Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study

Background Genetic variations of some driver genes in non-small cell lung cancer (NSCLC) had shown potential impact on immune microenvironment and associated with response or resistance to programmed cell death protein 1 (PD-1) blockade immunotherapy. We therefore undertook an exploratory analysis t...

Full description

Saved in:
Bibliographic Details
Main Authors: Jian Wang, Yi-Long Wu, Xue Bai, De-Hua Wu, Si-Cong Ma, Xin-Ran Tang, Shuai Kang, Qiang John Fu, Chuan-Hui Cao, He-San Luo, Yu-Han Chen, Hong-Bo Zhu, Hong-Hong Yan, Zhong-Yi Dong
Format: Article
Language:English
Published: BMJ Publishing Group 2020-05-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/8/1/e000381.full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846172650520444928
author Jian Wang
Yi-Long Wu
Xue Bai
De-Hua Wu
Si-Cong Ma
Xin-Ran Tang
Shuai Kang
Qiang John Fu
Chuan-Hui Cao
He-San Luo
Yu-Han Chen
Hong-Bo Zhu
Hong-Hong Yan
Zhong-Yi Dong
author_facet Jian Wang
Yi-Long Wu
Xue Bai
De-Hua Wu
Si-Cong Ma
Xin-Ran Tang
Shuai Kang
Qiang John Fu
Chuan-Hui Cao
He-San Luo
Yu-Han Chen
Hong-Bo Zhu
Hong-Hong Yan
Zhong-Yi Dong
author_sort Jian Wang
collection DOAJ
description Background Genetic variations of some driver genes in non-small cell lung cancer (NSCLC) had shown potential impact on immune microenvironment and associated with response or resistance to programmed cell death protein 1 (PD-1) blockade immunotherapy. We therefore undertook an exploratory analysis to develop a genomic mutation signature (GMS) and predict the response to anti-PD-(L)1 therapy.Methods In this multicohort analysis, 316 patients with non-squamous NSCLC treated with anti-PD-(L)1 from three independent cohorts were included in our study. Tumor samples from the patients were molecularly profiled by MSK-IMPACT or whole exome sequencing. We developed a risk model named GMS based on the MSK training cohort (n=123). The predictive model was first validated in the separate internal MSK cohort (n=82) and then validated in an external cohort containing 111 patients from previously published clinical trials.Results A GMS risk model consisting of eight genes (TP53, KRAS, STK11, EGFR, PTPRD, KMT2C, SMAD4, and HGF) was generated to classify patients into high and low GMS groups in the training cohort. Patients with high GMS in the training cohort had longer progression-free survival (hazard ratio (HR) 0.41, 0.28–0.61, p<0.0001) and overall survival (HR 0.53, 0.32–0.89, p=0.0275) compared with low GMS. We noted equivalent findings in the internal validation cohort and in the external validation cohort. The GMS was demonstrated as an independent predictive factor for anti-PD-(L)1 therapy comparing with tumor mutational burden. Meanwhile, GMS showed undifferentiated predictive value in patients with different clinicopathological features. Notably, both GMS and PD-L1 were independent predictors and demonstrated poorly correlated; inclusion of PD-L1 with GMS further improved the predictive capacity for PD-1 blockade immunotherapy.Conclusions Our study highlights the potential predictive value of GMS for immunotherapeutic benefit in non-squamous NSCLC. Besides, the combination of GMS and PD-L1 may serve as an optimal partner in guiding treatment decisions for anti-PD-(L)1 based therapy.
format Article
id doaj-art-2daf1a4f2e834ec6869612616cff4cc8
institution Kabale University
issn 2051-1426
language English
publishDate 2020-05-01
publisher BMJ Publishing Group
record_format Article
series Journal for ImmunoTherapy of Cancer
spelling doaj-art-2daf1a4f2e834ec6869612616cff4cc82024-11-09T13:55:11ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262020-05-018110.1136/jitc-2019-000381Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort studyJian Wang0Yi-Long Wu1Xue Bai2De-Hua Wu3Si-Cong Ma4Xin-Ran Tang5Shuai Kang6Qiang John Fu7Chuan-Hui Cao8He-San Luo9Yu-Han Chen10Hong-Bo Zhu11Hong-Hong Yan12Zhong-Yi Dong13Department of Pain Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan, ChinaGuangdong Lung Cancer Institute, Guangdong Provincial People`s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, China2University of Missouri School of Medicine, Columbia, MO, USA1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, China1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, China1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Beijing, China3 Department of Epidemiology and Biostatistics, Saint Louis University College for Public Health and Social Justice, Saint