Marcellus Augustine, Nuno R. Nené, Hongchang Fu, Christopher L. Pinder, Lorena Ligammari, Alexander P. Simpson, Irene Sanz-Fernández, Krupa Thakkar, Danwen Qian, Evelyn Fitzsimons, B S. Simpson, Roberto Vendramin, Andrea Castro, Heather Niederer, Samra Turajlic, Sergio A. Quezada, Nicholas McGranahan, Chris Watkins, Charles Swanton, Kevin Litchfield
Abstract Immunotherapy has revolutionized cancer treatment, yet only a minority of individuals respond clinically, necessitating alternative strategies that can benefit these patients. Novel immuno-oncology targets may achieve this through bypassing resistance mechanisms to standard therapies. We introduce Mining Immunotherapy Drug tArgetS (MIDAS), a multimodal graph neural network system for immuno-oncology target discovery. MIDAS leverages gene interactions, multi-omic patient profiles, immune cell biology, antigen processing, disease associations and phenotypic consequences of genetic perturbations. It generalizes to time-sliced data, outcompetes state-of-the-art baselines (including OpenTargets) and ranks approved targets above those in clinical development. Moreover, MIDAS recovers immunotherapy-response-associated genes in unseen patients, thereby capturing immunotherapy response determinants. Interpretability analyses reveal a reliance on autoimmunity, regulatory networks and immuno-oncology pathways. Functionally perturbing oncostatin M–oncostatin M receptor signalling, a proposed MIDAS target, in TRACERx melanoma-patient-derived explants yielded reduced dysfunctional CD8 + T cells, which associate with immunotherapy response, and reduced CCL4 levels. Furthermore, oncostatin M and oncostatin M receptor expression is associated with altered T cell and macrophage profiles in bulk transcriptomic data from patient samples. These data are consistent with a role for oncostatin M–oncostatin M in modulating the tumour microenvironment towards immunosuppressive, tumour-promoting phenotypes. Our results present a machine learning framework for analysing multimodal data for immuno-oncology target discovery.