Distinctive germline expression of class I human leukocyte antigen (HLA) alleles and DRB1 heterozygosis predict the outcome of patients with non-small cell lung cancer receiving PD-1/PD-L1 immune checkpoint blockade.


Journal

Journal for immunotherapy of cancer
ISSN: 2051-1426
Titre abrégé: J Immunother Cancer
Pays: England
ID NLM: 101620585

Informations de publication

Date de publication:
06 2020
Historique:
accepted: 05 05 2020
entrez: 20 6 2020
pubmed: 20 6 2020
medline: 21 8 2021
Statut: ppublish

Résumé

Nivolumab is a human monoclonal antibody against programmed cell death receptor-1 (PD-1) able to rescue quiescent tumor infiltrating cytotoxic T lymphocytes (CTLs) restoring their ability to kill target cells expressing specific tumor antigen-derived epitope peptides bound to homologue human leukocyte antigen (HLA) molecules. Nivolumab is currently an active but expensive therapeutic agent for metastatic non-small cell lung cancer (mNSCLC), producing, in some cases, immune-related adverse events (irAEs). At the present, no reliable biomarkers have been validated to predict either treatment response or adverse events in treated patients. We performed a retrospective multi-institutional analysis including 119 patients with mNSCLC who received PD-1 blockade since November 2015 to investigate the predictive role of germinal class I HLA and DRB1 genotype. We investigated the correlation among patients' outcome and irAEs frequency with specific HLA A, B, C and DRB1 alleles by reverse sequence-specific oligonucleotide (SSO) DNA typing. A poor outcome in patients negative for the expression of two most frequent HLA-A alleles was detected (HLA: HLA-A*01 and or A*02; progression-free survival (PFS): 7.5 (2.8 to 12.2) vs 15.9 (0 to 39.2) months, p=0.01). In particular, HLA-A*01-positive patients showed a prolonged PFS of 22.6 (10.2 to 35.0) and overall survival (OS) of 30.8 (7.7 to 53.9) months, respectively. We also reported that HLA-A and DRB1 locus heterozygosis (het) were correlated to a worse OS if we considered het in the locus A; in reverse, long survival was correlated to het in DRB1. This study demonstrate that class I and II HLA allele characterization to define tumor immunogenicity has relevant implications in predicting nivolumab efficacy in mNSCLC and provide the rationale for further prospective trials of cancer immunotherapy.

Sections du résumé

BACKGROUND
Nivolumab is a human monoclonal antibody against programmed cell death receptor-1 (PD-1) able to rescue quiescent tumor infiltrating cytotoxic T lymphocytes (CTLs) restoring their ability to kill target cells expressing specific tumor antigen-derived epitope peptides bound to homologue human leukocyte antigen (HLA) molecules. Nivolumab is currently an active but expensive therapeutic agent for metastatic non-small cell lung cancer (mNSCLC), producing, in some cases, immune-related adverse events (irAEs). At the present, no reliable biomarkers have been validated to predict either treatment response or adverse events in treated patients.
METHODS
We performed a retrospective multi-institutional analysis including 119 patients with mNSCLC who received PD-1 blockade since November 2015 to investigate the predictive role of germinal class I HLA and DRB1 genotype. We investigated the correlation among patients' outcome and irAEs frequency with specific HLA A, B, C and DRB1 alleles by reverse sequence-specific oligonucleotide (SSO) DNA typing.
RESULTS
A poor outcome in patients negative for the expression of two most frequent HLA-A alleles was detected (HLA: HLA-A*01 and or A*02; progression-free survival (PFS): 7.5 (2.8 to 12.2) vs 15.9 (0 to 39.2) months, p=0.01). In particular, HLA-A*01-positive patients showed a prolonged PFS of 22.6 (10.2 to 35.0) and overall survival (OS) of 30.8 (7.7 to 53.9) months, respectively. We also reported that HLA-A and DRB1 locus heterozygosis (het) were correlated to a worse OS if we considered het in the locus A; in reverse, long survival was correlated to het in DRB1.
CONCLUSIONS
This study demonstrate that class I and II HLA allele characterization to define tumor immunogenicity has relevant implications in predicting nivolumab efficacy in mNSCLC and provide the rationale for further prospective trials of cancer immunotherapy.

