AKR1C3-mediated adipose androgen generation drives lipotoxicity in women with polycystic ovary syndrome
Open accessAbstract
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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Insulin stimulates AKR1C3 expression in adipose tissue of women with polycystic ovary syndrome (PCOS).
“Insulin stimulates AKR1C3 expression in the adipose tissue of women with PCOS and its inhibition has been suggested as offering a therapeutic target to reduce the hyperandrogenism that is a feature of this disorder [101].”
From Endometrial Intracrinology: Oestrogens, Androgens and Endometrial Disorders (2018) · cites this paper as [101]
The Results report that insulin increased AKR1C3 expression in cultured primary female subcutaneous adipocytes, and the Methods identify their donors as healthy women—not women with PCOS. The paper also reports increased AKR1C3 expression in PCOS adipose tissue and proposes AKR1C3 as a therapeutic target, but it does not demonstrate insulin-stimulated expression in adipose tissue from women with PCOS. Page numbers were not provided in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredPharmacologic inhibition of AKR1C3 activity prevented androgen-mediated adverse effects on adipocyte lipogenesis.
“Using a human preadipocyte cell line, both testosterone and DHT increased de novo lipogenesis in the absence of insulin [95], whereas pharmacologic inhibition of AKR1C3 activity prevented androgen-mediated adverse effects on adipocyte lipogenesis.”
From Polycystic Ovary Syndrome: Pathophysiology, Presentation, and Treatment With Emphasis on Adolescent Girls (2019) · cites this paper as [95]
In the human preadipocyte cell line, insulin increased AKR1C3 expression.
“Using this model system, insulin increased AKR1C3 expression.”
From Polycystic Ovary Syndrome: Pathophysiology, Presentation, and Treatment With Emphasis on Adolescent Girls (2019) · cites this paper as [95]
In a human preadipocyte cell line, both testosterone and DHT increased de novo lipogenesis in the absence of insulin.
“Using a human preadipocyte cell line, both testosterone and DHT increased de novo lipogenesis in the absence of insulin [95], whereas pharmacologic inhibition of AKR1C3 activity prevented androgen-mediated adverse effects on adipocyte lipogenesis.”
From Polycystic Ovary Syndrome: Pathophysiology, Presentation, and Treatment With Emphasis on Adolescent Girls (2019) · cites this paper as [95]
A deep in vivo metabolic phenotyping study showed increased AKR1C3 and decreased SRD5A1 mRNA expression in subcutaneous fat of women with PCOS.
“A deep in vivo metabolic phenotyping study showed increased AKR1C3 and decreased SRD5A1 mRNA expression in subcutaneous fat of women with PCOS [95].”
From Polycystic Ovary Syndrome: Pathophysiology, Presentation, and Treatment With Emphasis on Adolescent Girls (2019) · cites this paper as [95]
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Self-citation
- 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
- 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
- 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 › Epidemiology › 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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