Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer

Background Napsin A is normally expressed in human lung pneumocytes and is a highly expressed cancer antigen in lung adenocarcinoma. We examined whether T cells specific for Napsin A may play a role in immune checkpoint inhibitor (ICI)-mediated responses. We used bulk T-cell receptor (TCR) repertoir...

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Main Authors: Crystal Mackall, Heather Wakelee, Sylvia Lee, Keith D Eaton, Cristina Rodriguez, Rafael Santana-Davila, Joel W Neal, Natalie J Miller, Elena Sotillo, Tatyana Pisarenko, Eric Q Konnick, Christina Baik, Fangdi Sun, Renato G Martins, Sukhmani K Padda, Alex Camai, Viswam S Nair, A McGarry Houghton, Shin-Heng Chiou, Diane Tseng
Format: Article
Language:English
Published: BMJ Publishing Group 2025-07-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/13/7/e011907.full
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author Crystal Mackall
Heather Wakelee
Sylvia Lee
Keith D Eaton
Cristina Rodriguez
Rafael Santana-Davila
Joel W Neal
Natalie J Miller
Elena Sotillo
Tatyana Pisarenko
Eric Q Konnick
Christina Baik
Fangdi Sun
Renato G Martins
Sukhmani K Padda
Alex Camai
Viswam S Nair
A McGarry Houghton
Shin-Heng Chiou
Diane Tseng
author_facet Crystal Mackall
Heather Wakelee
Sylvia Lee
Keith D Eaton
Cristina Rodriguez
Rafael Santana-Davila
Joel W Neal
Natalie J Miller
Elena Sotillo
Tatyana Pisarenko
Eric Q Konnick
Christina Baik
Fangdi Sun
Renato G Martins
Sukhmani K Padda
Alex Camai
Viswam S Nair
A McGarry Houghton
Shin-Heng Chiou
Diane Tseng
author_sort Crystal Mackall
collection DOAJ
description Background Napsin A is normally expressed in human lung pneumocytes and is a highly expressed cancer antigen in lung adenocarcinoma. We examined whether T cells specific for Napsin A may play a role in immune checkpoint inhibitor (ICI)-mediated responses. We used bulk T-cell receptor (TCR) repertoire data to assess whether the presence of Napsin A-specific clonotypes in the peripheral blood was associated with improved clinical responses to ICI.Methods Patients with metastatic non-small cell lung cancer (NSCLC) receiving anti-programmed cell death protein 1 (PD-1) and/or programmed death-ligand 1 (PD-L1) were enrolled at Fred Hutchinson Cancer Center and Stanford University Medical Center (n=62; histology of adenocarcinoma n=48, squamous n=9, NSCLC/other n=5). Peripheral blood mononuclear cells were collected for genomic DNA isolation at one pretreatment and one post-treatment time point (range 3 weeks to 3 months). TCRβ was bulk sequenced via the immunoSEQ platform (Adaptive Biotechnologies). Napsin A-specific TCRβ sequences were identified from publicly available data and their frequencies were quantified in each patient sample. We examined whether overall survival (OS) and progression-free survival (PFS) outcomes differed in patients with or without detectable Napsin A-specific TCRs (herein Napsin TCRs). We used Cox proportional hazards regression to assess the association between detectable Napsin TCRs and PFS or OS in univariable and multivariable analyses.Results Napsin TCRs were detectable in the blood in a large fraction of our cohort (n=25/62 (40%) pretreatment; n=21/42 (50%) post-treatment). Patients with detectable Napsin TCRs had a significant improvement in OS compared with patients without these TCRs (median OS 45.4 vs 14.8 months, p=0.0043 pretreatment; median OS 55.4 vs 18.9 months, p=0.0066 post-treatment). Among 27 HLA-A*02 carriers of 55 human leukocyte antigen-typed patients (49%), patients with detectable pretreatment Napsin TCRs had a significant improvement in OS (median 60.2 vs 16.5 months, p=0.0054) and PFS (median 21.5 vs 7.2 months, p=0.031) compared with patients without these TCRs. In univariate and multivariate analysis, the presence of Napsin TCRs pretreatment was associated with improved OS (p=0.0057, HR 0.40, 95% CI 0.21 to 0.76 univariate; p=0.033, HR 0.45, 95% CI 0.23 to 0.91 multivariate).Conclusions Napsin TCRs are frequently detected in patients with NSCLC and are associated with improved OS in patients with NSCLC receiving ICI.
