Pancreatic cancer has a devastating prognosis, with five-year survival around 5% and severely restricted treatment options, reflecting a high degree of molecular heterogeneity. The role of altered nutrient metabolism in tumours has attracted much recent interest, both in understanding tumourigenesis and as a potential therapeutic target. Mitochondria are key players in cellular metabolism. Many tumours exhibit accumulation of mitochondrial mutations but there has been little effort to link these observations to phenotypic changes through functional studies. Access to a cohort of patient-derived xenograft tumour cell lines (PDCLs) provides us with a unique opportunity to directly study links between genotype and phenotype in pancreatic cancer.
Here, we show that somatic mutations in mitochondrial and metabolic genes of pancreatic cancers drive a consistent metabolic phenotype. We identified 24 somatic mutations in the mitochondrial genomes of all 12 cell lines, most of which were non-synonymous and located in coding regions for electron transport chain (ETC) subunits. A further 18 mutations were identified in a targeted analysis of nuclear genes important for mitochondrial function and metabolism. Structural modeling predicted deleterious effects of mitochondrial mutations on assembly/function of ETC enzymes and we observed significantly altered expression of key ETC subunits in PDCLs harbouring mtDNA mutations. Compared with normal pancreatic ductal epithelial cells, all tumour cells exhibited mitochondrial and metabolic dysfunction - with reduced oxygen consumption and increased glycolysis. Metabolomics analysis of PDCLs showed reduced oxidative phosphorylation and initiation of reductive glutamine metabolism to promote production of biosynthetic intermediates, particularly via fatty acid synthesis. We propose that mutations in mitochondrial and metabolic genes drive metabolic adaptations in pancreatic tumours to meet the significant anabolic needs of rapid proliferation. These findings identify a potential therapeutic strategy targeting key enzymes in reductive glutamine metabolism and fatty acid biosynthesis.