Defective Mitochondrial Cardiolipin Remodeling Dampens HIF-1α Expression in Hypoxia

Cell Rep. 2018 Oct 16;25(3):561-570.e6. doi: 10.1016/j.celrep.2018.09.057.

Abstract

Mitochondria fulfill vital metabolic functions and act as crucial cellular signaling hubs, integrating their metabolic status into the cellular context. Here, we show that defective cardiolipin remodeling, upon loss of the cardiolipin acyl transferase tafazzin, decreases HIF-1α signaling in hypoxia. Tafazzin deficiency does not affect posttranslational HIF-1α regulation but rather HIF-1α gene expression, a dysfunction recapitulated in iPSC-derived cardiomyocytes from Barth syndrome patients with tafazzin deficiency. RNA-seq analyses confirmed drastically altered signaling in tafazzin mutant cells. In hypoxia, tafazzin-deficient cells display reduced production of reactive oxygen species (ROS) perturbing NF-κB activation and concomitantly HIF-1α gene expression. Tafazzin-deficient mice hearts display reduced HIF-1α levels and undergo maladaptive hypertrophy with heart failure in response to pressure overload challenge. We conclude that defective mitochondrial cardiolipin remodeling dampens HIF-1α signaling due to a lack of NF-κB activation through reduced mitochondrial ROS production, decreasing HIF-1α transcription.

Keywords: Barth syndrome; Hif1 alpha; NF-κB signaling; ROS; cardiolipin; lipid; mitochondria; respiratory chain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyltransferases
  • Animals
  • Barth Syndrome / genetics
  • Barth Syndrome / metabolism
  • Barth Syndrome / pathology*
  • Biomarkers / metabolism
  • Cardiolipins / genetics
  • Cardiolipins / metabolism*
  • Cells, Cultured
  • Gene Expression Regulation*
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Hypoxia / metabolism
  • Hypoxia / pathology*
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Mitochondria / metabolism
  • Mitochondria / pathology*
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • NF-kappa B / metabolism
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcription Factors / physiology*

Substances

  • Biomarkers
  • Cardiolipins
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • NF-kappa B
  • Reactive Oxygen Species
  • Transcription Factors
  • Acyltransferases
  • tafazzin protein, mouse
  • TAFAZZIN protein, human