Abstract
Defects in mitochondrial oxidative phosphorylation complexes,
altered bioenergetics and metabolic shift are often seen in
cancers. Here we show a role for the dysfunction of the electron
transport chain component cytochrome c oxidase (CcO) in cancer
progression. We show that genetic silencing of the CcO complex by
shRNA expression and loss of CcO activity in multiple cell types
from the mouse and human sources resulted in metabolic shift to
glycolysis, loss of anchorage-dependent growth and acquired
invasive phenotypes. Disruption of the CcO complex caused loss of
transmembrane potential and induction of Ca2+/Calcineurin- mediated
retrograde signaling. Propagation of this signaling includes
activation of PI3-kinase, IGF1R and Akt, Ca2+-sensitive
transcription factors and also TGF1, MMP16 and periostin, which are
involved in oncogenic progression. Whole-genome expression
analysis showed the upregulation of genes involved in cell
signaling, extracellular matrix interactions, cell morphogenesis,
cell motility and migration. The transcription proles reveal
extensive similarity to retrograde signaling initiated by partial
mitochondrial DNA depletion, although distinct differences are
observed in signaling induced by CcO dysfunction. The possible CcO
dysfunction as a biomarker for cancer progression was supported by
data showing that esophageal tumors from human patients show
reduced CcO subunits IVi1 and Vb in regions that were previously
shown to be the hypoxic core of the tumors. Our results show that
mitochondrial electron transport chain defect initiates a
retrograde signaling. These results suggest that a defect in the
CcO complex can potentially induce tumor progression.
(Oncogene, Volume 35, Page 1585-1595, doi:10.1038/onc.2015.227, 2016)