NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1

Abstract Background The NTRK fusion gene is a rare cancer driver and a typical representative "diamond mutation". Its unique role in tumor progression is highly important for the clinical diagnosis and treatment of patients with tumors. We searched for NTRK fusion-positive patients in our...

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Main Authors: Siqing Zeng, Ke Jiang, Jie Ge, Mimi Tang, Yuqi Wen, Xiaoting Ma, Heli Liu, Xingui Xiong
Format: Article
Language:English
Published: BMC 2024-12-01
Series:BMC Cancer
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Online Access:https://doi.org/10.1186/s12885-024-13271-w
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author Siqing Zeng
Ke Jiang
Jie Ge
Mimi Tang
Yuqi Wen
Xiaoting Ma
Heli Liu
Xingui Xiong
author_facet Siqing Zeng
Ke Jiang
Jie Ge
Mimi Tang
Yuqi Wen
Xiaoting Ma
Heli Liu
Xingui Xiong
author_sort Siqing Zeng
collection DOAJ
description Abstract Background The NTRK fusion gene is a rare cancer driver and a typical representative "diamond mutation". Its unique role in tumor progression is highly important for the clinical diagnosis and treatment of patients with tumors. We searched for NTRK fusion-positive patients in our hospital. As of August 2022, a total of 8 patients were affected. We discovered that NTRK fusion was associated with enhanced tumor invasion and migration ability. Previous reports also support this finding, but its underlying mechanism has not been elucidated. Methods We undertook a comprehensive exploration of the correlations between NTRK fusions and tumor invasion as well as migration by analysing clinical data, performing bioinformatics analysis via public databases, and conducting in vitro cell experiments. Results We ascertained that within the thyroid cancer (THCA) dataset and the pancancer dataset, ECM1 and NOVA1 were coexpressed with NTRKs. Additionally, they demonstrated a significant association with the activity of the epithelial‒mesenchymal transition (EMT) pathway. Furthermore, these genes are overexpressed in various cancers and are associated with advanced clinical stage and increased aggressiveness. Our in vitro study revealed that larolutinib potentially inhibited the invasion and metastasis ability of NTRK-fused cells. Interestingly, contrary to previous findings, the repression of ECM1 increased the migration and invasion ability of NTRK-fused tumor cells. Conclusions NTRK fusion tumors present heightened migratory and invasive potential in clinical settings. Further experiments confirmed the significant inhibitory effects of TRK inhibitors on the migration and invasion abilities of these cells. There is a complex relationship between ECM1, NOVA1 and NTRK fusion; however, further research is needed to determine whether NTRK fusion promotes tumor metastasis through these two genes.
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spelling doaj-art-9808fb83a0134444acb3b34fc5bf08c92025-08-20T02:30:54ZengBMCBMC Cancer1471-24072024-12-0124111610.1186/s12885-024-13271-wNTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1Siqing Zeng0Ke Jiang1Jie Ge2Mimi Tang3Yuqi Wen4Xiaoting Ma5Heli Liu6Xingui Xiong7Institute of Integrative Medicine, Department of Integrated Traditional Chinese and Western Medicine, Xiangya Hospital, Central South UniversityInstitute of Integrative Medicine, Department of Integrated Traditional Chinese and Western Medicine, Xiangya Hospital, Central South UniversityDepartment of Gastrointestinal Surgery, Xiangya Hospital, Central South UniversityDepartment of Pharmacy, Xiangya Hospital, Central South UniversityInstitute of Integrative Medicine, Department of Integrated Traditional Chinese and Western Medicine, Xiangya Hospital, Central South UniversityInstitute of Integrative Medicine, Department of Integrated Traditional Chinese and Western Medicine, Xiangya Hospital, Central South UniversityDepartment of Gastrointestinal Surgery, Xiangya Hospital, Central South UniversityInstitute of Integrative Medicine, Department of Integrated Traditional Chinese and Western Medicine, Xiangya Hospital, Central South UniversityAbstract Background The NTRK fusion gene is a rare cancer driver and a typical representative "diamond mutation". Its unique role in tumor progression is highly important for the clinical diagnosis and treatment of patients with tumors. We searched for NTRK fusion-positive patients in our hospital. As of August 2022, a total of 8 patients were affected. We discovered that NTRK fusion was associated with enhanced tumor invasion and migration ability. Previous reports also support this finding, but its underlying mechanism has not been elucidated. Methods We undertook a comprehensive exploration of the correlations between NTRK fusions and tumor invasion as well as migration by analysing clinical data, performing bioinformatics analysis via public databases, and conducting in vitro cell experiments. Results We ascertained that within the thyroid cancer (THCA) dataset and the pancancer dataset, ECM1 and NOVA1 were coexpressed with NTRKs. Additionally, they demonstrated a significant association with the activity of the epithelial‒mesenchymal transition (EMT) pathway. Furthermore, these genes are overexpressed in various cancers and are associated with advanced clinical stage and increased aggressiveness. Our in vitro study revealed that larolutinib potentially inhibited the invasion and metastasis ability of NTRK-fused cells. Interestingly, contrary to previous findings, the repression of ECM1 increased the migration and invasion ability of NTRK-fused tumor cells. Conclusions NTRK fusion tumors present heightened migratory and invasive potential in clinical settings. Further experiments confirmed the significant inhibitory effects of TRK inhibitors on the migration and invasion abilities of these cells. There is a complex relationship between ECM1, NOVA1 and NTRK fusion; however, further research is needed to determine whether NTRK fusion promotes tumor metastasis through these two genes.https://doi.org/10.1186/s12885-024-13271-wCancerNTRK fusionEMTECM1TRK inhibitor
spellingShingle Siqing Zeng
Ke Jiang
Jie Ge
Mimi Tang
Yuqi Wen
Xiaoting Ma
Heli Liu
Xingui Xiong
NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1
BMC Cancer
Cancer
NTRK fusion
EMT
ECM1
TRK inhibitor
title NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1
title_full NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1
title_fullStr NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1
title_full_unstemmed NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1
title_short NTRK fusion promotes tumor migration and invasion through epithelial–mesenchymal transition and closely interacts with ECM1 and NOVA1
title_sort ntrk fusion promotes tumor migration and invasion through epithelial mesenchymal transition and closely interacts with ecm1 and nova1
topic Cancer
NTRK fusion
EMT
ECM1
TRK inhibitor
url https://doi.org/10.1186/s12885-024-13271-w
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