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Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1

Agonists of glucocorticoid receptor (GR) are frequently given to cancer patients with platinum-containing chemotherapy to reduce inflammation, but how GR influences tumor growth in response to platinum-based chemotherapy such as cisplatin through inflammation-independent signaling remains largely un...

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Autores principales: Pan, Chaoyun, Kang, JiHoon, Hwang, Jung Seok, Li, Jie, Boese, Austin C., Wang, Xu, Yang, Likun, Boggon, Titus J., Chen, Georgia Z., Saba, Nabil F., Shin, Dong M., Magliocca, Kelly R., Jin, Lingtao, Kang, Sumin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8368102/
https://www.ncbi.nlm.nih.gov/pubmed/34400618
http://dx.doi.org/10.1038/s41467-021-24845-8
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author Pan, Chaoyun
Kang, JiHoon
Hwang, Jung Seok
Li, Jie
Boese, Austin C.
Wang, Xu
Yang, Likun
Boggon, Titus J.
Chen, Georgia Z.
Saba, Nabil F.
Shin, Dong M.
Magliocca, Kelly R.
Jin, Lingtao
Kang, Sumin
author_facet Pan, Chaoyun
Kang, JiHoon
Hwang, Jung Seok
Li, Jie
Boese, Austin C.
Wang, Xu
Yang, Likun
Boggon, Titus J.
Chen, Georgia Z.
Saba, Nabil F.
Shin, Dong M.
Magliocca, Kelly R.
Jin, Lingtao
Kang, Sumin
author_sort Pan, Chaoyun
collection PubMed
description Agonists of glucocorticoid receptor (GR) are frequently given to cancer patients with platinum-containing chemotherapy to reduce inflammation, but how GR influences tumor growth in response to platinum-based chemotherapy such as cisplatin through inflammation-independent signaling remains largely unclear. Combined genomics and transcription factor profiling reveal that MAST1, a critical platinum resistance factor that reprograms the MAPK pathway, is upregulated upon cisplatin exposure through activated transcription factor GR. Mechanistically, cisplatin binds to C622 in GR and recruits GR to the nucleus for its activation, which induces MAST1 expression and consequently reactivates MEK signaling. GR nuclear translocation and MAST1 upregulation coordinately occur in patient tumors collected after platinum treatment, and align with patient treatment resistance. Co-treatment with dexamethasone and cisplatin restores cisplatin-resistant tumor growth, whereas addition of the MAST1 inhibitor lestaurtinib abrogates tumor growth while preserving the inhibitory effect of dexamethasone on inflammation in vivo. These findings not only provide insights into the underlying mechanism of GR in cisplatin resistance but also offer an effective alternative therapeutic strategy to improve the clinical outcome of patients receiving platinum-based chemotherapy with GR agonists.
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spelling pubmed-83681022021-09-02 Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1 Pan, Chaoyun Kang, JiHoon Hwang, Jung Seok Li, Jie Boese, Austin C. Wang, Xu Yang, Likun Boggon, Titus J. Chen, Georgia Z. Saba, Nabil F. Shin, Dong M. Magliocca, Kelly R. Jin, Lingtao Kang, Sumin Nat Commun Article Agonists of glucocorticoid receptor (GR) are frequently given to cancer patients with platinum-containing chemotherapy to reduce inflammation, but how GR influences tumor growth in response to platinum-based chemotherapy such as cisplatin through inflammation-independent signaling remains largely unclear. Combined genomics and transcription factor profiling reveal that MAST1, a critical platinum resistance factor that reprograms the MAPK pathway, is upregulated upon cisplatin exposure through activated transcription factor GR. Mechanistically, cisplatin binds to C622 in GR and recruits GR to the nucleus for its activation, which induces MAST1 expression and consequently reactivates MEK signaling. GR nuclear translocation and MAST1 upregulation coordinately occur in patient tumors collected after platinum treatment, and align with patient treatment resistance. Co-treatment with dexamethasone and cisplatin restores cisplatin-resistant tumor growth, whereas addition of the MAST1 inhibitor lestaurtinib abrogates tumor growth while preserving the inhibitory effect of dexamethasone on inflammation in vivo. These findings not only provide insights into the underlying mechanism of GR in cisplatin resistance but also offer an effective alternative therapeutic strategy to improve the clinical outcome of patients receiving platinum-based chemotherapy with GR agonists. Nature Publishing Group UK 2021-08-16 /pmc/articles/PMC8368102/ /pubmed/34400618 http://dx.doi.org/10.1038/s41467-021-24845-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Pan, Chaoyun
Kang, JiHoon
Hwang, Jung Seok
Li, Jie
Boese, Austin C.
Wang, Xu
Yang, Likun
Boggon, Titus J.
Chen, Georgia Z.
Saba, Nabil F.
Shin, Dong M.
Magliocca, Kelly R.
Jin, Lingtao
Kang, Sumin
Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1
title Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1
title_full Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1
title_fullStr Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1
title_full_unstemmed Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1
title_short Cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via MAST1
title_sort cisplatin-mediated activation of glucocorticoid receptor induces platinum resistance via mast1
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8368102/
https://www.ncbi.nlm.nih.gov/pubmed/34400618
http://dx.doi.org/10.1038/s41467-021-24845-8
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