Madeleine Benguigui, Abby Lockwood, Rochani Rajendram, Turkan Gizer, Edward Carter, Eleni Maniati, Pedro Casado, Vinothini Rajeeve, Gilbert Fruhwirth, Cameron Lang, Juan Pedro Martinez-Barbera, Scott Haston, Kairbaan Hodivala-Dilke, Ana Rita Pedrosa
Platinum-based chemotherapy is widely used to treat non-small cell lung cancer: however, intrathoracic metastasis remains a major clinical challenge associated with increased morbidity. While chemotherapy is generally viewed as acting directly on tumour cells, it can also reprogramme the tumour microenvironment, including vascular endothelial cells. Here, we identify endothelial cell focal adhesion kinase (FAK) as a regulator of cisplatin-induced vascular stress responses that promote metastatic seeding in the lung. Using inducible endothelial cell-specific FAK loss- and endothelial cell-specific kinase-dead mouse models, we show that endothelial cell FAK is required for cisplatin-enhanced lung metastasis. In the pre-metastatic lung, cisplatin induces endothelial cell DNA damage and FAK-dependent transcriptional reprogramming enriched for p53-responsive, stress-adaptive, and senescence-associated genes. Cisplatin treatment also promotes an endothelial cell FAK-dependent secretory and adhesive state increasing tumour cell binding and metastasis seeding in the lung. Mechanistically, cisplatin triggers a transient nuclear accumulation of FAK, where kinase activity supports early ATM signaling and DNA repair. Overall, our data indicate that targeting endothelial cell FAK suppresses these responses and reduces cisplatin-induced lung metastasis.