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spelling doaj-art-d2c45fe7eb2c4d87a2ba7aac15c351462025-08-20T03:50:38ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262025-07-0113710.1136/jitc-2025-011907Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancerCrystal Mackall0Heather Wakelee1Sylvia Lee2Keith D Eaton3Cristina Rodriguez4Rafael Santana-Davila5Joel W Neal6Natalie J Miller7Elena Sotillo8Tatyana Pisarenko9Eric Q Konnick10Christina Baik11Fangdi Sun12Renato G Martins13Sukhmani K Padda14Alex Camai15Viswam S Nair16A McGarry Houghton17Shin-Heng Chiou18Diane Tseng197 Medicine and Pediatrics, Stanford University, Stanford, California, USA3 Department of Medicine, Stanford University, Stanford, California, USA1 University of Washington, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA3 Department of Medicine, Stanford University, Stanford, California, USA1 University of Washington, Seattle, Washington, USA6 Center for Cancer Cell Therapy, Stanford Cancer Institute, Stanford, California, USA2 Fred Hutchinson Cancer Center, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA3 Department of Medicine, Stanford University, Stanford, California, USA4 Virginia Commonwealth University, Richmond, Virginia, USA5 Fox Chase Cancer Center, Philadelphia, Pennsylvania, USA2 Fred Hutchinson Cancer Center, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA1 University of Washington, Seattle, Washington, USA8 Medicine, Rutgers Cancer Institute, New Brunswick, New Jersey, USA1 University of Washington, Seattle, Washington, USABackground Napsin A is normally expressed in human lung pneumocytes and is a highly expressed cancer antigen in lung adenocarcinoma. We examined whether T cells specific for Napsin A may play a role in immune checkpoint inhibitor (ICI)-mediated responses. We used bulk T-cell receptor (TCR) repertoire data to assess whether the presence of Napsin A-specific clonotypes in the peripheral blood was associated with improved clinical responses to ICI.Methods Patients with metastatic non-small cell lung cancer (NSCLC) receiving anti-programmed cell death protein 1 (PD-1) and/or programmed death-ligand 1 (PD-L1) were enrolled at Fred Hutchinson Cancer Center and Stanford University Medical Center (n=62; histology of adenocarcinoma n=48, squamous n=9, NSCLC/other n=5). Peripheral blood mononuclear cells were collected for genomic DNA isolation at one pretreatment and one post-treatment time point (range 3 weeks to 3 months). TCRβ was bulk sequenced via the immunoSEQ platform (Adaptive Biotechnologies). Napsin A-specific TCRβ sequences were identified from publicly available data and their frequencies were quantified in each patient sample. We examined whether overall survival (OS) and progression-free survival (PFS) outcomes differed in patients with or without detectable Napsin A-specific TCRs (herein Napsin TCRs). We used Cox proportional hazards regression to assess the association between detectable Napsin TCRs and PFS or OS in univariable and multivariable analyses.Results Napsin TCRs were detectable in the blood in a large fraction of our cohort (n=25/62 (40%) pretreatment; n=21/42 (50%) post-treatment). Patients with detectable Napsin TCRs had a significant improvement in OS compared with patients without these TCRs (median OS 45.4 vs 14.8 months, p=0.0043 pretreatment; median OS 55.4 vs 18.9 months, p=0.0066 post-treatment). Among 27 HLA-A*02 carriers of 55 human leukocyte antigen-typed patients (49%), patients with detectable pretreatment Napsin TCRs had a significant improvement in OS (median 60.2 vs 16.5 months, p=0.0054) and PFS (median 21.5 vs 7.2 months, p=0.031) compared with patients without these TCRs. In univariate and multivariate analysis, the presence of Napsin TCRs pretreatment was associated with improved OS (p=0.0057, HR 0.40, 95% CI 0.21 to 0.76 univariate; p=0.033, HR 0.45, 95% CI 0.23 to 0.91 multivariate).Conclusions Napsin TCRs are frequently detected in patients with NSCLC and are associated with improved OS in patients with NSCLC receiving ICI.https://jitc.bmj.com/content/13/7/e011907.full
spellingShingle Crystal Mackall
Heather Wakelee
Sylvia Lee
Keith D Eaton
Cristina Rodriguez
Rafael Santana-Davila
Joel W Neal
Natalie J Miller
Elena Sotillo
Tatyana Pisarenko
Eric Q Konnick
Christina Baik
Fangdi Sun
Renato G Martins
Sukhmani K Padda
Alex Camai
Viswam S Nair
A McGarry Houghton
Shin-Heng Chiou
Diane Tseng
Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer
Journal for ImmunoTherapy of Cancer
title Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer
title_full Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer
title_fullStr Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer
title_full_unstemmed Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer
title_short Napsin A-specific T-cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non-small cell lung cancer
title_sort napsin a specific t cell clonotypes are associated with improved clinical outcomes in patients receiving checkpoint immunotherapy for metastatic non small cell lung cancer
url https://jitc.bmj.com/content/13/7/e011907.full
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