IL-6 protects against hyperoxia-induced mitochondrial damage via Bcl-2-induced Bak interactions with mitofusins

Am J Respir Cell Mol Biol. 2009 Oct;41(4):385-96. doi: 10.1165/rcmb.2008-0302OC. Epub 2009 Jan 23.

Abstract

Overexpression of IL-6 markedly diminishes hyperoxic lung injury, hyperoxia-induced cell death, and DNA fragmentation, and enhances Bcl-2 expression. We hypothesized that changes in the interactions between Bcl-2 family members play an important role in the IL-6-mediated protective response to oxidative stress. Consistent with this hypothesis, we found that IL-6 induced Bcl-2 expression, both in vivo and in vitro, disrupted interactions between proapoptotic and antiapoptotic factors, and suppressed H(2)O(2)-induced loss of mitochondrial membrane potential in vitro. In addition, IL-6 overexpression in mice protects against hyperoxia-induced lung mitochondrial damage. The overexpression of Bcl-2 in vivo prolonged the survival of mice exposed to hyperoxia and inhibited alveolar capillary protein leakage. In addition, apoptosis-associated DNA fragmentation was substantially reduced in these animals. This IL-6-mediated protection was lost when Bcl-2 was silenced, demonstrating that Bcl-2 is an essential mediator of IL-6 cytoprotection. Finally, Bcl-2 blocked the dissociation of Bak from mitofusin protein (Mfn) 2, and inhibited the interaction between Bak and Mfn1. Taken together, our results suggest that IL-6 induces Bcl-2 expression to perform cytoprotective functions in response to oxygen toxicity, and that this effect is mediated by alterations in the interactions between Bak and Mfns.

Publication types

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

MeSH terms

  • Acute Lung Injury / etiology
  • Acute Lung Injury / physiopathology
  • Acute Lung Injury / prevention & control
  • Animals
  • Apoptosis Regulatory Proteins / metabolism
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • GTP Phosphohydrolases / metabolism*
  • Humans
  • Hyperoxia / drug therapy*
  • Hyperoxia / physiopathology
  • Interleukin-6 / genetics
  • Interleukin-6 / pharmacology
  • Interleukin-6 / physiology*
  • Lipid Peroxidation / drug effects
  • Lung / drug effects*
  • Lung / metabolism
  • Lung / pathology
  • Membrane Proteins / metabolism*
  • Membrane Transport Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondrial Membrane Transport Proteins
  • Mitochondrial Proteins / metabolism*
  • Oxidative Stress / drug effects*
  • Oxidative Stress / physiology
  • Oxygen / toxicity*
  • Protein Interaction Mapping
  • Proto-Oncogene Proteins c-bcl-2 / antagonists & inhibitors
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / physiology*
  • RNA, Small Interfering / pharmacology
  • Recombinant Fusion Proteins / physiology
  • bcl-2 Homologous Antagonist-Killer Protein / metabolism*

Substances

  • Apoptosis Regulatory Proteins
  • BAK1 protein, human
  • Bak1 protein, mouse
  • IL6 protein, human
  • Interleukin-6
  • Membrane Proteins
  • Membrane Transport Proteins
  • Mitochondrial Membrane Transport Proteins
  • Mitochondrial Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • RNA, Small Interfering
  • Recombinant Fusion Proteins
  • bcl-2 Homologous Antagonist-Killer Protein
  • GTP Phosphohydrolases
  • MFN2 protein, human
  • Mfn1 protein, mouse
  • Mfn2 protein, mouse
  • Mfn1 protein, human
  • Oxygen