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@ARTICLE{Sax:301262,
author = {A. Sax and P. May and S. Enssle and N. Soliman and T.
Nedelko and G. Mandracci and F. Stögbauer and L. Joachim
and C. Winter$^*$ and F. Bassermann$^*$ and K. Steiger and
N. El Khawanky and H. Poeck and S. Heidegger},
title = {{D}efects in the necroptosis machinery are a cancer
resistance mechanism to checkpoint inhibitor immunotherapy.},
journal = {Journal for ImmunoTherapy of Cancer},
volume = {13},
number = {5},
issn = {2051-1426},
address = {London},
publisher = {BioMed Central},
reportid = {DKFZ-2025-00947},
pages = {e010433},
year = {2025},
abstract = {Immune checkpoint inhibitors (ICIs) of programmed cell
death protein-1 (PD-1) or cytotoxic T-lymphocytes-associated
protein 4 (CTLA-4) reinvigorate strong polyclonal T-cell
immune responses against tumor cells. For many patients,
these therapies fail because the development of spontaneous
immune responses is often compromised, as the tumor
microenvironment (TME) lacks proinflammatory signals
resulting in suboptimal activation of antigen-presenting
cells (APCs). Necroptosis is a special form of programmed
cell death associated with leakage of inflammatory factors
that can lead to APC maturation. However, it is unclear to
which extent functional necroptosis in tumor cells
contributes to ICI immunotherapy.With genetically engineered
tumor cell lines that lack specific components of the
necroptosis machinery (mixed lineage kinase domain-like
pseudokinase (MLKL), receptor interacting protein kinase 3
(RIPK3)), we addressed the importance of necroptotic tumor
cell death for the efficacy of ICI immunotherapy in murine
models. Preclinical data were aligned with genome-wide
transcriptional programs in patient tumor samples at
diagnosis and during ICI treatment for the activity of these
pathways and association with treatment outcome.Mice bearing
MLKL-deficient or RIPK3-deficient tumors failed to control
tumor growth in response to anti-PD-1/anti-CTLA-4
immunotherapy. Mechanistically, defects in the necroptosis
pathway resulted in reduced tumor antigen cross-presentation
by type 1 conventional dendritic cells (DCs) in
tumor-draining lymph nodes, and subsequently impaired
immunotherapy-induced expansion of circulating tumor
antigen-specific CD8+ T cells and their accumulation and
activation in the TME. In vitro, co-culture of tumor cells
undergoing necroptotic but not apoptotic programmed cell
death resulted in increased uptake by phagocytic cells,
associated with maturation and activation of DCs. Treatment
of tumors with the epigenetic modulator azacytidine enhanced
intrinsic transcriptional activity of the necroptosis
machinery, and hence their susceptibility to ICI
immunotherapy. In humans, transcriptome analysis of melanoma
samples revealed a strong association between high
expression of MLKL and prolonged overall survival and
durable clinical response to immunotherapy with anti-PD-1
and/or anti-CTLA-4 checkpoint inhibitors.Defective
necroptosis signaling in tumor cells is a cancer resistance
mechanism to ICI immunotherapy. Reversion of epigenetic
silencing of the necroptosis pathway can render tumors
susceptible to checkpoint inhibition.},
keywords = {Necroptosis: drug effects / Animals / Immune Checkpoint
Inhibitors: pharmacology / Immune Checkpoint Inhibitors:
therapeutic use / Humans / Mice / Immunotherapy: methods /
Drug Resistance, Neoplasm / Neoplasms: drug therapy /
Neoplasms: immunology / Tumor Microenvironment / Cell Line,
Tumor / Immune Checkpoint Inhibitor (Other) / Immunotherapy
(Other) / T cell (Other) / Tumor microenvironment - TME
(Other) / Immune Checkpoint Inhibitors (NLM Chemicals)},
cin = {MU01},
ddc = {610},
cid = {I:(DE-He78)MU01-20160331},
pnm = {899 - ohne Topic (POF4-899)},
pid = {G:(DE-HGF)POF4-899},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:40345706},
doi = {10.1136/jitc-2024-010433},
url = {https://inrepo02.dkfz.de/record/301262},
}