does not display oxidative activity for the classical substrates of 3β-HSD. However, in common with the type I enzyme, it converts A-dione and DHT to the corresponding 3β-hydroxysteroids, thus showing an exclusive 3-ketosteroid reductase activity. When NADPH is used as co-factor, the affinity for DHT of the type III enzyme becomes 10-fold higher than that of the type I. Rat type III mRNA was below the detection limit in intact female liver. Following hypophysectomy, its concentration increased to 55% of the values measured in intact or hypophysectomized male rats, an increase which can be blocked by administration of ovine prolactin (oPRL). Treatment with oPRL for 10 days starting 15 days after hypophysectomy markedly decreased ovarian 3β-HSD mRNA accumulation accompanied by a similar decrease in 3β-HSD activity and protein levels. Treatment with the gonadotropin hCG reversed the potent inhibitory effect of oPRL on these parameters and stimulated 3β-HSD mRNA levels in ovarian interstitial cells. These data indicate that the presence of multiple 3β-HSD isoenzymes offers the possibility of tissue-specific expression and regulation of this enzymatic activity that plays an essential role in the biosynthesis of all hormonal steroids in classical as well as peripheral intracrine steroidogenic tissues.

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Women at menopause are not only deprived from estrogens because of rapid loss of ovarian activity but also have been deprived from androgens for a longer period because of progressive decrease of serum DHEA levels starting years before menopause.
“women, at menopause, are not only deprived from estrogens because of a rapid loss of ovarian activity but also have been deprived from androgens for a longer period because of a progressive decrease of serum DHEA levels starting quite a few years before menopause.”
From Endocrine and intracrine sources of androgens in women: inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone (2003) · cites this paper as [84]

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Authors: Labrie, F., Simard, J., Luu-The, V., Bélanger, A., & Pelletier, G.
Affiliations: Centre hospitalier de l'Université Laval (CA)
Corresponding author: Labrie, Fernand
ORCID: Simard, Jacques
Venue: The Journal of Steroid Biochemistry and Molecular Biology
Publisher: Elsevier BV
Published: 1992-12
Volume: 43
Issue: 8
Pages: 805-826
ISSN: 0960-0760 (ISSN-L)
DOI: 10.1016/0960-0760(92)90308-6
OpenAlex: W2020387392
Cited by: 132
References: 111
Citations by year: 2025: 1 · 2024: 1 · 2022: 4 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 4 · 2015: 3 · 2014: 4 · 2013: 1 · 2012: 1
FWCI: 8.18
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: The Journal of Steroid Biochemistry and Molecular Biology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Keywords: steroidogenic enzymes, tissue-specific gene expression, cDNA cloning, enzyme structure, site-directed mutagenesis, enzyme kinetics
MeSH terms: Adrenal Cortex Hormones, Adrenal Glands, Androstanes, Animals, Female, Humans, Male, Multienzyme Complexes, Organ Specificity, Ovary, Pregnanes, Progesterone Reductase, Steroid Isomerases, Steroids, Testis, 3-Hydroxysteroid Dehydrogenases, Gene Expression Regulation, Enzymologic, Autocrine Communication

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Structure, function and tissue-specific gene expression of 3β-hydroxysteroid dehydrogenase/5-ene-4-ene isomerase enzymes in classical and peripheral intracrine steroidogenic tissues.

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