Cancer-associated fibroblast-derived SEMA3C facilitates colorectal cancer liver metastasis via NRP2-mediated MAPK activation

Y Yuyuan Zhang (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) A Anning Zuo (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) Y Yuhao Ba (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) S Shutong Liu (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) J Jingqi Chen S Shuaixi Yang (Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University) S Siyuan Weng (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) Y Yukang Chen (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) H Hui Xu P Peng Luo Q Quan Cheng (Department of Neurosurgery, Xiangya Hospital, Central South University) B Bufu Tang (Department of Radiation Oncology, Zhongshan Hospital, Fudan University) B Benyu Liu (Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University) C Chuhan Zhang (Department of Oncology, The First Affiliated Hospital of Zhengzhou University) J Jingkuan Yang (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) X Xinwei Han (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University) Z Zaoqu Liu (Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University)

Abstract

Liver metastasis remains the predominant cause of mortality in patients with colorectal cancer (CRC). Nevertheless, the mechanisms underlying the initiation of colorectal cancer liver metastasis remain poorly elucidated. During the metastatic process of CRC cells from the primary site to the liver, we performed time-resolved analyses and identified a subset of tumor cells spatially located in the primary tumor and temporally distributed in the early stages of liver metastasis. These cells were termed liver metastasis-initiating cells (LMICs). LMICs exhibit high stemness, low proliferation, active interaction with surrounding stromal components, and a close association with liver metastasis. Notably, we found significant interactions between cancer-associated fibroblasts (CAFs) and LMICs via the SEMA3C–NRP2 receptor–ligand pair. Further in vivo and in vitro experiments confirmed that CAF-secreted SEMA3C could bind to the NRP2 receptor, which activates the MAPK pathway and promotes colorectal cancer liver metastasis. Our findings suggest potential therapeutic strategies for the early prevention of colorectal cancer liver metastasis.

Article Details

Volume / Issue Vol. 122, Issue 21
Published May 27, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

Y

Yuyuan Zhang

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

A

Anning Zuo

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

Y

Yuhao Ba

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

S

Shutong Liu

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

J

Jingqi Chen

S

Shuaixi Yang

Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University

S

Siyuan Weng

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

Y

Yukang Chen

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

H

Hui Xu

P

Peng Luo

Q

Quan Cheng

Department of Neurosurgery, Xiangya Hospital, Central South University

B

Bufu Tang

Department of Radiation Oncology, Zhongshan Hospital, Fudan University

B

Benyu Liu

Tianjian Laboratory of Advanced Biomedical Sciences, Academy of Medical Sciences, Zhengzhou University

C

Chuhan Zhang

Department of Oncology, The First Affiliated Hospital of Zhengzhou University

J

Jingkuan Yang

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

X

Xinwei Han

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University

Z

Zaoqu Liu

Department of Interventional Radiology, The First Affiliated Hospital of Zhengzhou University