Retrospective Study
Copyright ©The Author(s) 2022. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Oncol. Aug 15, 2022; 14(8): 1528-1539
Published online Aug 15, 2022. doi: 10.4251/wjgo.v14.i8.1528
Profiling of gene fusion involving targetable genes in Chinese gastric cancer
Zhen-Hua Liu, Bo-Wen Zhu, Min Shi, Yu-Rong Qu, Xun-Jun He, Hong-Ling Yuan, Jie Ma, Wei Li, Dan-Dan Zhao, Zheng-Chuang Liu, Bao-Ming Wang, Chun-Yang Wang, Hou-Quan Tao, Tong-Hui Ma
Zhen-Hua Liu, Department of Medical Oncology, Fujian Medical University, Fuzhou 350001, Fujian Province, China
Bo-Wen Zhu, Min Shi, Yu-Rong Qu, Hong-Ling Yuan, Wei Li, Dan-Dan Zhao, Bao-Ming Wang, Chun-Yang Wang, Medical Center, Genetron Health (Beijing) Technology, Co. Ltd., Beijing 102200, China
Xun-Jun He, Department of Genetics and Genomic Medicine, Zhejiang Provincial People’s Hospital, Hangzhou 310000, Zhejiang Province, China
Xun-Jun He, Zheng-Chuang Liu, Hou-Quan Tao, Key Laboratory of Gastroenterology of Zhejiang Province, Zhejiang Provincial People’s Hospital, Hangzhou 310000, Zhejiang Province, China
Jie Ma, Department of Pathology, Zhejiang Provincial People's Hospital, Hangzhou 310000, Zhejiang Province, China
Zheng-Chuang Liu, Hou-Quan Tao, Department of Gastroenterology of Zhejiang Province, Zhejiang Provincial People’s Hospital, Hangzhou 310000, Zhejiang Province, China
Tong-Hui Ma, Department of Translational Medicine, Genetron Health (Beijing) Technology, Co. Ltd., Beijing 102200, China
Author contributions: Liu ZH and Ma TH designed the study and reviewed the manuscript; Liu ZH, Zhu BW, Shi M analyzed the clinical and gene fusions data and wrote the manuscript; He XJ, Ma J, Liu ZC, and Tao HQ provided clinical advice; Yuan HL, Li W, Zhao DD, Wang BM, and Wang CY reviewed the manuscript and provided advice; All authors have read and approved the final manuscript.
Institutional review board statement: The study was reviewed and approved by the Fujian Provincial Hospital, Institutional Review Board (Approval No. K2022-03-101).
Informed consent statement: All study participants or their legal guardian provided informed written consent about personal and medical data collection prior to study enrolment.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Tong-Hui Ma, PhD, Director, Department of Translational Medicine, Genetron Health (Beijing) Technology, Co. Ltd., 1-2/F, Building 11, Zone 1, 8 Life Science Parkway, Changping District, Beijing 102200, China. tonghuima0818@sina.com
Received: March 30, 2022
Peer-review started: March 30, 2022
First decision: June 2, 2022
Revised: June 14, 2022
Accepted: July 19, 2022
Article in press: July 19, 2022
Published online: August 15, 2022
Processing time: 133 Days and 2.9 Hours
Abstract
BACKGROUND

Approximately half of all new cases of gastric cancer (GC) and related deaths occur in China. More than 80% of patients with GC are diagnosed at an advanced stage, which results in poor prognosis. Although HER2-directed therapy and immune checkpoint inhibitors have been somewhat successful, new drugs are still needed for the treatment of GC. Notably, several gene fusion-targeted drugs have been approved by the United States Food and Drug Administration for solid tumors, including GC, such as larotrectinib for NTRK fusion-positive cancers and zenocutuzumab for NRG1 fusion-positive cancers. However, gene fusions involving targetable genes have not been well characterized in Chinese patients with GC.

AIM

To identify the profile of fusions involving targetable genes in Chinese patients with GC using clinical specimens and determine the distribution of patients with gene fusion variants among the molecular subtypes of GC.

METHODS

We retrospectively analyzed gene fusion events in tumor tissue samples from 954 Chinese patients with GC. Clinicopathological characteristics were obtained from their medical records. Genetic alterations, such as single nucleotide variants, indels, amplifications, and gene fusions, were identified using a targeted sequencing panel containing 825 genes. Fusions were validated by fluorescence in situ hybridization (FISH) using break-apart probes. The microsatellite instability (MSI) status was evaluated using MSIsensor from the targeted sequencing panel data. Tumor mutational burden (TMB) was calculated using the total number of nonsynonymous mutations divided by the total genomic targeted region. Chi-square analysis was used to determine the enrichment of gene fusions associated with the molecular subtypes of GC.

RESULTS

We found that 1.68% (16/954) of patients harbored 20 fusion events involving targetable genes. RARA fusions (n = 5) were the most common, followed by FGFR2, BRAF, MET, FGFR3, RET, ALK, EGFR, NTRK2, and NRG1 fusions. Two of the RARA fusions, EML4-ALK (E6:E20) and EGFR-SEPTIN14 (E7:E10), have been identified in other tumors but not in GC. Surprisingly, 18 gene fusion events were previously not reported in any cancer types. Twelve of the eighteen novel gene fusions included complete exons encoding functional domains of targetable genes, such as the tyrosine kinase domain of receptor tyrosine kinases and the DNA- and ligand-binding domains of RARA. Consistent with the results of detection using the targeted sequencing fusion panel, the results of FISH (fluorescence in situ hybridization) confirmed the rearrangement of FGFR2 and BRAF in tumors from patients 04 and 09, respectively. Genetic analysis indicated that the fusion genes were significantly enriched in patients with ERBB2 amplification (P = 0.02); however, there were no significant differences between fusion-positive and fusion-negative patients in age, sex, MSI status, and TMB.

CONCLUSION

We characterized the landscape of fusions involving targetable genes in a Chinese GC cohort and found that 1.68% of patients with GC harbor potential targetable gene fusions, which were enriched in patients with ERBB2 amplification. Gene fusion detection may provide a potential treatment strategy for patients with GC with disease progression following standard therapy.

Keywords: Gene fusion; Targetable genes; Gastric cancer; Chinese population; ERBB2 amplification

Core Tip: The proportion of patients with gene fusions in Chinese patients with gastric cancer (GC) has not yet been characterized. In our analysis, we found that 1.68% of such patients harbor fusions involving targetable genes. Moreover, these fusion genes were enriched in patients with ERBB2 amplification. Our study indicates that gene fusion detection may provide a novel approach for GC therapy.