AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer

Oxaliplatin (OXA), a platinum-based chemotherapeutic agent, remains a mainstay in first-line treatments for advanced colorectal cancer (CRC). However, the eventual development of OXA resistance represents a significant clinical challenge. In the present study, we demonstrate that the aldo-keto reduc...

Full description

Saved in:
Bibliographic Details
Main Authors: Zhiwen Fu, Tingting Wu, Chen Gao, Lulu Wang, Yu Zhang, Chen Shi
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Acta Pharmaceutica Sinica B
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211383524003502
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850114147004448768
author Zhiwen Fu
Tingting Wu
Chen Gao
Lulu Wang
Yu Zhang
Chen Shi
author_facet Zhiwen Fu
Tingting Wu
Chen Gao
Lulu Wang
Yu Zhang
Chen Shi
author_sort Zhiwen Fu
collection DOAJ
description Oxaliplatin (OXA), a platinum-based chemotherapeutic agent, remains a mainstay in first-line treatments for advanced colorectal cancer (CRC). However, the eventual development of OXA resistance represents a significant clinical challenge. In the present study, we demonstrate that the aldo-keto reductase 1C1 (AKR1C1) is overexpressed in CRC cells upon acquisition of OXA resistance, evident in OXA-resistant CRC cell lines. We employed genetic silencing and pharmacological inhibition strategies to establish that suppression of AKR1C1 restores OXA sensitivity. Mechanistically, AKR1C1 interacts with and activates the transcription factor STAT3, which upregulates the glutamate transporter EAAT3, thereby elevating intracellular glutathione levels and conferring OXA resistance. Alantolactone, a potent natural product inhibitor of AKR1C1, effectively reverses this chemoresistance, restricting the growth of OXA-resistant CRC cells both in vitro and in vivo. Our findings uncover a critical AKR1C1-dependent mechanism behind OXA resistance and propose a promising combinatorial therapeutic strategy to overcome this resistance in CRC.
format Article
id doaj-art-df21e663c5bd4ff2b145db294059c737
institution OA Journals
issn 2211-3835
language English
publishDate 2024-12-01
publisher Elsevier
record_format Article
series Acta Pharmaceutica Sinica B
spelling doaj-art-df21e663c5bd4ff2b145db294059c7372025-08-20T02:36:58ZengElsevierActa Pharmaceutica Sinica B2211-38352024-12-0114125305532010.1016/j.apsb.2024.08.031AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancerZhiwen Fu0Tingting Wu1Chen Gao2Lulu Wang3Yu Zhang4Chen Shi5Department of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China; Hubei Province Clinical Research Center for Precision Medicine for Critical Illness, Wuhan 430022, ChinaDepartment of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China; Hubei Province Clinical Research Center for Precision Medicine for Critical Illness, Wuhan 430022, ChinaDepartment of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China; Hubei Province Clinical Research Center for Precision Medicine for Critical Illness, Wuhan 430022, ChinaDepartment of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China; Hubei Province Clinical Research Center for Precision Medicine for Critical Illness, Wuhan 430022, ChinaDepartment of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China; Hubei Province Clinical Research Center for Precision Medicine for Critical Illness, Wuhan 430022, ChinaDepartment of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China; Hubei Province Clinical Research Center for Precision Medicine for Critical Illness, Wuhan 430022, China; Corresponding author.Oxaliplatin (OXA), a platinum-based chemotherapeutic agent, remains a mainstay in first-line treatments for advanced colorectal cancer (CRC). However, the eventual development of OXA resistance represents a significant clinical challenge. In the present study, we demonstrate that the aldo-keto reductase 1C1 (AKR1C1) is overexpressed in CRC cells upon acquisition of OXA resistance, evident in OXA-resistant CRC cell lines. We employed genetic silencing and pharmacological inhibition strategies to establish that suppression of AKR1C1 restores OXA sensitivity. Mechanistically, AKR1C1 interacts with and activates the transcription factor STAT3, which upregulates the glutamate transporter EAAT3, thereby elevating intracellular glutathione levels and conferring OXA resistance. Alantolactone, a potent natural product inhibitor of AKR1C1, effectively reverses this chemoresistance, restricting the growth of OXA-resistant CRC cells both in vitro and in vivo. Our findings uncover a critical AKR1C1-dependent mechanism behind OXA resistance and propose a promising combinatorial therapeutic strategy to overcome this resistance in CRC.http://www.sciencedirect.com/science/article/pii/S2211383524003502Oxaliplatin resistanceAKR1C1Colorectal cancerAlantolactoneGlutathioneCombination therapy
spellingShingle Zhiwen Fu
Tingting Wu
Chen Gao
Lulu Wang
Yu Zhang
Chen Shi
AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
Acta Pharmaceutica Sinica B
Oxaliplatin resistance
AKR1C1
Colorectal cancer
Alantolactone
Glutathione
Combination therapy
title AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
title_full AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
title_fullStr AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
title_full_unstemmed AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
title_short AKR1C1 interacts with STAT3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
title_sort akr1c1 interacts with stat3 to increase intracellular glutathione and confers resistance to oxaliplatin in colorectal cancer
topic Oxaliplatin resistance
AKR1C1
Colorectal cancer
Alantolactone
Glutathione
Combination therapy
url http://www.sciencedirect.com/science/article/pii/S2211383524003502
work_keys_str_mv AT zhiwenfu akr1c1interactswithstat3toincreaseintracellularglutathioneandconfersresistancetooxaliplatinincolorectalcancer
AT tingtingwu akr1c1interactswithstat3toincreaseintracellularglutathioneandconfersresistancetooxaliplatinincolorectalcancer
AT chengao akr1c1interactswithstat3toincreaseintracellularglutathioneandconfersresistancetooxaliplatinincolorectalcancer
AT luluwang akr1c1interactswithstat3toincreaseintracellularglutathioneandconfersresistancetooxaliplatinincolorectalcancer
AT yuzhang akr1c1interactswithstat3toincreaseintracellularglutathioneandconfersresistancetooxaliplatinincolorectalcancer
AT chenshi akr1c1interactswithstat3toincreaseintracellularglutathioneandconfersresistancetooxaliplatinincolorectalcancer