Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation

Abstract Breast cancers present intricate microenvironments comprising heterotypic cellular interactions, yet a comprehensive spatial map remained to be established. Here, we employed the DNA nanoball-based genome-wide in situ sequencing (Stereo-seq) to visualize the geospatial architecture of 30 pr...

Full description

Saved in:
Bibliographic Details
Main Authors: Xin Wang, Zhanyu Wang, Qijun Liao, Pei Yuan, Junpu Mei, Yin Zhang, Chao Wu, Xiyu Kang, Sufei Zheng, Chenxuan Yang, Jiaxiang Liu, Qingyao Shang, Jiangtao Li, Bingning Wang, Liangyu Li, Hui Liu, Weining Hu, Zhensheng Dong, Jie Zhao, Linying Wang, Tao Liu, Yusheng Den, Chengrui Wang, Lijuan Han, Qianjun Chen, Huanming Yang, Xun Xu, Jie He, Zhen Yue, Nan Sun, Xiaodong Fang, Jianming Ying
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58511-0
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849737499403878400
author Xin Wang
Zhanyu Wang
Qijun Liao
Pei Yuan
Junpu Mei
Yin Zhang
Chao Wu
Xiyu Kang
Sufei Zheng
Chenxuan Yang
Jiaxiang Liu
Qingyao Shang
Jiangtao Li
Bingning Wang
Liangyu Li
Hui Liu
Weining Hu
Zhensheng Dong
Jie Zhao
Linying Wang
Tao Liu
Yusheng Den
Chengrui Wang
Lijuan Han
Qianjun Chen
Huanming Yang
Xun Xu
Jie He
Zhen Yue
Nan Sun
Xiaodong Fang
Jianming Ying
author_facet Xin Wang
Zhanyu Wang
Qijun Liao
Pei Yuan
Junpu Mei
Yin Zhang
Chao Wu
Xiyu Kang
Sufei Zheng
Chenxuan Yang
Jiaxiang Liu
Qingyao Shang
Jiangtao Li
Bingning Wang
Liangyu Li
Hui Liu
Weining Hu
Zhensheng Dong
Jie Zhao
Linying Wang
Tao Liu
Yusheng Den
Chengrui Wang
Lijuan Han
Qianjun Chen
Huanming Yang
Xun Xu
Jie He
Zhen Yue
Nan Sun
Xiaodong Fang
Jianming Ying
author_sort Xin Wang
collection DOAJ
description Abstract Breast cancers present intricate microenvironments comprising heterotypic cellular interactions, yet a comprehensive spatial map remained to be established. Here, we employed the DNA nanoball-based genome-wide in situ sequencing (Stereo-seq) to visualize the geospatial architecture of 30 primary breast tumors and metastatic lymph nodes across different molecular subtypes. This unprecedented high-resolution atlas unveils the fine structure of the tumor vasculature, highlighting heterogeneity in phenotype, spatial distribution, and intercellular communication within both endothelial and perivascular cells. In particular, venular smooth muscle cells are identified as the primary source of CCL21/CCL19 within the microenvironment. In collaboration with ACKR1-positive endothelial cells, they create a chemokine-rich venular niche to synergistically promote lymphocyte extravasation into tumors. High venule density predicts increased immune infiltration and improved clinical outcomes. This study provides a detailed spatial landscape of human breast cancer, offering key insights into the venular regulation of tumor immune infiltration.
format Article
id doaj-art-45a7a82fff974dc6ba9a7d088e2e01a6
institution DOAJ
issn 2041-1723
language English
publishDate 2025-04-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-45a7a82fff974dc6ba9a7d088e2e01a62025-08-20T03:06:54ZengNature PortfolioNature Communications2041-17232025-04-0116111810.1038/s41467-025-58511-0Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasationXin Wang0Zhanyu Wang1Qijun Liao2Pei Yuan3Junpu Mei4Yin Zhang5Chao Wu6Xiyu Kang7Sufei Zheng8Chenxuan Yang9Jiaxiang Liu10Qingyao Shang11Jiangtao Li12Bingning Wang13Liangyu Li14Hui Liu15Weining Hu16Zhensheng Dong17Jie Zhao18Linying Wang19Tao Liu20Yusheng Den21Chengrui Wang22Lijuan Han23Qianjun Chen24Huanming Yang25Xun Xu26Jie He27Zhen Yue28Nan Sun29Xiaodong Fang30Jianming Ying31Department of Breast Surgical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeBGI ResearchDepartment of Pathology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeBGI ResearchBGI ResearchBGI ResearchDepartment of Breast Surgical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Breast Surgical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Breast Surgical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Breast Surgical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Pathology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeDepartment of Pathology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeBGI ResearchBGI ResearchBGI ResearchBGI ResearchBGI ResearchBGI ResearchBGI ResearchState Key Laboratory of Dampness Syndrome of Chinese Medicine, The Second Affiliated Hospital of Guangzhou University of Chinese MedicineState Key Laboratory of Dampness Syndrome of Chinese Medicine, The Second Affiliated Hospital of Guangzhou University of Chinese MedicineState Key Laboratory of Dampness Syndrome of Chinese Medicine, The Second Affiliated Hospital of Guangzhou University of Chinese MedicineState