Nicotinamide nucleotide transhydrogenase activity impacts mitochondrial redox balance and the development of hypertension in mice

J Am Soc Hypertens. 2017 Feb;11(2):110-121. doi: 10.1016/j.jash.2016.12.002. Epub 2016 Dec 16.

Abstract

Oxidant stress contributes to the initiation and progression of hypertension (HTN) by enhancing endothelial dysfunction and/or causing perturbations in nitric oxide homeostasis. Differences in mitochondrial function may augment this process and provide insight into why age of onset and clinical outcomes differ among individuals from distinct ethnic groups. We have previously demonstrated that variation in normal mitochondrial function and oxidant production exists in endothelial cells from individuals of Caucasian and African-American ethnicity and that this variation contributes to endothelial dysfunction. To model these distinct mitochondrial redox phenotypes, we used C57Bl/6N (6N) and C57Bl/6J (6J) mice that also display unique mitochondrial functional properties due to the differential expression nicotinamide nucleotide transhydrogenase (NNT). We demonstrate that the absence of NNT in 6J cells led to distinct mitochondrial bioenergetic profiles and a pro-oxidative mitochondrial phenotype characterized by increased superoxide production and reduced glutathione peroxidase activity. Interestingly, we found that 6J animals have significantly higher systolic blood pressure compared to 6N animals, and this difference is exacerbated by angiotensin II treatment. The changes in pressure were accompanied by both mitochondrial and vascular dysfunction revealed by impaired respiratory control ratios and endothelial-dependent vessel dilation. All end points could be significantly ameliorated by treatment with the mitochondria-targeted superoxide dismutase mimetic MitoTEMPO demonstrating a critical role for the production of mitochondrial reactive oxygen species in the development of HTN in these animals. Taken together, these data indicate that the absence of NNT leads to variation in mitochondrial function and contributes to a unique mitochondrial redox phenotype that influences susceptibility to HTN by contributing to endothelial and vascular dysfunction.

Keywords: Mitochondria; NNT; reactive oxygen species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / pharmacology
  • Animals
  • Antioxidants / pharmacology
  • Blood Pressure / drug effects
  • Carotid Arteries
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelium / physiopathology*
  • Humans
  • Hypertension / pathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / metabolism
  • Myography
  • NADP Transhydrogenase, AB-Specific / metabolism*
  • Nitric Oxide / metabolism
  • Organophosphorus Compounds / pharmacology
  • Oxidation-Reduction
  • Oxidative Stress*
  • Piperidines / pharmacology
  • Primary Cell Culture
  • Superoxide Dismutase / metabolism
  • Superoxides / metabolism*
  • Vasoconstrictor Agents / pharmacology

Substances

  • Antioxidants
  • MitoTEMPO
  • Mitochondrial Proteins
  • Organophosphorus Compounds
  • Piperidines
  • Vasoconstrictor Agents
  • Superoxides
  • Angiotensin II
  • Nitric Oxide
  • Superoxide Dismutase
  • NADP Transhydrogenase, AB-Specific
  • Nnt protein, mouse