Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma

Abstract Background Pediatric lymphoepithelioma-like carcinoma (pLELC) is a rare neoplasm with unclear prognosis, genome, and tumor microenvironment. Our study aims to elucidate its genomic and clinical characteristics. Methods Forty-one pLELC patients were enrolled at Sun Yat-sen University Cancer...

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Main Authors: Yi Que, Xiuxia Lu, Suying Lu, Feifei Sun, Jia Zhu, Yu Zhang, Juan Wang, Junting Huang, Wei Liu, Fenghua Wang, Liping Li, Li Zhang, Min Gao, Zijun Zhen, Yizhuo Zhang
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-024-05921-1
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author Yi Que
Xiuxia Lu
Suying Lu
Feifei Sun
Jia Zhu
Yu Zhang
Juan Wang
Junting Huang
Wei Liu
Fenghua Wang
Liping Li
Li Zhang
Min Gao
Zijun Zhen
Yizhuo Zhang
author_facet Yi Que
Xiuxia Lu
Suying Lu
Feifei Sun
Jia Zhu
Yu Zhang
Juan Wang
Junting Huang
Wei Liu
Fenghua Wang
Liping Li
Li Zhang
Min Gao
Zijun Zhen
Yizhuo Zhang
author_sort Yi Que
collection DOAJ
description Abstract Background Pediatric lymphoepithelioma-like carcinoma (pLELC) is a rare neoplasm with unclear prognosis, genome, and tumor microenvironment. Our study aims to elucidate its genomic and clinical characteristics. Methods Forty-one pLELC patients were enrolled at Sun Yat-sen University Cancer Center from 2012 to 2023. Kaplan–Meier analysis was utilized to estimate progression-free survival (PFS) and overall survival (OS). Baseline plasma protein levels from 16 patients and 9 health controls were analyzed using a Olink proteomic platform and whole exon sequence (WES) was performed on 11 tumor samples from 10 pediatric patients. Immunohistochemistry (IHC) for PD-L1was performed, and the infiltration of CD4+ or CD8+ T cells was evaluated. Results Patients receiving anti PD-1 in combination with chemotherapy had a 1-year PFS of 100%, while the 2-year PFS was 72.92% (95%CI: 46.80‒100%). The 1-year OS for patients receiving anti PD-1 in combination with chemotherapy was 100%, and the 2-year OS was 87.5% (95%CI: 67.34–100%). Significant upregulation of immune checkpoint molecules was detected including LAG-3, PD-L1, and galectin-9 in LELC group by proteomic analysis (P < 0.05). The mutational landscape of pediatric LELC presented more genes mutated in pathways associated with immune, DNA repair, cell cycle and NOTCH. Pathway analysis of mutational profiles indicated DNA repair pathway and SWI/SNF complex were potential drug targets for pLELC patients. All the pediatric LELC patients evaluated exhibited positive PD-L1 expression and CD4+/CD8+ T cells infiltration. Conclusions Our findings indicate a promising response rate associated with the combination of PD-1 antibody treatment and chemotherapy in pediatric patients with LELC, providing a theoretical basis for targeting DNA repair pathways. These outcomes suggest that clinical trials involving immune checkpoint inhibitors are warranted in pediatric patients with LELC.
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spelling doaj-art-818ade6c0be34de8af1c02af7fba05b22024-12-08T12:44:48ZengBMCJournal of Translational Medicine1479-58762024-12-0122111710.1186/s12967-024-05921-1Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinomaYi Que0Xiuxia Lu1Suying Lu2Feifei Sun3Jia Zhu4Yu Zhang5Juan Wang6Junting Huang7Wei Liu8Fenghua Wang9Liping Li10Li Zhang11Min Gao12Zijun Zhen13Yizhuo Zhang14Department of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Radiology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pathology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Thoracic Surgery, Guangzhou Women and Children’s Medical CentreDepartment of Thoracic Surgery, Guangzhou Women and Children’s Medical CentreDepartment of Pathology, Guangzhou Women and Children’s Medical CentreDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterDepartment of Pediatric Oncology, State Key Laboratory of Oncology in South China, Guangdong Provincial Clinical Research Center for Cancer, Collaborative Innovation Center for Cancer Medicine, Sun Yat-Sen University Cancer CenterAbstract Background Pediatric lymphoepithelioma-like carcinoma (pLELC) is a rare neoplasm with unclear prognosis, genome, and tumor microenvironment. Our study aims to elucidate its genomic and clinical characteristics. Methods Forty-one pLELC patients were enrolled at Sun Yat-sen University Cancer Center from 2012 to 2023. Kaplan–Meier analysis was utilized to estimate progression-free survival (PFS) and overall survival (OS). Baseline plasma protein levels from 16 patients and 9 health controls were analyzed using a Olink proteomic platform and whole exon sequence (WES) was performed on 11 tumor samples from 10 pediatric patients. Immunohistochemistry (IHC) for PD-L1was performed, and the infiltration of CD4+ or CD8+ T cells was evaluated. Results Patients receiving anti PD-1 in combination with chemotherapy had a 1-year PFS of 100%, while the 2-year PFS was 72.92% (95%CI: 46.80‒100%). The 1-year OS for patients receiving anti PD-1 in combination with chemotherapy was 100%, and the 2-year OS was 87.5% (95%CI: 67.34–100%). Significant upregulation of immune checkpoint molecules was detected including LAG-3, PD-L1, and galectin-9 in LELC group by proteomic analysis (P < 0.05). The mutational landscape of pediatric LELC presented more genes mutated in pathways associated with immune, DNA repair, cell cycle and NOTCH. Pathway analysis of mutational profiles indicated DNA repair pathway and SWI/SNF complex were potential drug targets for pLELC patients. All the pediatric LELC patients evaluated exhibited positive PD-L1 expression and CD4+/CD8+ T cells infiltration. Conclusions Our findings indicate a promising response rate associated with the combination of PD-1 antibody treatment and chemotherapy in pediatric patients with LELC, providing a theoretical basis for targeting DNA repair pathways. These outcomes suggest that clinical trials involving immune checkpoint inhibitors are warranted in pediatric patients with LELC.https://doi.org/10.1186/s12967-024-05921-1PediatricLymphoepithelioma-like carcinomaPD-1Survival
spellingShingle Yi Que
Xiuxia Lu
Suying Lu
Feifei Sun
Jia Zhu
Yu Zhang
Juan Wang
Junting Huang
Wei Liu
Fenghua Wang
Liping Li
Li Zhang
Min Gao
Zijun Zhen
Yizhuo Zhang
Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma
Journal of Translational Medicine
Pediatric
Lymphoepithelioma-like carcinoma
PD-1
Survival
title Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma
title_full Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma
title_fullStr Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma
title_full_unstemmed Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma
title_short Genomic and clinical characterization of pediatric lymphoepithelioma-like carcinoma
title_sort genomic and clinical characterization of pediatric lymphoepithelioma like carcinoma
topic Pediatric
Lymphoepithelioma-like carcinoma
PD-1
Survival
url https://doi.org/10.1186/s12967-024-05921-1
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