Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3

Abstract The interaction between tumor-derived exosomes and stroma plays a crucial role in tumor progression. However, the mechanisms through which tumor cells influence stromal changes are not yet fully understood. In our study, through single-cell sequencing analysis of clear cell renal cell carci...

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Main Authors: Yang Yang, Cheng Qiang, Zhu Jie, Han Ce, Huang Yan, Li Xiu-bin, Fan Wen-mei, Zhang Xu, Gao Yu
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02434-8
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author Yang Yang
Cheng Qiang
Zhu Jie
Han Ce
Huang Yan
Li Xiu-bin
Fan Wen-mei
Zhang Xu
Gao Yu
author_facet Yang Yang
Cheng Qiang
Zhu Jie
Han Ce
Huang Yan
Li Xiu-bin
Fan Wen-mei
Zhang Xu
Gao Yu
author_sort Yang Yang
collection DOAJ
description Abstract The interaction between tumor-derived exosomes and stroma plays a crucial role in tumor progression. However, the mechanisms through which tumor cells influence stromal changes are not yet fully understood. In our study, through single-cell sequencing analysis of clear cell renal cell carcinoma tissues at varying stages of progression, we determined that the proportion of cancer-associated fibroblasts (CAFs) in advanced renal cell carcinoma tissues was notably higher compared to localized renal cell carcinoma tissues. Comparison of transcriptome sequencing and energy metabolism tests between CAFs primarily isolated from advanced renal cell carcinoma tissues and normal fibroblasts (NFs) revealed the occurrence of the Warburg effect during the fibroblast activation process. Additionally, we observed an increase in glucose transporter GLUT1 expression, total reactive oxygen species (ROS) levels, lactic acid production, and subsequent excretion of excess lactic acid through monocarboxylate transporter-4 (MCT4) in CAFs. Interestingly, renal cancer cells were found to uptake lactic acid via MCT1 upon interaction with CAFs, thereby enhancing their malignant phenotypes. Furthermore, the down-regulation of PANK3 induced by exosomes derived from renal cancer cells was identified as a crucial step in fibroblast activation. These findings indicate that exosomes play a role in facilitating intercellular communication between renal cancer cells and fibroblasts. Targeting this communication pathway could potentially offer new strategies for the prevention and treatment of advanced renal cell carcinoma.
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issn 2058-7716
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series Cell Death Discovery
spelling doaj-art-86ec93234267405bba3dca9c2de8e9142025-08-20T02:19:55ZengNature Publishing GroupCell Death Discovery2058-77162025-04-0111111110.1038/s41420-025-02434-8Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3Yang Yang0Cheng Qiang1Zhu Jie2Han Ce3Huang Yan4Li Xiu-bin5Fan Wen-mei6Zhang Xu7Gao Yu8Department of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalDepartment of Urology, the third Medical Centre, Chinese PLA General HospitalAbstract The interaction between tumor-derived exosomes and stroma plays a crucial role in tumor progression. However, the mechanisms through which tumor cells influence stromal changes are not yet fully understood. In our study, through single-cell sequencing analysis of clear cell renal cell carcinoma tissues at varying stages of progression, we determined that the proportion of cancer-associated fibroblasts (CAFs) in advanced renal cell carcinoma tissues was notably higher compared to localized renal cell carcinoma tissues. Comparison of transcriptome sequencing and energy metabolism tests between CAFs primarily isolated from advanced renal cell carcinoma tissues and normal fibroblasts (NFs) revealed the occurrence of the Warburg effect during the fibroblast activation process. Additionally, we observed an increase in glucose transporter GLUT1 expression, total reactive oxygen species (ROS) levels, lactic acid production, and subsequent excretion of excess lactic acid through monocarboxylate transporter-4 (MCT4) in CAFs. Interestingly, renal cancer cells were found to uptake lactic acid via MCT1 upon interaction with CAFs, thereby enhancing their malignant phenotypes. Furthermore, the down-regulation of PANK3 induced by exosomes derived from renal cancer cells was identified as a crucial step in fibroblast activation. These findings indicate that exosomes play a role in facilitating intercellular communication between renal cancer cells and fibroblasts. Targeting this communication pathway could potentially offer new strategies for the prevention and treatment of advanced renal cell carcinoma.https://doi.org/10.1038/s41420-025-02434-8
spellingShingle Yang Yang
Cheng Qiang
Zhu Jie
Han Ce
Huang Yan
Li Xiu-bin
Fan Wen-mei
Zhang Xu
Gao Yu
Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3
Cell Death Discovery
title Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3
title_full Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3
title_fullStr Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3
title_full_unstemmed Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3
title_short Exosomes derived from ccRCC cells confers fibroblasts activation to foster tumor progression through Warburg effect by downregulating PANK3
title_sort exosomes derived from ccrcc cells confers fibroblasts activation to foster tumor progression through warburg effect by downregulating pank3
url https://doi.org/10.1038/s41420-025-02434-8
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