Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity

Abstract G-quadruplex (G4) is a noncanonical DNA secondary structure known to induce DNA damage and regulate the expression of immune-related genes. We aim to exploit the G4 folding as a treatment strategy to trigger anti-tumor immune response. In this study, we observe that the abundant genomic G4...

Full description

Saved in:
Bibliographic Details
Main Authors: Peisi Li, Dawang Zhou, Yumo Xie, Ze Yuan, Mingzhe Huang, Gaopo Xu, Junfeng Huang, Zhuokai Zhuang, Yanxin Luo, Huichuan Yu, Xiaolin Wang
Format: Article
Language:English
Published: Nature Publishing Group 2024-11-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-024-07215-2
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846164834454863872
author Peisi Li
Dawang Zhou
Yumo Xie
Ze Yuan
Mingzhe Huang
Gaopo Xu
Junfeng Huang
Zhuokai Zhuang
Yanxin Luo
Huichuan Yu
Xiaolin Wang
author_facet Peisi Li
Dawang Zhou
Yumo Xie
Ze Yuan
Mingzhe Huang
Gaopo Xu
Junfeng Huang
Zhuokai Zhuang
Yanxin Luo
Huichuan Yu
Xiaolin Wang
author_sort Peisi Li
collection DOAJ
description Abstract G-quadruplex (G4) is a noncanonical DNA secondary structure known to induce DNA damage and regulate the expression of immune-related genes. We aim to exploit the G4 folding as a treatment strategy to trigger anti-tumor immune response. In this study, we observe that the abundant genomic G4 in epithelial cells coexists with increased infiltration of CD8+ T cells in colorectal cancer tissue. Furthermore, our data substantiate the inhibitory effect of the G4 ligand TMPyP4 on cancer progression while concurrently stimulating anti-tumor immunity. Mechanistically, TMPyP4 impedes cancer cell proliferation and induces G2/M cell cycle arrest. Additionally, in vivo experiments demonstrate that TMPyP4 enhances the anti-tumor immune response by triggering DNA damage and activating the cGAS-STING pathway, which fosters CD8+ T cell activation and dendritic cell maturation. Importantly, the combined treatment of TMPyP4 and anti-PD1 exhibits a synergistic therapeutic effect on colorectal cancer. In summary, our findings underscore the potential of the G4 ligand TMPyP4 as a dual strategy to target colorectal cancer: inhibiting cancer progression and augmenting anti-tumor immunity through the activation of cGAS-STING pathway.
format Article
id doaj-art-b53b6fc60c694b14991ff661020377d0
institution Kabale University
issn 2041-4889
language English
publishDate 2024-11-01
publisher Nature Publishing Group
record_format Article
series Cell Death and Disease
spelling doaj-art-b53b6fc60c694b14991ff661020377d02024-11-17T12:50:58ZengNature Publishing GroupCell Death and Disease2041-48892024-11-01151111010.1038/s41419-024-07215-2Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunityPeisi Li0Dawang Zhou1Yumo Xie2Ze Yuan3Mingzhe Huang4Gaopo Xu5Junfeng Huang6Zhuokai Zhuang7Yanxin Luo8Huichuan Yu9Xiaolin Wang10Guangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityDepartment of Hepatobiliary and Pancreatic Surgery, Sun Yat-Sen University Cancer CenterGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityGuangdong Institute of Gastroenterology, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Disease, The Sixth Affiliated Hospital, Sun Yat-sen UniversityAbstract G-quadruplex (G4) is a noncanonical DNA secondary structure known to induce DNA damage and regulate the expression of immune-related genes. We aim to exploit the G4 folding as a treatment strategy to trigger anti-tumor immune response. In this study, we observe that the abundant genomic G4 in epithelial cells coexists with increased infiltration of CD8+ T cells in colorectal cancer tissue. Furthermore, our data substantiate the inhibitory effect of the G4 ligand TMPyP4 on cancer progression while concurrently stimulating anti-tumor immunity. Mechanistically, TMPyP4 impedes cancer cell proliferation and induces G2/M cell cycle arrest. Additionally, in vivo experiments demonstrate that TMPyP4 enhances the anti-tumor immune response by triggering DNA damage and activating the cGAS-STING pathway, which fosters CD8+ T cell activation and dendritic cell maturation. Importantly, the combined treatment of TMPyP4 and anti-PD1 exhibits a synergistic therapeutic effect on colorectal cancer. In summary, our findings underscore the potential of the G4 ligand TMPyP4 as a dual strategy to target colorectal cancer: inhibiting cancer progression and augmenting anti-tumor immunity through the activation of cGAS-STING pathway.https://doi.org/10.1038/s41419-024-07215-2
spellingShingle Peisi Li
Dawang Zhou
Yumo Xie
Ze Yuan
Mingzhe Huang
Gaopo Xu
Junfeng Huang
Zhuokai Zhuang
Yanxin Luo
Huichuan Yu
Xiaolin Wang
Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity
Cell Death and Disease
title Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity
title_full Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity
title_fullStr Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity
title_full_unstemmed Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity
title_short Targeting G-quadruplex by TMPyP4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti-tumor immunity
title_sort targeting g quadruplex by tmpyp4 for inhibition of colorectal cancer through cell cycle arrest and boosting anti tumor immunity
url https://doi.org/10.1038/s41419-024-07215-2
work_keys_str_mv AT peisili targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT dawangzhou targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT yumoxie targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT zeyuan targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT mingzhehuang targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT gaopoxu targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT junfenghuang targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT zhuokaizhuang targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT yanxinluo targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT huichuanyu targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity
AT xiaolinwang targetinggquadruplexbytmpyp4forinhibitionofcolorectalcancerthroughcellcyclearrestandboostingantitumorimmunity