Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer

Research output: Contribution to journalJournal articleResearchpeer-review

Standard

Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer. / Pippione, Agnese Chiara; Kovachka, Sandra; Vigato, Chiara; Bertarini, Laura; Mannella, Iole; Sainas, Stefano; Rolando, Barbara; Denasio, Enrica; Piercy-Mycock, Helen; Romalho, Linda; Salladini, Edoardo; Adinolfi, Salvatore; Zonari, Daniele; Peraldo-Neia, Caterina; Chiorino, Giovanna; Passoni, Alice; Mirza, Osman Asghar; Frydenvang, Karla; Pors, Klaus; Lolli, Marco Lucio; Spyrakis, Francesca; Oliaro-Bosso, Simonetta; Boschi, Donatella.

In: European Journal of Medicinal Chemistry, Vol. 268, 116193, 2024.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Pippione, AC, Kovachka, S, Vigato, C, Bertarini, L, Mannella, I, Sainas, S, Rolando, B, Denasio, E, Piercy-Mycock, H, Romalho, L, Salladini, E, Adinolfi, S, Zonari, D, Peraldo-Neia, C, Chiorino, G, Passoni, A, Mirza, OA, Frydenvang, K, Pors, K, Lolli, ML, Spyrakis, F, Oliaro-Bosso, S & Boschi, D 2024, 'Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer', European Journal of Medicinal Chemistry, vol. 268, 116193. https://doi.org/10.1016/j.ejmech.2024.116193

APA

Pippione, A. C., Kovachka, S., Vigato, C., Bertarini, L., Mannella, I., Sainas, S., Rolando, B., Denasio, E., Piercy-Mycock, H., Romalho, L., Salladini, E., Adinolfi, S., Zonari, D., Peraldo-Neia, C., Chiorino, G., Passoni, A., Mirza, O. A., Frydenvang, K., Pors, K., ... Boschi, D. (2024). Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer. European Journal of Medicinal Chemistry, 268, [116193]. https://doi.org/10.1016/j.ejmech.2024.116193

Vancouver

Pippione AC, Kovachka S, Vigato C, Bertarini L, Mannella I, Sainas S et al. Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer. European Journal of Medicinal Chemistry. 2024;268. 116193. https://doi.org/10.1016/j.ejmech.2024.116193

Author

Pippione, Agnese Chiara ; Kovachka, Sandra ; Vigato, Chiara ; Bertarini, Laura ; Mannella, Iole ; Sainas, Stefano ; Rolando, Barbara ; Denasio, Enrica ; Piercy-Mycock, Helen ; Romalho, Linda ; Salladini, Edoardo ; Adinolfi, Salvatore ; Zonari, Daniele ; Peraldo-Neia, Caterina ; Chiorino, Giovanna ; Passoni, Alice ; Mirza, Osman Asghar ; Frydenvang, Karla ; Pors, Klaus ; Lolli, Marco Lucio ; Spyrakis, Francesca ; Oliaro-Bosso, Simonetta ; Boschi, Donatella. / Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer. In: European Journal of Medicinal Chemistry. 2024 ; Vol. 268.

Bibtex

@article{04b758c2547a465ba86f7591208fe306,
title = "Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer",
abstract = "AKR1C3 is an enzyme that is overexpressed in several types of radiotherapy- and chemotherapy-resistant cancers. Despite AKR1C3 is a validated target for drug development, no inhibitor has been approved for clinical use. In this manuscript, we describe our study of a new series of potent AKR1C3-targeting 3-hydroxybenzoisoxazole based inhibitors that display high selectivity over the AKR1C2 isoform and low micromolar activity in inhibiting 22Rv1 prostate cancer cell proliferation. In silico studies suggested proper substituents to increase compound potency and provided with a mechanistic explanation that could clarify their different activity, later confirmed by X-ray crystallography. Both the in-silico studies and the crystallographic data highlight the importance of 90° rotation around the single bond of the biphenyl group, in ensuring that the inhibitor can adopt the optimal binding mode within the active pocket. The p-biphenyls that bear the meta-methoxy, and the ortho- and meta-trifluoromethyl substituents (in compounds 6a, 6e and 6f respectively) proved to be the best contributors to cellular potency as they provided the best IC50 values in series (2.3, 2.0 and 2.4 μM respectively) and showed no toxicity towards human MRC-5 cells. Co-treatment with scalar dilutions of either compound 6 or 6e and the clinically used drug abiraterone led to a significant reduction in cell proliferation, and thus confirmed that treatment with both CYP171A1-and AKR1C3-targeting compounds possess the potential to intervene in key steps in the steroidogenic pathway. Taken together, the novel compounds display desirable biochemical potency and cellular target inhibition as well as good in-vitro ADME properties, which highlight their potential for further preclinical studies.",
keywords = "AKR1C3 inhibitors, Benzoisoxazoles, Prostate cancer, X-ray crystallography",
author = "Pippione, {Agnese Chiara} and Sandra Kovachka and Chiara Vigato and Laura Bertarini and Iole Mannella and Stefano Sainas and Barbara Rolando and Enrica Denasio and Helen Piercy-Mycock and Linda Romalho and Edoardo Salladini and Salvatore Adinolfi and Daniele Zonari and Caterina Peraldo-Neia and Giovanna Chiorino and Alice Passoni and Mirza, {Osman Asghar} and Karla Frydenvang and Klaus Pors and Lolli, {Marco Lucio} and Francesca Spyrakis and Simonetta Oliaro-Bosso and Donatella Boschi",
note = "Publisher Copyright: {\textcopyright} 2024 The Authors",
year = "2024",
doi = "10.1016/j.ejmech.2024.116193",
language = "English",
volume = "268",
journal = "European Journal of Medicinal Chemistry",
issn = "0223-5234",
publisher = "Elsevier Masson",

