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Dissecting Transcriptional Heterogeneity in Primary Gastric Adenocarcinoma by Single Cell RNA Sequencing

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Dissecting Transcriptional Heterogeneity in Primary Gastric Adenocarcinoma by Single Cell RNA Sequencing Stomach Original research Dissecting transcriptional heterogeneity in primary Gut: first published as 10.1136/gutjnl-2019-320368 on 12 June 2020. Downloaded from gastric adenocarcinoma by single cell RNA sequencing Min Zhang,1,2 Shuofeng Hu,1,3 Min Min,2 Yanli Ni,2 Zheng Lu,2 Xiaotian Sun,2,4 Jiaqi Wu,1,3 Bing Liu,1,2 Xiaomin Ying,1,3 Yan Liu 2 ► Additional material is ABSTRact published online only. To view, Objective Tumour heterogeneity represents a major Significance of this study please visit the journal online obstacle to accurate diagnosis and treatment in gastric (http:// dx. doi. org/ 10. 1136/ What is already known on this subject? gutjnl- 2019- 320368). adenocarcinoma (GA). Here, we report a systematic ► Gastric adenocarcinoma (GA) is a highly 1 transcriptional atlas to delineate molecular and cellular Academy of Military Medical heterogeneous malignant disease that is Sciences, Beijing, China heterogeneity in GA using single- cell RNA sequencing 2 affected by multiple genetic and environmental The Fifth Medical Center of (scRNA- seq). Chinese PLA General Hospital, Design We performed unbiased transcriptome-wide factors. Beijing, China ► The molecular and cellular heterogeneity in GA 3 scRNA-seq analysis on 27 677 cells from 9 tumour Center for Computational and 3 non-tumour samples. Analysis results were are rarely described at single-cell resolution. Biology, Institute of Military ► Chief cell predominant GA (GA- FG- CCP) is a Cognition and Brain Sciences, validated using large-scale histological assays and bulk Academy of Military Medical transcriptomic datasets. rare variant of gastric cancer in the fundic gland Sciences, Beijing, China Results Our integrative analysis of tumour cells region predominant of differentiated chief cells. 4 Department of internal identified five cell subgroups with distinct expression medicine, Beijing South Medical What are the new findings? profiles. A panel of differentiation-related genes reveals District of Chinese PLA General ► We delineated cellular and differentiation Hospital, Beijing, China a high diversity of differentiation degrees within and heterogeneity within and between patients between tumours. Low differentiation degrees can with GA at single cell resolution. predict poor prognosis in GA. Among them, three Correspondence to ► Transcriptomically, we delineated the molecular Prof Yan Liu and Prof Bing Liu, subgroups exhibited different differentiation grade characteristics of a rare GA type, GA-FG- CCP , at The Fifth Medical Center of which corresponded well to histopathological features of http://gut.bmj.com/ Chinese PLA General Hospital, single- cell resolution and validated its presence Beijing, 100071, China; Lauren’s subtypes. Interestingly, the other two subgroups in two public bulk transcriptomic datasets. displayed unique transcriptome features. One subgroup liuyan1799@ 126. com, ► Computational analysis of non- malignant bingliu17@ yahoo. com and expressing chief-cell markers (eg, LIPF and PGC) and epithelium uncovers a potential transition Prof Xiaomin Ying, Center for RNF43 with Wnt/β-catenin signalling pathway activated from chief cells to MUC6+TFF2+ spasmolytic Computational Biology, Institute is consistent with the previously described entity fundic of Military Cognition and Brain polypeptide expressing metaplasia. Sciences, Academy of Military gland- type GA (chief cell- predominant, GA- FG- CCP). Sciences, Beijing, 100850, We further confirmed the presence of GA-FG- CCP in How might it impact on clinical practice in the on September 26, 2021 by guest. Protected copyright. China; yingxmbio@ foxmail. com two public bulk datasets using transcriptomic profiles foreseeable future? and histological images. The other subgroup specifically ► The comprehensive transcriptome atlas is MZ, SH and MM contributed equally. expressed immune-related signature genes (eg, LY6K a valuable resource for deciphering gastric BL, XY and YL contributed and major histocompatibility complex class II) with tumour heterogeneity. equally. the infection of Epstein-Barr virus. In addition, we ► Tumour differentiation degree is a potential also analysed non-malignant epithelium and provided good predictor of GA prognosis. Received 27 November 2019 molecular evidences for potential transition from gastric ► Our results revealed that single- cell RNA Revised 19 May 2020 + + Accepted 26 May 2020 chief cells into MUC6 TFF2 spasmolytic polypeptide sequencing can be employed in detection Published Online First expressing metaplasia. of rare tumour types (eg, GA- FG- CCP) and 12 June 2020 Conclusion Altogether, our study offers valuable accurate