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ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy

Chemoresistance is one of the major reasons leading to ovarian cancer high mortality and poor survival. Studies have shown that the alteration of cellular autophagy is associated with cancer cell chemoresistance. Here, we investigated whether the ovarian cancer chemoresistance is associated with the...

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Autores principales: Meng, Jiao, Liu, Kaiyi, Shao, Yang, Feng, Xu, Ji, Zhaodong, Chang, Bin, Wang, Yan, Xu, Ling, Yang, Gong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7033197/
https://www.ncbi.nlm.nih.gov/pubmed/32080166
http://dx.doi.org/10.1038/s41419-020-2327-1
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author Meng, Jiao
Liu, Kaiyi
Shao, Yang
Feng, Xu
Ji, Zhaodong
Chang, Bin
Wang, Yan
Xu, Ling
Yang, Gong
author_facet Meng, Jiao
Liu, Kaiyi
Shao, Yang
Feng, Xu
Ji, Zhaodong
Chang, Bin
Wang, Yan
Xu, Ling
Yang, Gong
author_sort Meng, Jiao
collection PubMed
description Chemoresistance is one of the major reasons leading to ovarian cancer high mortality and poor survival. Studies have shown that the alteration of cellular autophagy is associated with cancer cell chemoresistance. Here, we investigated whether the ovarian cancer chemoresistance is associated with the autophagy induced by the inhibitor of DNA binding 1 (ID1). By using gene overexpression or silencing, luciferase assay and human specimens, we show that ID1 induces high autophagy and confers cancer cell chemoresistance. The mechanistic study demonstrates that ID1 first activates the NF-κB signaling through facilitating the nuclear translocation of NF-κB p65, which strengthens the expression and secretion of IL-6 from cancer cells to subsequently activate the signal transducer and activator of transcription 3 (STAT3) through the protein phosphorylation at Y705. We further identified that STAT3 functions to promote the transcription of the activating transcription factor 6 (ATF6), which induces endoplasmic reticulum stress to promote cellular autophagy, granting cancer cell resistance to both cisplatin and paclitaxel treatment. Moreover, we found a significant correlation between the expression of ID1 and ATF6 in 1104 high grade serous ovarian cancer tissues, and that patients with the high expression of ID1 or ATF6 were resistant to platinum treatment and had the poor overall survival and progression-free survival. Thus, we have uncovered a mechanism in which ID1 confers cancer cell chemoresistance largely through the STAT3/ATF6-induced autophagy. The involved molecules, including ID1, STAT3, and ATF6, may have a potential to be targeted in combination with chemotherapeutic agents to improve ovarian cancer survival.
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spelling pubmed-70331972020-02-25 ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy Meng, Jiao Liu, Kaiyi Shao, Yang Feng, Xu Ji, Zhaodong Chang, Bin Wang, Yan Xu, Ling Yang, Gong Cell Death Dis Article Chemoresistance is one of the major reasons leading to ovarian cancer high mortality and poor survival. Studies have shown that the alteration of cellular autophagy is associated with cancer cell chemoresistance. Here, we investigated whether the ovarian cancer chemoresistance is associated with the autophagy induced by the inhibitor of DNA binding 1 (ID1). By using gene overexpression or silencing, luciferase assay and human specimens, we show that ID1 induces high autophagy and confers cancer cell chemoresistance. The mechanistic study demonstrates that ID1 first activates the NF-κB signaling through facilitating the nuclear translocation of NF-κB p65, which strengthens the expression and secretion of IL-6 from cancer cells to subsequently activate the signal transducer and activator of transcription 3 (STAT3) through the protein phosphorylation at Y705. We further identified that STAT3 functions to promote the transcription of the activating transcription factor 6 (ATF6), which induces endoplasmic reticulum stress to promote cellular autophagy, granting cancer cell resistance to both cisplatin and paclitaxel treatment. Moreover, we found a significant correlation between the expression of ID1 and ATF6 in 1104 high grade serous ovarian cancer tissues, and that patients with the high expression of ID1 or ATF6 were resistant to platinum treatment and had the poor overall survival and progression-free survival. Thus, we have uncovered a mechanism in which ID1 confers cancer cell chemoresistance largely through the STAT3/ATF6-induced autophagy. The involved molecules, including ID1, STAT3, and ATF6, may have a potential to be targeted in combination with chemotherapeutic agents to improve ovarian cancer survival. Nature Publishing Group UK 2020-02-20 /pmc/articles/PMC7033197/ /pubmed/32080166 http://dx.doi.org/10.1038/s41419-020-2327-1 Text en © The Author(s) 2020 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Meng, Jiao
Liu, Kaiyi
Shao, Yang
Feng, Xu
Ji, Zhaodong
Chang, Bin
Wang, Yan
Xu, Ling
Yang, Gong
ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
title ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
title_full ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
title_fullStr ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
title_full_unstemmed ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
title_short ID1 confers cancer cell chemoresistance through STAT3/ATF6-mediated induction of autophagy
title_sort id1 confers cancer cell chemoresistance through stat3/atf6-mediated induction of autophagy
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7033197/
https://www.ncbi.nlm.nih.gov/pubmed/32080166
http://dx.doi.org/10.1038/s41419-020-2327-1
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