Louis, Missouri, USA1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, China1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, China1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, China2 Hepatology Unit and Department of Infectious Diseases, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, ChinaGuangdong Lung Cancer Institute, Guangdong Provincial People`s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, China1 Department of Radiation Oncology, Southern Medical University Nanfang Hospital, Guangzhou, Guangdong, ChinaBackground Genetic variations of some driver genes in non-small cell lung cancer (NSCLC) had shown potential impact on immune microenvironment and associated with response or resistance to programmed cell death protein 1 (PD-1) blockade immunotherapy. We therefore undertook an exploratory analysis to develop a genomic mutation signature (GMS) and predict the response to anti-PD-(L)1 therapy.Methods In this multicohort analysis, 316 patients with non-squamous NSCLC treated with anti-PD-(L)1 from three independent cohorts were included in our study. Tumor samples from the patients were molecularly profiled by MSK-IMPACT or whole exome sequencing. We developed a risk model named GMS based on the MSK training cohort (n=123). The predictive model was first validated in the separate internal MSK cohort (n=82) and then validated in an external cohort containing 111 patients from previously published clinical trials.Results A GMS risk model consisting of eight genes (TP53, KRAS, STK11, EGFR, PTPRD, KMT2C, SMAD4, and HGF) was generated to classify patients into high and low GMS groups in the training cohort. Patients with high GMS in the training cohort had longer progression-free survival (hazard ratio (HR) 0.41, 0.28–0.61, p<0.0001) and overall survival (HR 0.53, 0.32–0.89, p=0.0275) compared with low GMS. We noted equivalent findings in the internal validation cohort and in the external validation cohort. The GMS was demonstrated as an independent predictive factor for anti-PD-(L)1 therapy comparing with tumor mutational burden. Meanwhile, GMS showed undifferentiated predictive value in patients with different clinicopathological features. Notably, both GMS and PD-L1 were independent predictors and demonstrated poorly correlated; inclusion of PD-L1 with GMS further improved the predictive capacity for PD-1 blockade immunotherapy.Conclusions Our study highlights the potential predictive value of GMS for immunotherapeutic benefit in non-squamous NSCLC. Besides, the combination of GMS and PD-L1 may serve as an optimal partner in guiding treatment decisions for anti-PD-(L)1 based therapy.https://jitc.bmj.com/content/8/1/e000381.full
spellingShingle Jian Wang
Yi-Long Wu
Xue Bai
De-Hua Wu
Si-Cong Ma
Xin-Ran Tang
Shuai Kang
Qiang John Fu
Chuan-Hui Cao
He-San Luo
Yu-Han Chen
Hong-Bo Zhu
Hong-Hong Yan
Zhong-Yi Dong
Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study
Journal for ImmunoTherapy of Cancer
title Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study
title_full Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study
title_fullStr Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study
title_full_unstemmed Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study
title_short Development and validation of a genomic mutation signature to predict response to PD-1 inhibitors in non-squamous NSCLC: a multicohort study
title_sort development and validation of a genomic mutation signature to predict response to pd 1 inhibitors in non squamous nsclc a multicohort study
url https://jitc.bmj.com/content/8/1/e000381.full
work_keys_str_mv AT jianwang developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT yilongwu developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT xuebai developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT dehuawu developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT sicongma developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT xinrantang developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT shuaikang developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT qiangjohnfu developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT chuanhuicao developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT hesanluo developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT yuhanchen developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT hongbozhu developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT honghongyan developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy
AT zhongyidong developmentandvalidationofagenomicmutationsignaturetopredictresponsetopd1inhibitorsinnonsquamousnsclcamulticohortstudy