Steroid sulphatase and its inhibitors: past, present, and future

Foster, Paul A.

doi:10.3390/molecules26102852

Cited by 49Estrogen and related hormone effectsSteroid Chemistry and BiochemistryProstate Cancer Treatment and Research

Steroid sulphatase and its inhibitors: past, present, and future

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Foster, Paul A.·2021·Molecules

DOI 10.3390/molecules26102852PMC PMC8151039

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Abstract

Steroid sulphatase (STS), involved in the hydrolysis of steroid sulphates, plays an important role in the formation of both active oestrogens and androgens. Since these steroids significantly impact the proliferation of both oestrogen- and androgen-dependent cancers, many research groups over the past 30 years have designed and developed STS inhibitors. One of the main contributors to this field has been Prof. Barry Potter, previously at the University of Bath and now at the University of Oxford. Upon Prof. Potter's imminent retirement, this review takes a look back at the work on STS inhibitors and their contribution to our understanding of sulphate biology and as potential therapeutic agents in hormone-dependent disease. A number of potent STS inhibitors have now been developed, one of which, Irosustat (STX64, 667Coumate, BN83495), remains the only one to have completed phase I/II clinical trials against numerous indications (breast, prostate, endometrial). These studies have provided new insights into the origins of androgens and oestrogens in women and men. In addition to the therapeutic role of STS inhibition in breast and prostate cancer, there is now good evidence to suggest they may also provide benefits in patients with colorectal and ovarian cancer, and in treating endometriosis. To explore the potential of STS inhibitors further, a number of second- and third-generation inhibitors have been developed, together with single molecules that possess aromatase-STS inhibitory properties. The further development of potent STS inhibitors will allow their potential therapeutic value to be explored in a variety of hormone-dependent cancers and possibly other non-oncological conditions.