diagnosis of GA. resource for deciphering gastric tumour heterogeneity, ► The trajectory analysis of potential chief cells which will provide assistance for precision diagnosis and transition presented should help to clarify the prognosis. mechanism of gastric carcinogenesis. © Author(s) (or their employer(s)) 2021. Re-use permitted under CC BY-NC . No INTRODUCTION heterogeneous malignant disease, which is featured commercial re-use . See rights Tumour heterogeneity including morphological with diverse subtypes and clinical behaviours.1 2 and permissions. Published heterogeneity and genetic heterogeneity remains a For years, morphological heterogeneity has long by BMJ. topic of great interest in cancer research because it been the basis of many tumour grading and prog- To cite: Zhang M, Hu S, poses a series of challenges to both accurate diag- nostic classification systems. According to struc- Min M, et al. Gut nosis and personalised therapy. Gastric adeno- tural gland atypia and the differentiation degree of 2021;70:464–475. carcinoma (GA) is an archetypal example of a GA mucosa, the Lauren’s classification3 generally 464 Zhang M, et al. Gut 2021;70:464–475. doi:10.1136/gutjnl-2019-320368 Stomach classifies GA into intestinal and diffuse type. Later, the mixed RESULTS type has been proposed to describe intermediate histology cases. A single-cell transcriptome atlas in diverse GA types Gut: first published as 10.1136/gutjnl-2019-320368 on 12 June 2020. Downloaded from The intestinal- type GA characteristically form glandular struc- To investigate the cell populations and the associated molecular tures and show various degrees of differentiation, which are characteristics within the gastric mucosa of various lesions, five usually developed through well-characterised sequential patho- intestinal- histology GA samples (one with EBV infection), three logical stages, such as chronic gastritis (CG), atrophy, intestinal mixed-histology GA samples, one diffuse- histology GA sample metaplasia and dysplasia. The diffuse- type GA generally exhibit and three non- malignant samples (control, one CG sample from a poorly differentiated status, characterised by poorly differenti- adjacent tumour and two normal samples from gastric polyps) ated infiltrative growth, associated with aggressive behaviour and were included in our scRNA- seq survey (figure 1A,B, online poor prognosis. Another histopathology-based guidelines—the supplementary figure S1). The enrolled patients were all newly WHO classification4 has also been developed for GA diagnosis diagnosed and had not been diagnosed with any other tumours. which divides GA into papillary, tubular, mucinous (colloid) Patients did not receive chemotherapy or radiotherapy prior and poorly cohesive carcinomas. Although these methods are to surgery. The clinical characteristics of these participants, straightforward and simple to use, the pathology results may including H. pylori infection status, EBV infection status, patho- vary because of subjective discrimination and complex back- logical features and tumour classification according to Lauren’s ground factors such as Helicobacter pylori (H. pylori) bacterium5 system, were recorded at the time of recruitment (table 1). and Epstein- Barr virus (EBV).6 Furthermore, the molecular basis After removal of low-quality cells (see ‘Methods’ section in of the phenotypic expression associated with gastric tumour online supplementary materials), 27 677 cells were retained biological behaviour remains poorly understood, limiting the for biological analysis, which detected a median of 1227 genes dissection of tumour heterogeneity. and 3809 transcripts per cell (online supplementary figure S2). The advent of high-throughput sequencing technology has After normalisation of gene expression and principal component accelerated the pace of research on molecular profiling of analysis (PCA), we used graph- based clustering (see ‘Methods’ many human tumours dramatically. In addition, it has been section in online supplementary materials) to partition the cells recognised that analysis of tumour behaviour at the molecular into 14 clusters. These clusters could be assigned to nine known level are increasingly important for dissecting heterogeneity. To cell lineages through marker genes (figure 1C–E): epithelium date, large-scale genomic and transcriptomic studies have char- (10 411 cells, 37.6%, marked with EPCAM, KRT18 and KRT8), acterised the genetic and epigenetic heterogeneity of GA. The parietal cell (215 cells, 0.8%, marked with ATP4A), endocrine molecular profiling studies such as The Cancer Genome Atlas cell (486 cells, 1.8%, marked with CHGA); B cells (6131 cells, (TCGA),7 Singapore8 and Asian Cancer Research Group9 geno- 22.1%, marked with MS4A1 and CD79A); T cells (6819 cells, typing have extended our knowledge for basic research of GA. 24.6%, marked with CD2, CD3D and CD3E);
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