Mitochondrial dysfunction in human immunodeficiency virus-1 transgenic mouse cardiac myocytes

J Cell Physiol. 2019 Apr;234(4):4432-4444. doi: 10.1002/jcp.27232. Epub 2018 Sep 7.

Abstract

The pathophysiology of human immunodeficiency virus (HIV)-associated cardiomyopathy remains uncertain. We used HIV-1 transgenic (Tg26) mice to explore mechanisms by which HIV-related proteins impacted on myocyte function. Compared to adult ventricular myocytes isolated from nontransgenic (wild type [WT]) littermates, Tg26 myocytes had similar mitochondrial membrane potential (ΔΨ m ) under normoxic conditions but lower Δ Ψ m after hypoxia/reoxygenation (H/R). In addition, Δ Ψ m in Tg26 myocytes failed to recover after Ca 2+ challenge. Functionally, mitochondrial Ca 2+ uptake was severely impaired in Tg26 myocytes. Basal and maximal oxygen consumption rates (OCR) were lower in normoxic Tg26 myocytes, and further reduced after H/R. Complex I subunit and ATP levels were lower in Tg26 hearts. Post-H/R, mitochondrial superoxide (O 2•- ) levels were higher in Tg26 compared to WT myocytes. Overexpression of B-cell lymphoma 2-associated athanogene 3 (BAG3) reduced O 2•- levels in hypoxic WT and Tg26 myocytes back to normal. Under normoxic conditions, single myocyte contraction dynamics were similar between WT and Tg26 myocytes. Post-H/R and in the presence of isoproterenol, myocyte contraction amplitudes were lower in Tg26 myocytes. BAG3 overexpression restored Tg26 myocyte contraction amplitudes to those measured in WT myocytes post-H/R. Coimmunoprecipitation experiments demonstrated physical association of BAG3 and the HIV protein Tat. We conclude: (a) Under basal conditions, mitochondrial Ca 2+ uptake, OCR, and ATP levels were lower in Tg26 myocytes; (b) post-H/R, Δ Ψ m was lower, mitochondrial O 2•- levels were higher, and contraction amplitudes were reduced in Tg26 myocytes; and (c) BAG3 overexpression decreased O 2•- levels and restored contraction amplitudes to normal in Tg26 myocytes post-H/R in the presence of isoproterenol.

Keywords: HIV cardiomyopathy; adenovirus; adult myocyte culture; mitochondria bioenergetics; reactive oxygen species.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Cardiomyopathies / genetics
  • Cardiomyopathies / metabolism*
  • Cardiomyopathies / physiopathology
  • Cardiomyopathies / virology
  • Cell Hypoxia
  • Cells, Cultured
  • Disease Models, Animal
  • Energy Metabolism*
  • HIV Infections / complications*
  • HIV Infections / virology
  • HIV-1 / genetics*
  • Membrane Potential, Mitochondrial
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mitochondria, Heart / metabolism*
  • Mitochondria, Heart / virology
  • Myocardial Contraction
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / virology
  • Oxidation-Reduction
  • Oxidative Stress
  • Oxygen Consumption
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Ventricular Function, Left

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • Bag3 protein, mouse
  • Reactive Oxygen Species