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            <funder>This work was supported by INCa (PRT-K 19-033, PLBIO 23-031), La Ligue contre le cancer (France, Comité du Rhône, #R19147CC), financial support from ITMO Cancer of Aviesan within the framework of the 2021-2030 Cancer Control Strategy, on funds administered by Inserm (PCSI call), and the DevWeCan Laboratories of Excellence network (ANR-LABX-061) and the French National Research Agency (ANR) within the framework of the IHU EVEREST (ANR-23-IAHU-0008) as part of the program “Investissements d’Avenir”. AARS is the recipient of an ANRS grant (ECTZ206376). IC is the recipient of an ANRS predoctoral fellowship (ECTZ63958). JML is supported by grants from the European Commission (Horizon Europe-Mission Cancer, THRIVE, Ref. 101136622), by an Accelerator Award from Cancer Research UK, Fondazione per la Ricerca sul Cancro (AIRC) and Fundación Científica de la Asociación Española Contra el Cáncer (FAECC) (HUNTER, Ref. C9380/A26813), by the NIH (R01-CA273932-01, RO1DK56621 and RO1DK128289), the Samuel Waxman Cancer Research Foundation, by the Spanish National Health Institute (Project PID2022-139365OB-I00, funded by MICIU/AEI/10.13039/501100011033 and FEDER), by the Asociación Española Contra el Cáncer (Proyectos Generales: PRYGN223117LLOV; Reto AECC 70% Supervivencia: RETOS245779LLOV), the Generalitat de Catalunya (AGAUR, 2021-SGR 01347), and from \&amp;quot;la Caixa\&amp;quot; Banking Foundation. JML is supported by the Fundació de Recerca Clínic Barcelona -IDIBAPS and a grant from the Spanish National Health Institute (MICINN, PID2022-139365OB-I00, funded by MICIU/AEI/10.13039/501100011033 and FEDER).</funder>
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              <p>Background &amp;amp; aims: Owing to unexplained interpatient variation and treatment failure in hepatocellular carcinoma (HCC), novel therapeutic approaches remain an urgent clinical need. Hepatic neurons, belonging to the autonomic nervous system (ANS), mediate liver/whole body crosstalk. Pathological innervation of the ANS has been identified in cancer, nurturing tumor stroma and conferring stronger carcinogenic properties.Methods: We characterized the innervation of liver tumors from the French Liver Biobank, then applied bioinformatics to TCGA (The Cancer Genome Atlas), several other datasets and a European validation cohort, to re-evaluate patient stratification. Cell biology and pharmacology studies were also performed.Results: Densely packed nucleated DCX+, synaptophysin+, NeuN+, VAChT+, TH-, CD31-, CD45- clusters, to date undetected, were identified in human HCCs, and independently confirmed by single-cell RNA sequencing data. Using the new concept of a neuronal score, human and rat HCCs displayed tightly netrin-1-associated neural reconfiguration towards cholinergic polarity, which was associated with chronic liver disease progression, cancer onset and many features of aggressive (proliferative class) HCC, including shortened survival. This score was conditioned by tumoral hepatocytes, and predicted sorafenib efficacy in the STORM HCC phase III trial. Conversely, intratumoral adrenergic lymphocytes were enriched in TEMRA and cytotoxic phenotypes. Amongst all cholinergic transcripts, the medically targeted CHRM3 receptor was enriched and associated with pathogenic traits in HCC, as well as poor prognosis in HCC stages 1-2, while its level dropped upon experimental re-differentiation. Its pharmacological inhibition with low concentrations of anticholinergic drugs, but not cholinomimetics, decreased anchorage-independent growth and anoikis, synergized with sorafenib and lenvatinib in HCC class 1 to 3 lines, yet not in primary human hepatocytes, and preserved mature hepatocyte functions.Conclusion: These data identify cholinergic processes as instrumental in liver carcinogenesis and support the use of EMA/FDA-approved cholinergic drugs in HCC research.Impact and implications: Hepatocellular carcinoma (HCC) care has long been hampered by the enigmatic nature of disease evolution, as well as of response or resistance to treatment. Hepatic neurons are likely the least studied liver cell type and mediate patients singularities from the ANS to the organ in real-time. Cholinergic inputs identified in this study as pathogenic may be targeted with the well charted pharmacopoeia of neurotropic drugs already available, for basic or clinical research purposes, with an expected high level of safety.</p>
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