Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis

The development of anticancer drugs to treat triple-negative breast cancer (TNBC) is an ongoing challenge. Immunogenic cell death (ICD) has garnered considerable interest worldwide as a promising synergistic modality for cancer chemoimmunotherapy. However, only few drugs or treatment modalities can...

Full description

Saved in:
Bibliographic Details
Main Authors: Yuan Lu, Shan-Shan Wang, Meng-Ya Li, Rong Liu, Meng-Fan Zhu, Liang-Mei Yang, Feng-Yang Wang, Ke-Bin Huang, Hong Liang
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Acta Pharmaceutica Sinica B
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S221138352400248X
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850196229730861056
author Yuan Lu
Shan-Shan Wang
Meng-Ya Li
Rong Liu
Meng-Fan Zhu
Liang-Mei Yang
Feng-Yang Wang
Ke-Bin Huang
Hong Liang
author_facet Yuan Lu
Shan-Shan Wang
Meng-Ya Li
Rong Liu
Meng-Fan Zhu
Liang-Mei Yang
Feng-Yang Wang
Ke-Bin Huang
Hong Liang
author_sort Yuan Lu
collection DOAJ
description The development of anticancer drugs to treat triple-negative breast cancer (TNBC) is an ongoing challenge. Immunogenic cell death (ICD) has garnered considerable interest worldwide as a promising synergistic modality for cancer chemoimmunotherapy. However, only few drugs or treatment modalities can trigger an ICD response and none of them exert a considerable clinical effect against TNBC. Therefore, new agents with potentially effective chemoimmunotherapeutic response are required. In this study, five new cyclometalated Ir(III) complexes containing isoquinoline alkaloid CˆN ligands were designed and synthesized. Among them, Ir-1 exhibited the highest in vitro cytotoxicity. Mechanistically, Ir-1 could trigger autophagy-dependent ferroptosis and a subsequent ferroptosis-dependent ICD response as well as indoleamine 2,3-dioxygenase (IDO) inhibition via reactive oxygen species (ROS)-mediated endoplasmic reticulum (ER) stress in MDA-MB-231 cells. When immunocompetent BALB/c mice were vaccinated with Ir-1-treated dying TNBC cells, antitumor CD8+ T-cell response and Foxp3+ T-cell depletion were induced, resulting in long-lasting antitumor immunity in TNBC cells. Moreover, combination therapy with Ir-1 and anti-PD1 could substantially augment in vivo therapeutic effects. Based on these results, Ir-1 is a promising candidate for chemoimmunotherapy against TNBC and its effects are mediated synergistically via ICD induction and IDO blockage.
format Article
id doaj-art-e029a03819d4425397d4b98b0602cfdd
institution OA Journals
issn 2211-3835
language English
publishDate 2025-01-01
publisher Elsevier
record_format Article
series Acta Pharmaceutica Sinica B
spelling doaj-art-e029a03819d4425397d4b98b0602cfdd2025-08-20T02:13:31ZengElsevierActa Pharmaceutica Sinica B2211-38352025-01-0115142443710.1016/j.apsb.2024.06.017Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosisYuan Lu0Shan-Shan Wang1Meng-Ya Li2Rong Liu3Meng-Fan Zhu4Liang-Mei Yang5Feng-Yang Wang6Ke-Bin Huang7Hong Liang8State Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, China; Department of Pharmacy, School of Medicine, Guangxi University of Science and Technology, Liuzhou 545005, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, ChinaState Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, China; Corresponding authors.State Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources (Ministry of Education of China), Collaborative Innovation Center for Guangxi Ethnic Medicine, School of Chemistry and Pharmaceutical Sciences, Guangxi Normal University, Guilin 541004, China; Corresponding authors.The development of anticancer drugs to treat triple-negative breast cancer (TNBC) is an ongoing challenge. Immunogenic cell death (ICD) has garnered considerable interest worldwide as a promising synergistic modality for cancer chemoimmunotherapy. However, only few drugs or treatment modalities can trigger an ICD response and none of them exert a considerable clinical effect against TNBC. Therefore, new agents with potentially effective chemoimmunotherapeutic response are required. In this study, five new cyclometalated Ir(III) complexes containing isoquinoline alkaloid CˆN ligands were designed and synthesized. Among them, Ir-1 exhibited the highest in vitro cytotoxicity. Mechanistically, Ir-1 could trigger autophagy-dependent ferroptosis and a subsequent ferroptosis-dependent ICD response as well as indoleamine 2,3-dioxygenase (IDO) inhibition via reactive oxygen species (ROS)-mediated endoplasmic reticulum (ER) stress in MDA-MB-231 cells. When immunocompetent BALB/c mice were vaccinated with Ir-1-treated dying TNBC cells, antitumor CD8+ T-cell response and Foxp3+ T-cell depletion were induced, resulting in long-lasting antitumor immunity in TNBC cells. Moreover, combination therapy with Ir-1 and anti-PD1 could substantially augment in vivo therapeutic effects. Based on these results, Ir-1 is a promising candidate for chemoimmunotherapy against TNBC and its effects are mediated synergistically via ICD induction and IDO blockage.http://www.sciencedirect.com/science/article/pii/S221138352400248XOrganometallic complexCyclometalated iridium complexIsoquinoline alkaloidER stressAutophagy-dependent ferroptosisImmunogenic cell death
spellingShingle Yuan Lu
Shan-Shan Wang
Meng-Ya Li
Rong Liu
Meng-Fan Zhu
Liang-Mei Yang
Feng-Yang Wang
Ke-Bin Huang
Hong Liang
Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis
Acta Pharmaceutica Sinica B
Organometallic complex
Cyclometalated iridium complex
Isoquinoline alkaloid
ER stress
Autophagy-dependent ferroptosis
Immunogenic cell death
title Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis
title_full Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis
title_fullStr Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis
title_full_unstemmed Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis
title_short Cyclometalated iridium(III) complex based on isoquinoline alkaloid synergistically elicits the ICD response and IDO inhibition via autophagy-dependent ferroptosis
title_sort cyclometalated iridium iii complex based on isoquinoline alkaloid synergistically elicits the icd response and ido inhibition via autophagy dependent ferroptosis
topic Organometallic complex
Cyclometalated iridium complex
Isoquinoline alkaloid
ER stress
Autophagy-dependent ferroptosis
Immunogenic cell death
url http://www.sciencedirect.com/science/article/pii/S221138352400248X
work_keys_str_mv AT yuanlu cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT shanshanwang cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT mengyali cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT rongliu cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT mengfanzhu cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT liangmeiyang cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT fengyangwang cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT kebinhuang cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis
AT hongliang cyclometalatediridiumiiicomplexbasedonisoquinolinealkaloidsynergisticallyelicitstheicdresponseandidoinhibitionviaautophagydependentferroptosis