Evolution of immune and stromal cell states and ecotypes during gastric adenocarcinoma progression

Ruiping Wang, Shumei Song, Jiangjiang Qin, Katsuhiro Yoshimura, Fuduan Peng, Yanshuo Chu, Yuan Li, Yibo Fan, Jiankang Jin, Minghao Dang, Enyu Dai, Guangsheng Pei, Guangchun Han, Dapeng Hao, Yating Li, Deyali Chatterjee, Kazuto Harada, Melissa Pool Pizzi, Ailing W. Scott, Ghia TatlonghariXinmiao Yan, Zhiyuan Xu, Can Hu, Shaowei Mo, Namita Shanbhag, Yang Lu, Matheus Sewastjanow-Silva, Ahmed Adel Fouad Abdelhakeem, Guang Peng, Samir M. Hanash, George A. Calin, Cassian Yee, Pawel Mazur, Autumn N. Marsden, Andrew Futreal, Zhenning Wang, Xiangdong Cheng, Jaffer A. Ajani, Linghua Wang

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

Understanding tumor microenvironment (TME) reprogramming in gastric adenocarcinoma (GAC) progression may uncover novel therapeutic targets. Here, we performed single-cell profiling of precancerous lesions, localized and metastatic GACs, identifying alterations in TME cell states and compositions as GAC progresses. Abundant IgA+ plasma cells exist in the premalignant microenvironment, whereas immunosuppressive myeloid and stromal subsets dominate late-stage GACs. We identified six TME ecotypes (EC1-6). EC1 is exclusive to blood, while EC4, EC5, and EC2 are highly enriched in uninvolved tissues, premalignant lesions, and metastases, respectively. EC3 and EC6, two distinct ecotypes in primary GACs, associate with histopathological and genomic characteristics, and survival outcomes. Extensive stromal remodeling occurs in GAC progression. High SDC2 expression in cancer-associated fibroblasts (CAFs) is linked to aggressive phenotypes and poor survival, and SDC2 overexpression in CAFs contributes to tumor growth. Our study provides a high-resolution GAC TME atlas and underscores potential targets for further investigation.

Original languageEnglish (US)
Pages (from-to)1407-1426.e9
JournalCancer cell
Volume41
Issue number8
DOIs
StatePublished - Aug 14 2023

Keywords

  • Cancer-associated fibroblast
  • Chronic Atrophic Gastritis
  • Ecotype
  • Gastric Adenocarcinoma
  • Immune-Stroma Crosstalk
  • Intestinal Metaplasia
  • Peritoneal Carcinomatosis
  • Single Cell RNA Sequencing
  • Syndecan 2
  • Tumor Microenvironment

ASJC Scopus subject areas

  • Oncology
  • Cancer Research

MD Anderson CCSG core facilities

  • Research Animal Support Facility
  • Cytogenetics and Cell Authentication Core
  • Tissue Biospecimen and Pathology Resource
  • Advanced Technology Genomics Core

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