Cited by 215Ovarian function and disordersAdipokines, Inflammation, and Metabolic DiseasesLipid metabolism and biosynthesis

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AKR1C3-Mediated Adipose Androgen Generation Drives Lipotoxicity in Women With Polycystic Ovary Syndrome

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O’Reilly, Michael W, Kempegowda, Punith, Walsh, Mark, Taylor, Angela E, Manolopoulos, Konstantinos N, Allwood, J William, Semple, Robert K, Hebenstreit, Daniel, Dunn, Warwick B, Tomlinson, Jeremy W, Arlt, Wiebke·2017·The Journal of Clinical Endocrinology & Metabolism

DOI 10.1210/jc.2017-00947PMC PMC5587066

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Abstract

Context: Polycystic ovary syndrome (PCOS) is a prevalent metabolic disorder occurring in up to 10% of women of reproductive age. PCOS is associated with insulin resistance and cardiovascular risk. Androgen excess is a defining feature of PCOS and has been suggested as causally associated with insulin resistance; however, mechanistic evidence linking both is lacking. We hypothesized that adipose tissue is an important site linking androgen activation and metabolic dysfunction in PCOS. Methods: We performed a human deep metabolic in vivo phenotyping study examining the systemic and intra-adipose effects of acute and chronic androgen exposure in 10 PCOS women, in comparison with 10 body mass index-matched healthy controls, complemented by in vitro experiments. Results: PCOS women had increased intra-adipose concentrations of testosterone (P = 0.0006) and dihydrotestosterone (P = 0.01), with increased expression of the androgen-activating enzyme aldo-ketoreductase type 1 C3 (AKR1C3) (P = 0.04) in subcutaneous adipose tissue. Adipose glycerol levels in subcutaneous adipose tissue microdialysate supported in vivo suppression of lipolysis after acute androgen exposure in PCOS (P = 0.04). Mirroring this, nontargeted serum metabolomics revealed prolipogenic effects of androgens in PCOS women only. In vitro studies showed that insulin increased adipose AKR1C3 expression and activity, whereas androgen exposure increased adipocyte de novo lipid synthesis. Pharmacologic AKR1C3 inhibition in vitro decreased de novo lipogenesis. Conclusions: These findings define an intra-adipose mechanism of androgen activation that contributes to adipose remodeling and a systemic lipotoxic metabolome, with intra-adipose androgens driving lipid accumulation and insulin resistance in PCOS. AKR1C3 represents a promising therapeutic target in PCOS.

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Authors: O’Reilly, M. W., Kempegowda, P., Walsh, M., Taylor, A. E., Manolopoulos, K. N., Allwood, J. W., Semple, R. K., Hebenstreit, D., Dunn, W. B., Tomlinson, J. W., & Arlt, W.
Affiliations: University of Birmingham (GB)
University of Warwick (GB)
University of Cambridge (GB)
Churchill Hospital (GB)
NIHR Birmingham Liver Biomedical Research Unit (GB)
Corresponding author: Arlt, Wiebke
ORCID: O’Reilly, Michael W
Kempegowda, Punith
Walsh, Mark
Taylor, Angela E
Manolopoulos, Konstantinos N
Allwood, J William
Semple, Robert K
Hebenstreit, Daniel
Dunn, Warwick B
Tomlinson, Jeremy W
Arlt, Wiebke
Venue: The Journal of Clinical Endocrinology & Metabolism
Publisher: The Endocrine Society
Published: 2017-06-22
Volume: 102
Issue: 9
Pages: 3327-3339
ISSN: 0021-972X (ISSN-L)
1945-7197
DOI: 10.1210/jc.2017-00947
PMC: PMC5587066
OpenAlex: W2684997942
Cited by: 215
References: 48
Citations by year: 2026: 30 · 2025: 36 · 2024: 23 · 2023: 25 · 2022: 21 · 2021: 24 · 2020: 21 · 2019: 20 · 2018: 14 · 2017: 1
FWCI: 17.73
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
Locations: The Journal of Clinical Endocrinology & Metabolism (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Spiral (Imperial College London) (submittedVersion, cc-by)
Apollo (University of Cambridge) (submittedVersion, cc-by)
Apollo (cc-by)
Funders: Bayer
Wellcome Trust (099909, 098498/Z/12/Z, 092283, WT098498)
National Institute for Health and Care Research
National Institutes of Health
Directorate for Biological Sciences
Medical Research Council (MR/M009157/1, MR/P011462/1)
Biotechnology and Biological Sciences Research Council (BB/L006340/1)
Topics: Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Keywords: polycystic ovary syndrome, AKR1C3, testosterone, dihydrotestosterone, lipotoxicity, insulin resistance, lipolysis, de novo lipogenesis, adipose tissue remodeling, serum metabolomics, insulin signaling
MeSH terms: Aldo-Keto Reductase Family 1 Member C3, Adolescent, Adult, Analysis of Variance, Androgens, Cells, Cultured, Dehydroepiandrosterone, Female, Humans, Hydroxyprostaglandin Dehydrogenases, Insulin Resistance, Lipolysis, Polycystic Ovary Syndrome, Reference Values, 3-Hydroxysteroid Dehydrogenases, Biomarkers, Case-Control Studies, Adipocytes, Statistics, Nonparametric, Area Under Curve, Subcutaneous Fat, Lipid Metabolism, Young Adult, Real-Time Polymerase Chain Reaction

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AKR1C3-Mediated Adipose Androgen Generation Drives Lipotoxicity in Women With Polycystic Ovary Syndrome

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