Key Laboratory of Dampness Syndrome of Chinese Medicine, The Second Affiliated Hospital of Guangzhou University of Chinese MedicineBGI ResearchBGI ResearchDepartment of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeBGI ResearchDepartment of Thoracic Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeBGI ResearchState Key Laboratory of Molecular Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical CollegeAbstract Breast cancers present intricate microenvironments comprising heterotypic cellular interactions, yet a comprehensive spatial map remained to be established. Here, we employed the DNA nanoball-based genome-wide in situ sequencing (Stereo-seq) to visualize the geospatial architecture of 30 primary breast tumors and metastatic lymph nodes across different molecular subtypes. This unprecedented high-resolution atlas unveils the fine structure of the tumor vasculature, highlighting heterogeneity in phenotype, spatial distribution, and intercellular communication within both endothelial and perivascular cells. In particular, venular smooth muscle cells are identified as the primary source of CCL21/CCL19 within the microenvironment. In collaboration with ACKR1-positive endothelial cells, they create a chemokine-rich venular niche to synergistically promote lymphocyte extravasation into tumors. High venule density predicts increased immune infiltration and improved clinical outcomes. This study provides a detailed spatial landscape of human breast cancer, offering key insights into the venular regulation of tumor immune infiltration.https://doi.org/10.1038/s41467-025-58511-0
spellingShingle Xin Wang
Zhanyu Wang
Qijun Liao
Pei Yuan
Junpu Mei
Yin Zhang
Chao Wu
Xiyu Kang
Sufei Zheng
Chenxuan Yang
Jiaxiang Liu
Qingyao Shang
Jiangtao Li
Bingning Wang
Liangyu Li
Hui Liu
Weining Hu
Zhensheng Dong
Jie Zhao
Linying Wang
Tao Liu
Yusheng Den
Chengrui Wang
Lijuan Han
Qianjun Chen
Huanming Yang
Xun Xu
Jie He
Zhen Yue
Nan Sun
Xiaodong Fang
Jianming Ying
Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
Nature Communications
title Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
title_full Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
title_fullStr Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
title_full_unstemmed Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
title_short Spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
title_sort spatially resolved atlas of breast cancer uncovers intercellular machinery of venular niche governing lymphocyte extravasation
url https://doi.org/10.1038/s41467-025-58511-0
work_keys_str_mv AT xinwang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT zhanyuwang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT qijunliao spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT peiyuan spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT junpumei spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT yinzhang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT chaowu spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT xiyukang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT sufeizheng spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT chenxuanyang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT jiaxiangliu spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT qingyaoshang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT jiangtaoli spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT bingningwang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT liangyuli spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT huiliu spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT weininghu spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT zhenshengdong spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT jiezhao spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT linyingwang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT taoliu spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT yushengden spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT chengruiwang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT lijuanhan spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT qianjunchen spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT huanmingyang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT xunxu spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT jiehe spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT zhenyue spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT nansun spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT xiaodongfang spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation
AT jianmingying spatiallyresolvedatlasofbreastcanceruncoversintercellularmachineryofvenularnichegoverninglymphocyteextravasation