S100A9 and HMGB1 orchestrate MDSC-mediated immunosuppression in melanoma through TLR4 signaling.


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:
11 Sep 2024
Historique:
accepted: 01 08 2024
medline: 13 9 2024
pubmed: 13 9 2024
entrez: 12 9 2024
Statut: epublish

Résumé

Immunotherapies for malignant melanoma are challenged by the resistance developed in a significant proportion of patients. Myeloid-derived suppressor cells (MDSC), with their ability to inhibit antitumor T-cell responses, are a major contributor to immunosuppression and resistance to immune checkpoint therapies in melanoma. Damage-associated molecular patterns S100A8, S100A9, and HMGB1, acting as toll like receptor 4 (TLR4) and receptor for advanced glycation endproducts (RAGE) ligands, are highly expressed in the tumor microenvironment and drive MDSC activation. However, the role of TLR4 and RAGE signaling in the acquisition of MDSC immunosuppressive properties remains to be better defined. Our study investigates how the signaling via TLR4 and RAGE as well as their ligands S100A9 and HMGB1, shape MDSC-mediated immunosuppression in melanoma. MDSC were isolated from the peripheral blood of patients with advanced melanoma or generated in vitro from healthy donor-derived monocytes. Monocytes were treated with S100A9 or HMGB1 for 72 hours. The immunosuppressive capacity of treated monocytes was assessed in the inhibition of T-cell proliferation assay in the presence or absence of TLR4 and RAGE inhibitors. Plasma levels of S100A8/9 and HMGB1 were quantified by ELISA. Single-cell RNA sequencing (scRNA-seq) was performed on monocytes from patients with melanoma and healthy donors. We showed that exposure to S100A9 and HMGB1 converted healthy donor-derived monocytes into MDSC through TLR4 signaling. Our scRNA-seq data revealed in patient monocytes enriched inflammatory genes, including These findings highlight the critical role of TLR4 and, to a lesser extent, RAGE signaling in the conversion of monocytes into MDSC-like cells, underscore the potential of targeting S100A9 to prevent this conversion, and highlight the prognostic value of S100A8/9 as a plasma biomarker in melanoma.

Sections du résumé

BACKGROUND BACKGROUND
Immunotherapies for malignant melanoma are challenged by the resistance developed in a significant proportion of patients. Myeloid-derived suppressor cells (MDSC), with their ability to inhibit antitumor T-cell responses, are a major contributor to immunosuppression and resistance to immune checkpoint therapies in melanoma. Damage-associated molecular patterns S100A8, S100A9, and HMGB1, acting as toll like receptor 4 (TLR4) and receptor for advanced glycation endproducts (RAGE) ligands, are highly expressed in the tumor microenvironment and drive MDSC activation. However, the role of TLR4 and RAGE signaling in the acquisition of MDSC immunosuppressive properties remains to be better defined. Our study investigates how the signaling via TLR4 and RAGE as well as their ligands S100A9 and HMGB1, shape MDSC-mediated immunosuppression in melanoma.
METHODS METHODS
MDSC were isolated from the peripheral blood of patients with advanced melanoma or generated in vitro from healthy donor-derived monocytes. Monocytes were treated with S100A9 or HMGB1 for 72 hours. The immunosuppressive capacity of treated monocytes was assessed in the inhibition of T-cell proliferation assay in the presence or absence of TLR4 and RAGE inhibitors. Plasma levels of S100A8/9 and HMGB1 were quantified by ELISA. Single-cell RNA sequencing (scRNA-seq) was performed on monocytes from patients with melanoma and healthy donors.
RESULTS RESULTS
We showed that exposure to S100A9 and HMGB1 converted healthy donor-derived monocytes into MDSC through TLR4 signaling. Our scRNA-seq data revealed in patient monocytes enriched inflammatory genes, including
CONCLUSIONS CONCLUSIONS
These findings highlight the critical role of TLR4 and, to a lesser extent, RAGE signaling in the conversion of monocytes into MDSC-like cells, underscore the potential of targeting S100A9 to prevent this conversion, and highlight the prognostic value of S100A8/9 as a plasma biomarker in melanoma.

Identifiants

pubmed: 39266214
pii: jitc-2024-009552
doi: 10.1136/jitc-2024-009552
pii:
doi:

Substances chimiques

Calgranulin B 0
Toll-Like Receptor 4 0
HMGB1 Protein 0
S100A9 protein, human 0
TLR4 protein, human 0
HMGB1 protein, human 0

Types de publication

Journal Article

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: None declared.

Auteurs

Feyza Gül Özbay Kurt (FG)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.
DKFZ-Hector Cancer Institute at the University Medical Center Mannheim, Mannheim, Germany.
Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Beatrice-Ana Cicortas (BA)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.
DKFZ-Hector Cancer Institute at the University Medical Center Mannheim, Mannheim, Germany.
Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Bianca M Balzasch (BM)

Department of Immunobiochemistry, Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Carolina De la Torre (C)

NGS Core Facility, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Volker Ast (V)

NGS Core Facility, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Ece Tavukcuoglu (E)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.

Cagla Ak (C)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.
DKFZ-Hector Cancer Institute at the University Medical Center Mannheim, Mannheim, Germany.
Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Sebastian A Wohlfeil (SA)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.

Adelheid Cerwenka (A)

Department of Immunobiochemistry, Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Jochen Utikal (J)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.
DKFZ-Hector Cancer Institute at the University Medical Center Mannheim, Mannheim, Germany.
Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

Viktor Umansky (V)

Skin Cancer Unit, German Cancer Research Center, Heidelberg, Germany V.Umansky@dkfz-heidelberg.de.
Department of Dermatology Venereology and Allergology, University Medical Centre Mannheim, Heidelberg University, Mannheim, Germany.
DKFZ-Hector Cancer Institute at the University Medical Center Mannheim, Mannheim, Germany.
Mannheim Institute for Innate Immunoscience (MI3), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.

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