Favorable impact of PD1/PD-L1 antagonists on bone remodeling: an exploratory prospective clinical study and ex vivo validation.


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:
03 May 2024
Historique:
accepted: 19 04 2024
medline: 4 5 2024
pubmed: 4 5 2024
entrez: 3 5 2024
Statut: epublish

Résumé

Skeletal morbidity in patients with cancer has a major impact on the quality of life, and preserving bone health while improving outcomes is an important goal of modern antitumor treatment strategies. Despite their widespread use in early disease stages, the effects of immune checkpoint inhibitors (ICIs) on the skeleton are still poorly defined. Here, we initiated a comprehensive investigation of the impact of ICIs on bone health by longitudinal assessment of bone turnover markers in patients with cancer and by validation in a novel bioengineered 3D model of bone remodeling. An exploratory longitudinal study was conducted to assess During the first month of treatment, CTX levels decreased sharply but transiently. In contrast, we observed a delayed increase of serum levels of PINP and OCN after 4 months of therapy. In vitro, ICIs impaired the maturation of preosteoclasts by inhibiting STAT3/NFATc1 signaling but not JNK, ERK, and AKT while lacking any direct effect on osteogenesis. However, using our bioengineered 3D bone model, which enables the simultaneous differentiation of OB and OC precursor cells, we confirmed the uncoupling of the OC/OB activity on exposure to ICIs by demonstrating impaired OC maturation along with increased OB differentiation. Our study indicates that the inhibition of the PD1/PD-L1 signaling axis interferes with bone turnover and may exert a protective effect on bone by indirectly promoting osteogenesis.

Sections du résumé

BACKGROUND BACKGROUND
Skeletal morbidity in patients with cancer has a major impact on the quality of life, and preserving bone health while improving outcomes is an important goal of modern antitumor treatment strategies. Despite their widespread use in early disease stages, the effects of immune checkpoint inhibitors (ICIs) on the skeleton are still poorly defined. Here, we initiated a comprehensive investigation of the impact of ICIs on bone health by longitudinal assessment of bone turnover markers in patients with cancer and by validation in a novel bioengineered 3D model of bone remodeling.
METHODS METHODS
An exploratory longitudinal study was conducted to assess
RESULTS RESULTS
During the first month of treatment, CTX levels decreased sharply but transiently. In contrast, we observed a delayed increase of serum levels of PINP and OCN after 4 months of therapy. In vitro, ICIs impaired the maturation of preosteoclasts by inhibiting STAT3/NFATc1 signaling but not JNK, ERK, and AKT while lacking any direct effect on osteogenesis. However, using our bioengineered 3D bone model, which enables the simultaneous differentiation of OB and OC precursor cells, we confirmed the uncoupling of the OC/OB activity on exposure to ICIs by demonstrating impaired OC maturation along with increased OB differentiation.
CONCLUSION CONCLUSIONS
Our study indicates that the inhibition of the PD1/PD-L1 signaling axis interferes with bone turnover and may exert a protective effect on bone by indirectly promoting osteogenesis.

Identifiants

pubmed: 38702145
pii: jitc-2023-008669
doi: 10.1136/jitc-2023-008669
pii:
doi:

Substances chimiques

Immune Checkpoint Inhibitors 0
Programmed Cell Death 1 Receptor 0
B7-H1 Antigen 0
CD274 protein, human 0
PDCD1 protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© Author(s) (or their employer(s)) 2024. 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: KP has received speaker’s honoraria from Celgene, Amgen Inc, and Janssen Pharmaceuticals; consultancy fees from Celgene, Takeda, Janssen Pharmaceuticals, and Amgen; and research support from Roche Pharmaceuticals. SV has received speaker's honoraria from Bristol Myers Squibb, Pfizer, MSD, and Merck; consultancy fees from Roche, MSD, EUSA Pharma, and Merck; and travel support from Pfizer, Roche, Pierre Fabre, and Angelini.

Auteurs

Tamara Gassner (T)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Christina Chittilappilly (C)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Theo Pirich (T)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Benjamin Neuditschko (B)

Institute Krems Bioanalytics, IMC University of Applied Sciences, Krems an der Donau, Austria.

Klaus Hackner (K)

Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.
Division of Pneumology, University Hospital Krems, Krems an der Donau, Austria.

Judith Lind (J)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Osman Aksoy (O)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Uwe Graichen (U)

Department of General Health Studies, Division Biostatistics and Data Sciences, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Sascha Klee (S)

Department of General Health Studies, Division Biostatistics and Data Sciences, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.

Franz Herzog (F)

Institute Krems Bioanalytics, IMC University of Applied Sciences, Krems an der Donau, Austria.

Christoph Wiesner (C)

Department of Medical and Pharmaceutical Biotechnology, IMC University of Applied Sciences, Krems an der Donau, Austria.

Peter Errhalt (P)

Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.
Division of Pneumology, University Hospital Krems, Krems an der Donau, Austria.

Martin Pecherstorfer (M)

Division of Internal Medicine 2, University Hospital Krems, Krems an der Donau, Austria.
Karl Landsteiner Institute of Supportive Cancer Therapy, Karl Landsteiner Gesellschaft, St. Poelten, Austria.

Klaus Podar (K)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria.
Division of Internal Medicine 2, University Hospital Krems, Krems an der Donau, Austria.

Sonia Vallet (S)

Department of Basic and Translational Oncology and Hematology, Division of Molecular Oncology and Hematology, Karl Landsteiner University of Health Sciences, Krems an der Donau, Austria sonia.vallet@krems.lknoe.at.
Division of Internal Medicine 2, University Hospital Krems, Krems an der Donau, Austria.
Karl Landsteiner Institute of Supportive Cancer Therapy, Karl Landsteiner Gesellschaft, St. Poelten, Austria.

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