}

RIS

TY - JOUR

T1 - Structure-guided optimization of 3-hydroxybenzoisoxazole derivatives as inhibitors of Aldo-keto reductase 1C3 (AKR1C3) to target prostate cancer

AU - Pippione, Agnese Chiara

AU - Kovachka, Sandra

AU - Vigato, Chiara

AU - Bertarini, Laura

AU - Mannella, Iole

AU - Sainas, Stefano

AU - Rolando, Barbara

AU - Denasio, Enrica

AU - Piercy-Mycock, Helen

AU - Romalho, Linda

AU - Salladini, Edoardo

AU - Adinolfi, Salvatore

AU - Zonari, Daniele

AU - Peraldo-Neia, Caterina

AU - Chiorino, Giovanna

AU - Passoni, Alice

AU - Mirza, Osman Asghar

AU - Frydenvang, Karla

AU - Pors, Klaus

AU - Lolli, Marco Lucio

AU - Spyrakis, Francesca

AU - Oliaro-Bosso, Simonetta

AU - Boschi, Donatella

N1 - Publisher Copyright: © 2024 The Authors

PY - 2024

Y1 - 2024

N2 - AKR1C3 is an enzyme that is overexpressed in several types of radiotherapy- and chemotherapy-resistant cancers. Despite AKR1C3 is a validated target for drug development, no inhibitor has been approved for clinical use. In this manuscript, we describe our study of a new series of potent AKR1C3-targeting 3-hydroxybenzoisoxazole based inhibitors that display high selectivity over the AKR1C2 isoform and low micromolar activity in inhibiting 22Rv1 prostate cancer cell proliferation. In silico studies suggested proper substituents to increase compound potency and provided with a mechanistic explanation that could clarify their different activity, later confirmed by X-ray crystallography. Both the in-silico studies and the crystallographic data highlight the importance of 90° rotation around the single bond of the biphenyl group, in ensuring that the inhibitor can adopt the optimal binding mode within the active pocket. The p-biphenyls that bear the meta-methoxy, and the ortho- and meta-trifluoromethyl substituents (in compounds 6a, 6e and 6f respectively) proved to be the best contributors to cellular potency as they provided the best IC50 values in series (2.3, 2.0 and 2.4 μM respectively) and showed no toxicity towards human MRC-5 cells. Co-treatment with scalar dilutions of either compound 6 or 6e and the clinically used drug abiraterone led to a significant reduction in cell proliferation, and thus confirmed that treatment with both CYP171A1-and AKR1C3-targeting compounds possess the potential to intervene in key steps in the steroidogenic pathway. Taken together, the novel compounds display desirable biochemical potency and cellular target inhibition as well as good in-vitro ADME properties, which highlight their potential for further preclinical studies.

AB - AKR1C3 is an enzyme that is overexpressed in several types of radiotherapy- and chemotherapy-resistant cancers. Despite AKR1C3 is a validated target for drug development, no inhibitor has been approved for clinical use. In this manuscript, we describe our study of a new series of potent AKR1C3-targeting 3-hydroxybenzoisoxazole based inhibitors that display high selectivity over the AKR1C2 isoform and low micromolar activity in inhibiting 22Rv1 prostate cancer cell proliferation. In silico studies suggested proper substituents to increase compound potency and provided with a mechanistic explanation that could clarify their different activity, later confirmed by X-ray crystallography. Both the in-silico studies and the crystallographic data highlight the importance of 90° rotation around the single bond of the biphenyl group, in ensuring that the inhibitor can adopt the optimal binding mode within the active pocket. The p-biphenyls that bear the meta-methoxy, and the ortho- and meta-trifluoromethyl substituents (in compounds 6a, 6e and 6f respectively) proved to be the best contributors to cellular potency as they provided the best IC50 values in series (2.3, 2.0 and 2.4 μM respectively) and showed no toxicity towards human MRC-5 cells. Co-treatment with scalar dilutions of either compound 6 or 6e and the clinically used drug abiraterone led to a significant reduction in cell proliferation, and thus confirmed that treatment with both CYP171A1-and AKR1C3-targeting compounds possess the potential to intervene in key steps in the steroidogenic pathway. Taken together, the novel compounds display desirable biochemical potency and cellular target inhibition as well as good in-vitro ADME properties, which highlight their potential for further preclinical studies.

KW - AKR1C3 inhibitors

KW - Benzoisoxazoles

KW - Prostate cancer

KW - X-ray crystallography

U2 - 10.1016/j.ejmech.2024.116193

DO - 10.1016/j.ejmech.2024.116193

M3 - Journal article

C2 - 38364714

VL - 268

JO - European Journal of Medicinal Chemistry

JF - European Journal of Medicinal Chemistry

SN - 0223-5234

M1 - 116193

ER -

ID: 384573411