Single-cell mass cytometric analysis of peripheral immunity and multiplex plasma marker profiling of non-small cell lung cancer patients receiving PD-1 targeting immune checkpoint inhibitors in comparison with platinum-based chemotherapy

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Abstract

Introduction

The effect of platinum-based chemotherapy (Chem.) and second- or multiple- line immune checkpoint PD-1 blocking therapy by Nivolumab or Pembrolizumab (ICI) was assayed in the peripheral blood of non-small cell lung cancer (NSCLC) patients.

Methods

Flow cytometry was used to detect NSCLC-related antigen binding IgG antibodies. The Luminex MagPix multiplex bead-based cytokine/chemokine detecting system was used to quantitatively measure 17 soluble markers in the plasma samples. Single-cell mass cytometry was applied for the immunophenotyping of peripheral leukocytes.

Results

The incubation of patient derived plasma with human NSCLC tumor cell lines, such as A549, H1975, and H1650, detected NSCLC-specific antibodies reaching a maximum of up to 32% reactive IgG-positive NSCLC cells. The following markers were detected in significantly higher concentration in the plasma of Chem. group versus healthy non-smoker and smoker controls: BTLA, CD27, CD28, CD40, CD80, CD86, GITRL, ICOS, LAG-3, PD-1, PD-L1, and TLR-2. The following markers were detected in significantly higher concentration in the plasma of ICI group versus healthy non-smoker and smoker controls: CD27, CD28, CD40, GITRL, LAG-3, PD-1, PD-L1, and TLR-2. We showed the induction of CD69 and IL-2R on CD4+ CD25+ T-cells upon chemotherapy; the exhaustion of one CD8+ T-cell population was detected by the loss of CD127 and a decrease in CD27. CD19+CD20+, CD79B+, or activated B-cell subtypes showed CD69 increase and downregulation of BTLA, CD27, and IL-2R in NSCLC patients following chemotherapy or ICI.

Discussion

Peripheral immunophenotype caused by chemotherapy or PD-1 blocking was shown in the context of advanced NSCLC.

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Most cited references 53

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Nivolumab versus Docetaxel in Advanced Nonsquamous Non–Small-Cell Lung Cancer

Hossein Borghaei, Luis Paz-Ares, Leora Horn … (2015)

Nivolumab, a fully human IgG4 programmed death 1 (PD-1) immune-checkpoint-inhibitor antibody, disrupts PD-1-mediated signaling and may restore antitumor immunity.

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Nivolumab versus Docetaxel in Advanced Squamous-Cell Non–Small-Cell Lung Cancer

Julie Brahmer, Karen L. Reckamp, Paul Baas … (2015)

New England Journal of Medicine, 373(2), 123-135

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Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial.

Roy S. Herbst, Paul Baas, Dong-Wan Kim … (2016)

Despite recent advances in the treatment of advanced non-small-cell lung cancer, there remains a need for effective treatments for progressive disease. We assessed the efficacy of pembrolizumab for patients with previously treated, PD-L1-positive, advanced non-small-cell lung cancer.

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Author and article information

Contributors

László G. Puskás: URI : https://loop.frontiersin.org/people/549053

Gábor J. Szebeni: URI : https://loop.frontiersin.org/people/545765

Journal

Journal ID (nlm-ta): Front Immunol

Journal ID (iso-abbrev): Front Immunol

Journal ID (publisher-id): Front. Immunol.

Title: Frontiers in Immunology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-3224

Publication date (Electronic): 13 October 2023

Publication date Collection: 2023

Volume: 14

Electronic Location Identifier: 1243233

Affiliations

[1] ¹ Laboratory of Functional Genomics, HUN-REN Biological Research Centre , Szeged, Hungary

[2] ² PhD School in Biology, University of Szeged , Szeged, Hungary

[3] ³ Csongrád County Hospital of Chest Diseases , Deszk, Hungary

[4] ⁴ Department of Pathology, University of Szeged , Szeged, Hungary

[5] ⁵ Department of Surgery, University of Szeged , Szeged, Hungary

[6] ⁶ Avicor Ltd. , Szeged, Hungary

[7] ⁷ Department of Physiology, Anatomy and Neuroscience, Faculty of Science and Informatics, University of Szeged , Szeged, Hungary

[8] ⁸ CS-Smartlab Devices Ltd. , Kozármisleny, Hungary

Author notes

Edited by: Qun Xue, Affiliated Hospital of Nantong University, China

Reviewed by: Jessica Dal Col, University of Salerno, Italy; Isabel Barragan, University of Malaga, Spain

*Correspondence: László G. Puskás, laszlo@ 123456avidinbiotech.com ; Gábor J. Szebeni, szebeni.gabor@ 123456brc.hu

†These authors have contributed equally to this work

Article

DOI: 10.3389/fimmu.2023.1243233

PMC ID: 10611454

PubMed ID: 37901220

SO-VID: 44a51e50-18f6-4729-8e74-c7f5a54afbbd

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 20 June 2023

Date accepted : 27 September 2023

Page count

Figures: 4, Tables: 3, Equations: 0, References: 53, Pages: 14, Words: 7358

Funding

This research was funded by the 2020‐1.1.6‐JÖVŐ−2021‐00003 and 142877 FK22, KFI_16-1-2017-0105 grant from the National Research, Development, and Innovation Office (NKFI), Hungary. This work was supported by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences BO/00582/22/8 (GS) and by the by the ÚNKP-23-5 -SZTE-694 New National Excellence Program of the Ministry for Innovation and Technology (GS). This manuscript was supported by the KDP-2021 Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund for NG (C1764415).

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section-in-acceptance Cancer Immunity and Immunotherapy

ScienceOpen disciplines: Immunology

Keywords: non-small cell lung cancer,platinum-based chemotherapy,pd-1 blocking,nivolumab,pembrolizumab

Data availability:

ScienceOpen disciplines: Immunology

Keywords: non-small cell lung cancer, platinum-based chemotherapy, pd-1 blocking, nivolumab, pembrolizumab

Single-cell mass cytometric analysis of peripheral immunity and multiplex plasma marker profiling of non-small cell lung cancer patients receiving PD-1 targeting immune checkpoint inhibitors in comparison with platinum-based chemotherapy

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Abstract

Introduction

Methods

Results

Discussion

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Most cited references 53

Nivolumab versus Docetaxel in Advanced Nonsquamous Non–Small-Cell Lung Cancer

Nivolumab versus Docetaxel in Advanced Squamous-Cell Non–Small-Cell Lung Cancer

Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial.

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