RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity

Background Natural killer (NK) cells are recognized for their ability to kill tumor cells for tumor control, but tumor cells often develop resistance to evade NK cell-mediated cytotoxicity. Identification of molecular mechanisms by which tumor cells evade from NK cell-mediated killing may offer nove...

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Main Authors: Lin Li, Hui Guo, Jie Hu, Lei Cui, Zining Wang, Feifei Xu, Xiaojuan Wang, Huanling Zhang, Chunyuan Xie, Yongxiang Liu, Xiaojun Xia, Zixuan Guo, Heping Li, Tiantian Wang, Ruhui Yao, Huan Jin, Yanxun Lin
Format: Article
Language:English
Published: BMJ Publishing Group 2025-05-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/13/5/e010931.full
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author Lin Li
Hui Guo
Jie Hu
Lei Cui
Zining Wang
Feifei Xu
Xiaojuan Wang
Huanling Zhang
Chunyuan Xie
Yongxiang Liu
Xiaojun Xia
Zixuan Guo
Heping Li
Tiantian Wang
Ruhui Yao
Huan Jin
Yanxun Lin
author_facet Lin Li
Hui Guo
Jie Hu
Lei Cui
Zining Wang
Feifei Xu
Xiaojuan Wang
Huanling Zhang
Chunyuan Xie
Yongxiang Liu
Xiaojun Xia
Zixuan Guo
Heping Li
Tiantian Wang
Ruhui Yao
Huan Jin
Yanxun Lin
author_sort Lin Li
collection DOAJ
description Background Natural killer (NK) cells are recognized for their ability to kill tumor cells for tumor control, but tumor cells often develop resistance to evade NK cell-mediated cytotoxicity. Identification of molecular mechanisms by which tumor cells evade from NK cell-mediated killing may offer novel therapeutic strategies for potentiating NK-based cancer immunotherapy.Methods An in vitro tumor-NK cell co-culture system was employed to identify the most significantly altered genes in tumor cells following NK cell interaction. The cell death rate of tumor cells by NK cell exposure was quantified using flow cytometry. EL4 and HCT116 tumor models in C57BL/6, BALB/c-nu, and NOD/SCID mice were used for evaluating tumor growth differences induced by Rac2 knockdown or knockout. The cellular and molecular impact of Rac2 knockdown or knockout on the sensitivity of tumor cells to NK cell-mediated cytotoxicity was assessed using quantitative PCR, immunofluorescence, and mutation analysis.Results By screening expression levels of the Ras homology (Rho) GTPase family genes in tumor cells after co-culture with NK cells, we identified RAC2 as a key regulator of tumor cell resistance to NK cell-mediated cytotoxicity among the Rho GTPase family members. Furthermore, knockout of RAC2 in human colorectal cancer cells leads to increased tumor susceptibility to NK cell-mediated cytotoxicity in a xenograft tumor model. Mechanistically, the absence of RAC2 enhances tumor cell sensitivity to NK cell-mediated killing by facilitating cell–cell contact.Conclusions These findings indicate that the inhibition of RAC2 in tumor cells substantially enhances their susceptibility to NK cell-mediated cytotoxicity, thereby providing a potential therapeutic target for optimizing NK cell therapy.
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institution Kabale University
issn 2051-1426
language English
publishDate 2025-05-01
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series Journal for ImmunoTherapy of Cancer
spelling doaj-art-bd85d757449c42ce94f0aa95d186c0602025-08-20T03:48:31ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262025-05-0113510.1136/jitc-2024-010931RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicityLin Li0Hui Guo1Jie Hu2Lei Cui3Zining Wang4Feifei Xu5Xiaojuan Wang6Huanling Zhang7Chunyuan Xie8Yongxiang Liu9Xiaojun Xia10Zixuan Guo11Heping Li12Tiantian Wang13Ruhui Yao14Huan Jin15Yanxun Lin161 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China2 Department of Medical Oncology, The First Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China3 Department of Oncology, Third Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China4 Guangzhou National Laboratory, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China4 Guangzhou National Laboratory, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China5 Department of Medical Oncology, Sun Yat-Sen Memorial Hospital, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, China1 Department of Experiment Medicine, Sun Yat-sen University Cancer Center, Guangzhou, Guangdong, ChinaBackground Natural killer (NK) cells are recognized for their ability to kill tumor cells for tumor control, but tumor cells often develop resistance to evade NK cell-mediated cytotoxicity. Identification of molecular mechanisms by which tumor cells evade from NK cell-mediated killing may offer novel therapeutic strategies for potentiating NK-based cancer immunotherapy.Methods An in vitro tumor-NK cell co-culture system was employed to identify the most significantly altered genes in tumor cells following NK cell interaction. The cell death rate of tumor cells by NK cell exposure was quantified using flow cytometry. EL4 and HCT116 tumor models in C57BL/6, BALB/c-nu, and NOD/SCID mice were used for evaluating tumor growth differences induced by Rac2 knockdown or knockout. The cellular and molecular impact of Rac2 knockdown or knockout on the sensitivity of tumor cells to NK cell-mediated cytotoxicity was assessed using quantitative PCR, immunofluorescence, and mutation analysis.Results By screening expression levels of the Ras homology (Rho) GTPase family genes in tumor cells after co-culture with NK cells, we identified RAC2 as a key regulator of tumor cell resistance to NK cell-mediated cytotoxicity among the Rho GTPase family members. Furthermore, knockout of RAC2 in human colorectal cancer cells leads to increased tumor susceptibility to NK cell-mediated cytotoxicity in a xenograft tumor model. Mechanistically, the absence of RAC2 enhances tumor cell sensitivity to NK cell-mediated killing by facilitating cell–cell contact.Conclusions These findings indicate that the inhibition of RAC2 in tumor cells substantially enhances their susceptibility to NK cell-mediated cytotoxicity, thereby providing a potential therapeutic target for optimizing NK cell therapy.https://jitc.bmj.com/content/13/5/e010931.full
spellingShingle Lin Li
Hui Guo
Jie Hu
Lei Cui
Zining Wang
Feifei Xu
Xiaojuan Wang
Huanling Zhang
Chunyuan Xie
Yongxiang Liu
Xiaojun Xia
Zixuan Guo
Heping Li
Tiantian Wang
Ruhui Yao
Huan Jin
Yanxun Lin
RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity
Journal for ImmunoTherapy of Cancer
title RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity
title_full RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity
title_fullStr RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity
title_full_unstemmed RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity
title_short RAC2 inhibition enhances tumor sensitivity to NK cell-mediated cytotoxicity
title_sort rac2 inhibition enhances tumor sensitivity to nk cell mediated cytotoxicity
url https://jitc.bmj.com/content/13/5/e010931.full
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