Identifiants

pubmed: 32554614
pii: jitc-2020-000733
doi: 10.1136/jitc-2020-000733
pmc: PMC7304840
pii:
doi:

Substances chimiques

HLA Antigens 0
Immune Checkpoint Inhibitors 0

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Déclaration de conflit d'intérêts

Competing interests: None declared.

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Auteurs

Pierpaolo Correale (P)

Medical Oncology Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy michele.caraglia@unicampania.it correalep@yahoo.com.

Rita Emilena Saladino (RE)

Tissue Typing Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Diana Giannarelli (D)

Regina Elena National Cancer Institute, IRCCS, Rome, Italy.

Rocco Giannicola (R)

Medical Oncology Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Rita Agostino (R)

Medical Oncology Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Nicoletta Staropoli (N)

Medical and Translational Oncology Unit, Department of Experimental and Clinical Medicine, Magna Graecia University, Catanzaro, Italy.

Alessandra Strangio (A)

Medical Oncology Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Teresa Del Giudice (T)

Medical and Translational Oncology Unit, Department of Experimental and Clinical Medicine, Magna Graecia University, Catanzaro, Italy.

Valerio Nardone (V)

Radiotherapy Unit, "Ospedale del Mare", ASL Napoli 1, Naples, Italy.

Maria Altomonte (M)

Unit of Pharmacy, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Pierpaolo Pastina (P)

Section of Radiation Oncology, Medical School, University of Siena, Siena, Italy.

Paolo Tini (P)

Section of Radiation Oncology, Medical School, University of Siena, Siena, Italy.

Antonia Consuelo Falzea (AC)

Medical Oncology Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Natale Imbesi (N)

Tissue Typing Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Valentina Arcati (V)

Tissue Typing Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Giuseppa Romeo (G)

Tissue Typing Unit, Grand Metropolitan Hospital "Bianchi-Melacrino-Morelli", Reggio Calabria, Italy.

Daniele Caracciolo (D)

Medical and Translational Oncology Unit, Department of Experimental and Clinical Medicine, Magna Graecia University, Catanzaro, Italy.

Amalia Luce (A)

Department of Precision Medicine, University of Campania "L. Vanvitelli", Naples, Italy.

Michele Caraglia (M)

Department of Precision Medicine, University of Campania "L. Vanvitelli", Naples, Italy michele.caraglia@unicampania.it correalep@yahoo.com.
Biogem Scarl, Institute of Genetic Research, Laboratory of Precision and Molecular Oncology, Ariano Irpino, Avellino, Italy.

Antonio Giordano (A)

Sbarro Institute for Cancer Research and Molecular Medicine and Center of Biotechnology, College of Science and Technology, Temple University, Philadelphia, Pennsylvania, USA.
Department of Medical Biotechnology, University of Siena, Siena, Italy.

Luigi Pirtoli (L)

Sbarro Institute for Cancer Research and Molecular Medicine and Center of Biotechnology, College of Science and Technology, Temple University, Philadelphia, Pennsylvania, USA.

Alois Necas (A)

Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic.

Evzen Amler (E)

Department of Biophysics, 2nd Faculty of Medicine, Charles University in Prague, Prague, Czech Republic.

Vito Barbieri (V)

Medical and Translational Oncology Unit, Department of Experimental and Clinical Medicine, Magna Graecia University, Catanzaro, Italy.

Pierfrancesco Tassone (P)

Medical and Translational Oncology Unit, Department of Experimental and Clinical Medicine, Magna Graecia University, Catanzaro, Italy.
Sbarro Institute for Cancer Research and Molecular Medicine and Center of Biotechnology, College of Science and Technology, Temple University, Philadelphia, Pennsylvania, USA.

Pierosandro Tagliaferri (P)

Medical and Translational Oncology Unit, Department of Experimental and Clinical Medicine, Magna Graecia University, Catanzaro, Italy.

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