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T3S is markedly preferred as a substrate over T3 by the D1 deiodinase enzyme expressed in the liver, kidney, and intestine.
“T3S is markedly preferred as a substrate over T3 by the D1 deiodinase enzyme expressed in the liver, kidney, and intestine (67).”
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The Use of Steroid Sulfatase Inhibitors as a Novel Therapeutic Strategy Against Hormone-Dependent Endometrial Cancer
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Synthesis and biochemical studies of estrone sulfatase inhibitors
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Inhibition of estrone sulfatase enzyme in human placenta and human breast carcinoma
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Human steroid sulfatase induces Wnt/β-catenin signaling and epithelial-mesenchymal transition by upregulating Twist1 and HIF-1α in human prostate and cervical cancer cells
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The Development of Steroid Sulfatase Inhibitors for Hormone‐Dependent Cancer Therapy
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Docking studies of sulphamate inhibitors of estrone sulphatase in human carbonic anhydrase II
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Dehydroepiandrosterone (DHEA) is an anabolic steroid like dihydrotestosterone (DHT), the most potent natural androgen, and tetrahydrogestrinone (THG)
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Recent advances in the development of steroid sulphatase inhibitors
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Expression level of enzymes related to in situ estrogen synthesis and clinicopathological parameters in breast cancer patients
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Regulation and Inhibition of Steroid Sulfatase Activity in Breast Cancer a
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Estrone sulfate (E1S), a prognosis marker for tumor aggressiveness in prostate cancer (PCa)
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A phase I dose escalation study to determine the optimal biological dose of irosustat, an oral steroid sulfatase inhibitor, in postmenopausal women with estrogen receptor-positive breast cancer
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Efficacy of three potent steroid sulfatase inhibitors: pre-clinical investigations for their use in the treatment of hormone-dependent breast cancer
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Clinical significance of the estrogen-modifying enzymes steroid sulfatase and estrogen sulfotransferase in epithelial ovarian cancer
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The Significance of the Sulfatase Pathway for Local Estrogen Formation in Endometrial Cancer
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Steroid Sulfatase Expression in Ovarian Clear Cell Adenocarcinoma: Immunohistochemical Study
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Synthesis and Structure–Activity Relationship Studies of Derivatives of the Dual Aromatase–Sulfatase Inhibitor 4‐{[(4‐Cyanophenyl)(4H‐1,2,4‐triazol‐4‐yl)amino]methyl}phenyl sulfamate
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Estrone sulfate transport and steroid sulfatase activity in colorectal cancer: implications for hormone replacement therapy
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Sulfate derivatives of 2-phenylindols as novel steroid sulfatase inhibitors
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Immunolocalization of estrogen‐producing and metabolizing enzymes in benign breast disease: Comparison with normal breast and breast carcinoma
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First Dual Inhibitors of Steroid Sulfatase (STS) and 17β-Hydroxysteroid Dehydrogenase Type 1 (17β-HSD1): Designed Multiple Ligands as Novel Potential Therapeutics for Estrogen-Dependent Diseases
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IPET study: an FLT-PET window study to assess the activity of the steroid sulfatase inhibitor irosustat in early breast cancer
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Evidence of estrone-sulfate uptake modification in young and middle-aged rat prostate
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Interaction of Androst-5-ene-3β,17β-diol and 5α-androstane-3β,17β-diol with estrogen and androgen receptors: A combined binding and cell study
Chen, J., Wang, W., & Lin, S. (2013) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2013.01.012 · Cited by 27 · see citing works
In SituSteroid Sulfatase Activity in Human Epithelial Carcinoma Cells of Vaginal, Ovarian, and Endometrial Origin*
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High mRNA levels of 17β-hydroxysteroid dehydrogenase type 1 correlate with poor prognosis in endometrial cancer
Cornel, K. M. C., Krakstad, C., Delvoux, B., Xanthoulea, S., Jori, B., Bongers, M. Y., Konings, G. F. J., Kooreman, L. F. S., Kruitwagen, R. F., Salvesen, H. B., et al. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.11.030 · Cited by 26 · see citing works
Bicyclic Derivatives of the Potent Dual Aromatase–Steroid Sulfatase Inhibitor 2‐Bromo‐4‐{[(4‐cyanophenyl)(4H‐1,2,4‐triazol‐4‐yl)amino]methyl}phenylsulfamate: Synthesis, SAR, Crystal Structure, and in vitro and in vivo Activities
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Conversion of circulating estrone sulfate to 17β-estradiol by ovarian tumor tissue: A possible mechanism behind elevated circulating concentrations of 17β-estradiol in postmenopausal women with ovarian tumors
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Steroid-converting enzymes in human ovarian carcinomas
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Estrone 3-Sulfate Mimics, Inhibitors of Estrone Sulfatase Activity: Homology Model Construction and Docking Studies
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Contribution of Estrone Sulfate to Cell Proliferation in Aromatase Inhibitor (AI) -Resistant, Hormone Receptor-Positive Breast Cancer
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Discovery of a sulfamate-based steroid sulfatase inhibitor with intrinsic selective estrogen receptor modulator properties
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A new series of aryl sulfamate derivatives: Design, synthesis, and biological evaluation
El-Gamal, M. I., Zaraei, S., Foster, P., Anbar, H. S., El‐Gamal, R., El‐Awady, R., & Potter, B. V. L. (2020) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2020.115406 · Cited by 22 · see citing works
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Enzyme histochemical patterns in human tumours—I. Hydrolytic enzymes in carcinoma of the colon and the breast
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Steroid Sulfatase Stimulates Intracrine Androgen Synthesis and is a Therapeutic Target for Advanced Prostate Cancer
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Preclinical pharmacokinetic, toxicological and biomarker evaluation of SR16157, a novel dual-acting steroid sulfatase inhibitor and selective estrogen receptor modulator
