AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer

Abstract Cancer cells can be induced to dormancy initially by specific cancer therapies, but can be reactivated for subsequent relapse as therapy-resistant cancer cells. Although the treatment-induced dormancy-to-reactivation switch is an important process in tumour spread and recurrence, little is...

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Main Authors: Sangsang Li, Yifan Zhang, Maoxing Luo, Weiwei Zhou, Yitong Chen, Dinglan Wu, Qiang Wei, Yan Chang, Hailiang Hu
Format: Article
Language:English
Published: Nature Publishing Group 2025-08-01
Series:Cell Discovery
Online Access:https://doi.org/10.1038/s41421-025-00817-w
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author Sangsang Li
Yifan Zhang
Maoxing Luo
Weiwei Zhou
Yitong Chen
Dinglan Wu
Qiang Wei
Yan Chang
Hailiang Hu
author_facet Sangsang Li
Yifan Zhang
Maoxing Luo
Weiwei Zhou
Yitong Chen
Dinglan Wu
Qiang Wei
Yan Chang
Hailiang Hu
author_sort Sangsang Li
collection DOAJ
description Abstract Cancer cells can be induced to dormancy initially by specific cancer therapies, but can be reactivated for subsequent relapse as therapy-resistant cancer cells. Although the treatment-induced dormancy-to-reactivation switch is an important process in tumour spread and recurrence, little is known about the underlying molecular mechanisms, particularly the metabolic underpinnings. In this study, we demonstrated that the tryptophan catabolism-related tryptophan 2,3-dioxygenase (TDO2) -kynurenine (Kyn) -aryl hydrocarbon receptor (AhR) signalling axis was responsible for both sustaining the survival of dormant prostate cancer cells induced by androgen deprivation therapy (ADT) and promoting the reactivation of dormant cells and their recurrent outgrowth, which facilitated the development of therapeutic resistance by allowing the dormancy-to-reactivation switch. Mechanistically, we found that ADT upregulated the expression of TDO2 to produce Kyn, which activated AhR and maintained the survival of ADT-induced dormant cells. Interestingly, the switch of transcription factors from the androgen receptor (AR) to the glucocorticoid receptor (GR) modulated the persistent expression of TDO2 and promoted the reactivation of dormant cells through the same TDO2-Kyn-AhR signalling axis. Additionally, tumour recurrence following ADT was delayed by pharmacological suppression of TDO2-Kyn-AhR signalling with a TDO2 inhibitor or an AhR inhibitor. In summary, we describe a signalling circuit mediated by tryptophan metabolism for regulating tumour cell dormancy and recurrence and propose TDO2 as a new target for the treatment of androgen-sensitive prostate cancer patients in combination with ADT.
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spelling doaj-art-24eaf36d405a4ba48d36c3cc18723ca52025-08-20T03:45:45ZengNature Publishing GroupCell Discovery2056-59682025-08-0111111610.1038/s41421-025-00817-wAR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancerSangsang Li0Yifan Zhang1Maoxing Luo2Weiwei Zhou3Yitong Chen4Dinglan Wu5Qiang Wei6Yan Chang7Hailiang Hu8Department of Biochemistry, SUSTech Homeostatic Medicine Institute, School of Medicine, Southern University of Science and TechnologyDepartment of Biochemistry, SUSTech Homeostatic Medicine Institute, School of Medicine, Southern University of Science and TechnologyDepartment of Biochemistry, SUSTech Homeostatic Medicine Institute, School of Medicine, Southern University of Science and TechnologyDepartment of Biochemistry, SUSTech Homeostatic Medicine Institute, School of Medicine, Southern University of Science and TechnologyDepartment of Biochemistry, SUSTech Homeostatic Medicine Institute, School of Medicine, Southern University of Science and TechnologyShenzhen Key Laboratory of Viral Oncology, Clinical Innovation and Research Center (CIRC), Shenzhen Hospital of Southern Medical UniversityDepartment of Urology, Nanfang Hospital, Southern Medical UniversityInstitute of Clinical Pharmacology, Anhui Medical University, Key Laboratory of Anti-Inflammatory and Immune Medicine, Ministry of EducationDepartment of Biochemistry, SUSTech Homeostatic Medicine Institute, School of Medicine, Southern University of Science and TechnologyAbstract Cancer cells can be induced to dormancy initially by specific cancer therapies, but can be reactivated for subsequent relapse as therapy-resistant cancer cells. Although the treatment-induced dormancy-to-reactivation switch is an important process in tumour spread and recurrence, little is known about the underlying molecular mechanisms, particularly the metabolic underpinnings. In this study, we demonstrated that the tryptophan catabolism-related tryptophan 2,3-dioxygenase (TDO2) -kynurenine (Kyn) -aryl hydrocarbon receptor (AhR) signalling axis was responsible for both sustaining the survival of dormant prostate cancer cells induced by androgen deprivation therapy (ADT) and promoting the reactivation of dormant cells and their recurrent outgrowth, which facilitated the development of therapeutic resistance by allowing the dormancy-to-reactivation switch. Mechanistically, we found that ADT upregulated the expression of TDO2 to produce Kyn, which activated AhR and maintained the survival of ADT-induced dormant cells. Interestingly, the switch of transcription factors from the androgen receptor (AR) to the glucocorticoid receptor (GR) modulated the persistent expression of TDO2 and promoted the reactivation of dormant cells through the same TDO2-Kyn-AhR signalling axis. Additionally, tumour recurrence following ADT was delayed by pharmacological suppression of TDO2-Kyn-AhR signalling with a TDO2 inhibitor or an AhR inhibitor. In summary, we describe a signalling circuit mediated by tryptophan metabolism for regulating tumour cell dormancy and recurrence and propose TDO2 as a new target for the treatment of androgen-sensitive prostate cancer patients in combination with ADT.https://doi.org/10.1038/s41421-025-00817-w
spellingShingle Sangsang Li
Yifan Zhang
Maoxing Luo
Weiwei Zhou
Yitong Chen
Dinglan Wu
Qiang Wei
Yan Chang
Hailiang Hu
AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer
Cell Discovery
title AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer
title_full AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer
title_fullStr AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer
title_full_unstemmed AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer
title_short AR to GR switch modulates differential TDO2-Kyn-AhR signalling to promote the survival and recurrence of treatment-induced dormant cells in prostate cancer
title_sort ar to gr switch modulates differential tdo2 kyn ahr signalling to promote the survival and recurrence of treatment induced dormant cells in prostate cancer
url https://doi.org/10.1038/s41421-025-00817-w
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