The Mitochondrial Fusion Protein, Optic Atrophy 1 (OPA1), Alters Cellular Metabolism to Support Cancer Cell Viability

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Punter, Kaylee B.

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thesis

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eng

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Mitochondria , Mitochondrial dynamics , Mitochondrial fusion , OPA1 , Optic Atrophy 1 , Triple Negative Breast Cancer , TNBC , Breast cancer , Metabolism , Altered metabolism , Mitochondrial dysfunction , Amino acids , Glycolysis , TCA cycle , Nucleotide synthesis , OPA1 inhibitor , MYLS22

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Abstract

Triple negative breast cancer (TNBC) is widely recognized to be aggressive and difficult to treat due to a lack of targetable hormone receptors. We have become interested in whether TNBC is critically dependent upon alterations in mitochondrial-governed metabolism. To preserve homeostasis, mitochondria undergo an equilibrium of two counteracting remodelling processes: fission (division) and fusion (elongation). The inner mitochondrial membrane GTPase, OPA1, is a cristae-organizing protein that directly organizes formation of the electron transport chain for oxidative phosphorylation and thereby further coordinates with the tricarboxylic acid (TCA) cycle. To study mitochondrial fusion as a target, we found that silencing of OPA1 in TNBC models led to suppressed growth in anchorage-independent soft agar and tumour xenograft experiments. OPA1 silencing disrupted cristae formation and triggered activation of stress pathways. Furthermore, profiling of OPA1-silenced cells revealed reprogramming of steady-state intracellular metabolites spanning intermediates of amino acids, TCA cycle and nucleotide biosynthetic pathways. To investigate nutrient usage, we performed stable isotope tracer analyses using [13C5]- and [15N2]-glutamine, which revealed increased incorporation into amino acid derivatives, TCA cycle, and pyrimidine intermediates. To confirm reprogramming events, we assessed gene expression patterns and observed differential expression of genes involved in amino acid and nucleotide biosynthetic pathways. OPA1 silencing also showed decreased levels of genes in glycolysis and PI3K/AKT/mTOR signalling pathways, which could also underlie decreased growth properties. Lastly, we sought to determine if similar effects could be triggered using a novel OPA1 inhibitor, MYLS22. At the transcript level, MYLS22 treatment led to changes that largely overlapped with gene silencing data. In sum, we demonstrate that targeting of OPA1 and mitochondrial fusion leads to metabolic reprogramming events correlated to decreased growth abilities. Overall, our findings further support the critical importance of OPA1 in maintaining proper metabolic homeostasis in order to drive tumorigenic growth in TNBC.

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