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Inhibition of dehydroepiandosterone sulfate action in androgen-sensitive tissues by EM-1913, an inhibitor of steroid sulfatase
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Recent progress in the development of steroid sulphatase inhibitors – examples of the novel and most promising compounds from the last decade
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Inhibitory effect of a novel non-steroidal aromatase inhibitor, YM511 on the proliferation of MCF-7 human breast cancer cell
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Induction of steroid sulfatase expression by tumor necrosis factor-α through phosphatidylinositol 3-kinase/Akt signaling pathway in PC-3 human prostate cancer cells
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In breast cancer subtypes steroid sulfatase (STS) is associated with less aggressive tumour characteristics
McNamara, K. M., Guestini, F., Sauer, T., Touma, J., Bukholm, I., Lindstrøm, J. C., Sasano, H., & Geisler, J. (2018) · British Journal of Cancer · doi:10.1038/s41416-018-0034-9 · Cited by 18 · see citing works
Association between the reproductive health of young women and cardiovascular disease in later life: umbrella review
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Steroid sulfatase inhibitor DU-14 protects spatial memory and synaptic plasticity from disruption by amyloid β protein in male rats
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Adrenal androgens rescue prostatic dihydrotestosterone production and growth of prostate cancer cells after castration
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Steroid sulfatase inhibiting lanostane triterpenes – Structure activity relationship and in silico insights
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Effects of estrogen receptor signaling on prostate cancer carcinogenesis
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A new molecular risk pathway for postpartum mood disorders: clues from steroid sulfatase–deficient individuals
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Synthesis and in vitro evaluation of piperazinyl-ureido sulfamates as steroid sulfatase inhibitors
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Recent Patents on New Steroid Agents Targeting the Steroidogenesis for Endocrine Cancer Treatments
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SULFATION PATHWAYS: Contribution of intracrine oestrogens to the aetiology of endometriosis
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The sulfatase pathway as estrogen supply in endometrial cancer
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COLON CANCER AND SEX
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The importance of sulfur-containing motifs in drug design and discovery
Mustafa, M., & Winum, J. (2022) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2022.2044783 · Cited by 257 · see citing works
An overview on Estrogen receptors signaling and its ligands in breast cancer
Khan, M. Z. I., Uzair, M., Nazli, A., & Chen, J. (2022) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2022.114658 · Cited by 82 · see citing works
Syntheses, reactivity, and biological applications of coumarins
Citarella, A., Vittorio, S., Dank, C., et al. (2024) · Frontiers in Chemistry · doi:10.3389/fchem.2024.1362992 · Cited by 73 · see citing works
“STS is overexpressed in breast cancer and its inhibition reduces estrogen formation, hindering tumor proliferation thus paving the way towards the development of anticancer agents (Foster, 2021).”
Background
Pharmacology of Natural Volatiles and Essential Oils in Food, Therapy, and Disease Prophylaxis
Sadgrove, N. J., Padilla-González, G. F., Leuner, O., Melnikovová, I., & Fernández-Cusimamani, E. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.740302 · Cited by 59 · see citing works
“Cancers express high levels of β-glucuronidase (Su et al., 2014) and steroid sulphatases (Foster, 2021).”
Background
Steroid Sulfation in Neurodegenerative Diseases
Vítků, J., Hill, M., Kolátorová, L., Havrdová, E., & Kancheva, R. L. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.839887 · Cited by 40 · see citing works
“Interestingly, the concept of inhibition of STS has been longer studied in the context of hormone dependent cancers (reviewed in (Foster, 2021)).”
Background
Gut Steroids and Microbiota: Effect of Gonadectomy and Sex
Diviccaro, S., FitzGerald, J. A., Cioffi, L., Falvo, E., Crispie, F., Cotter, P. D., O’Mahony, S. M., Giatti, S., Caruso, D., & Melcangi, R. C. (2022) · Biomolecules · doi:10.3390/biom12060767 · Cited by 28 · see citing works
“Accordingly, the gene expression of steroid sulfatase (STS) [66], the enzyme converting PREG sulphate into free PREG, was upregulated (Figure 2e), whereas that of hydroxysteroid sulfotransferase (SULT2B1a), the enzyme which catalyses the sulfation of PREG [66], was unchanged in control females vs. GDX females (Figure…”
BackgroundInfluential
Boron in cancer therapeutics: An overview
Kulkarni, S., Bhandary, D., Singh, Y., Monga, V., & Thareja, S. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108548 · Cited by 28 · see citing works
Targeting sex steroid biosynthesis for breast and prostate cancer therapy
POUTANEN, M. H., Thulin, M. H., & Härkönen, P. L. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00609-y · Cited by 28 · see citing works
Targeting the formation of estrogens for treatment of hormone dependent diseases–current status
Rižner, T. L., & Romano, A. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1155558 · Cited by 26 · see citing works
“Studies have also shown that inhibition of aromatase can increase the expression and activity of STS in breast cancer (Foster, 2021).”
Background
Structures and functions of human placental aromatase and steroid sulfatase, two key enzymes in estrogen biosynthesis
Ghosh, D. (2023) · Steroids · doi:10.1016/j.steroids.2023.109249 · Cited by 23 · see citing works
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Authors: Foster, P. A.
Affiliations: University of Birmingham (GB)
Corresponding author: Foster, Paul A.
ORCID: Foster, Paul A.
Venue: Molecules
Publisher: MDPI AG
Published: 2021-05-11
Volume: 26
Issue: 10
Pages: 2852
ISSN: 1420-3049 (ISSN-L)
DOI: 10.3390/molecules26102852
PMC: PMC8151039
OpenAlex: W3161445211
Semantic Scholar: 88830bc3f95edcb8e1fa00682e0bf68976992c4c
Cited by: 49
References: 155
Citations by year: 2026: 6 · 2025: 7 · 2024: 8 · 2023: 13 · 2022: 13 · 2021: 2
FWCI: 1.40
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Molecules (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Steroid Chemistry and Biochemistry
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Prostate Cancer Treatment and Research
Keywords: steroid sulphatase, hormone-dependent tumors, breast cancer, prostate cancer, endometrial cancer, colorectal cancer, ovarian cancer, endometriosis
MeSH terms: Drug Development, Animals, Clinical Trials as Topic, Enzyme Inhibitors, Humans, Steryl-Sulfatase, Biosynthetic Pathways

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Steroid sulphatase and its inhibitors: past, present, and future

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