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Immune-checkpoint blockade lacks anti-tumorgenicity in NASH-induced HCC

UID: 10667

Author(s): Pfister, Dominik, Núñez, Nicolás Gonzalo, Pinyol, Roser, Govaere, Olivier, Pinter, Matthias, Szydlowska, Marta, Gupta, Revant, Qiu, Mengjie, Deczkowska, Aleksandra, Weiner, Assaf, Müller, Florian, Yousuf, Suhail, Sinha, Ankit, Friebel, Ekaterina, Engleitner, Thomas, Lenggenhager, Daniela, Heide , Danijela, Moncsek, Anja, Stirm, Kristin, Kosla, Jan, Prokosch, Sandra, Rothermel, Ulrike, Dudek, Michael, O'Connor, Tracy, Kotsiliti, Eleni, Leone, Valentina, Inverso, Donato, Jansen, Jitske, Singh, Indrabahadur, Yabal, Monica, Castet, Florian, Montironi, Carla*, Haber, Philipp K, Torrecilla, Sara, Eichwald, Viktoria, Jugold, Manfred, Öllinger, Rupert, Matter, Maurice, Terracciano, Luigi M, Tiniakos, Dina, Bedossa, Pierre, Cockell, Simon, Younes, Ramy, Vacca, Michele, Marra, Fabio, Schattenberg, Jörn M., Allison, Michael, Bugianesi, Elisabetta, Ratziu, Vlad, Daly, Ann K, Scheiner, Bernhard, Pomej, Katharina, Kirstein, Martha M, Vogel, Arndt, Peck-Radosavljevic, Markus, Hucke, Florian, Finkelmeier, Fabian, Waidmann, Oliver, Trojan, Jörg, Schulze, Kornelius, Wege, Henning, Koch, Sandra, Weinmann, Arndt, Bueter, Marco, Rössler, Fabian, Schmid, Johannes A, Müllhaupt, Beat, Kaeser, Rafael, Boettler, Tobias, Thimme, Robert, Siebenhüner, Alexander, De Dosso, Sara, Augustin, Hellmut G, Schietinger, Andrea*, Groth, Christopher, Umansky, Viktor, Billeter, Adrian, Müller-Stich, Beat, Mallm, Jan-Philipp, Mei, Henrik E, Schultz, Axel R., Luedde, Tom, Ringelhan, Marc*, Malek, Nisar, Spahn , Stephan, Bitzer, Michael, Rahbari, Nuh, Dufour, Jean-Francois, Pinato, David J, Marron, Thomas U, Kaseb, Ahmed, Kudo, Masatoshi, Huang, Yi-Hsiang, Knolle, Percy, Roth, Susanne, Weber, Achim, Decaens, Thomas, Jilkova, Zuzana M., Rad, Roland, Mertens, Joachim C, Unger, Kristian, Meissner, Felix, Claassen, Manfred, Anstee, Quentin M, Amit, Ido, Becher, Burkhard, Llovet, Josep M., Heikenwälder, Mathias * MSK affiliated

Description
Summary from the GEO: "Hepatocellular carcinoma (HCC) has dismal treatment responses to systemic therapies and is caused by both, viral and non-viral etiologies, including non-alcoholic steatohepatitis (NASH) 1–5. NASH - triggered by high caloric intake and sedentary lifestyle - has become an important driver for HCC development. Immunotherapy has been recently approved for HCC but stratification of responders versus non-responders has remained an unmet need 5–8. Here, we found a progressive accumulation of non-classical activated CD8+PD-1+ T-cells in livers of NASH-affected patients and mice. PD-L1/PD-1-targeted immunotherapy of NASH-induced HCC administered either at cancer-initiation or after cancer-establishment lacked beneficial effects in mice. On the contrary, PD-1-targeted immunotherapy drove hepatic necro-inflammation and increased liver cancer incidence, tumor number, and nodule size. Anti-CD8 or anti-CD8/anti-NK1.1 treatment suppressed liver cancer development, implicating CD8+ T-cells as liver cancer drivers in the context of NASH. In line, PD-1-/- mice challenged with a NASH-inducing diet displayed early-onset of liver cancer. Mechanistically, PD-1-targeted immunotherapy triggered necro-inflammation and a pro-tumorigenic environment in the context of NASH, increasing the abundance of hepatic TOX+CXCR6+ expressing CD8+PD-1+ TNF+ T-cells. Anti-CD8/anti-PD-1 or anti-TNF/anti-PD-1, but not anti-CD4/anti-PD-1 treatment reverted anti-PD1 treatment-related increase of liver inflammation, NASH severity and tumorigenesis. Gene expression profile and increased abundance of murine hepatic CD8+PD-1+ T-cells were corroborated in human CD8+PD-1+ T cells derived from NASH patients. In a meta-analysis of clinical trials testing PD-1-targeting immune checkpoint inhibitors alone (i.e. pembrolizumab) or in combination in 1656 patients with advanced HCC, immunotherapy was not favorable over to control treatment in non-viral- when compared to viral-related HCC. Similarly, in two clinical cohorts tested, patients with NASH-driven HCC had a significantly worse overall survival with PD-1-targeted immunotherapy than HCC patients with other etiologies. Our data identify non-viral etiologies, particularly NASH, as potentially non-responsive in the context of HCC immunotherapy, providing a strong rational basis for patient stratification."

Overall design from the GEO: "mRNA profiles of liver tissues from 10 patients with different pathological characteristics"
Subject of Study
Subject(s)
OncoTree Cancer Type(s)
Hepatocellular Carcinoma
Access via GEO

CSV, MTX, TSV files of expression profiling by high throughput sequencing
Accession #: GSE159977

Access via SRA

RNA Sequence reads for 10 samples
Accession #: SRP288365

Access via BioProject

Additional information about overall initiative.
Accession #: PRJNA671310

Access Restrictions
Free to All
Access Instructions
The NCBI Gene Expression Omnibus, SRA, and BioProject databases provide open access to these files.
Associated Publications
Data Type
Equipment Used
Illumina NovaSeq 6000
Software Used
SRA Toolkit
Dataset Format(s)
CSV, TSV, SRA, MTX
Data Tool(s)
RNA Seq
Dataset Size
965.6 Mb (TAR of MTX, TSV), 513.5 Mb (CSV), 146.1 GB (SRA)
Data Catalog Record Updated
2023-12-07