ROS Control Mitochondrial Motility through p38 and the Motor Adaptor Miro/Trak

Cell Rep. 2017 Nov 7;21(6):1667-1680. doi: 10.1016/j.celrep.2017.10.060.

Abstract

Mitochondrial distribution and motility are recognized as central to many cellular functions, but their regulation by signaling mechanisms remains to be elucidated. Here, we report that reactive oxygen species (ROS), either derived from an extracellular source or intracellularly generated, control mitochondrial distribution and function by dose-dependently, specifically, and reversibly decreasing mitochondrial motility in both rat hippocampal primary cultured neurons and cell lines. ROS decrease motility independently of cytoplasmic [Ca2+], mitochondrial membrane potential, or permeability transition pore opening, known effectors of oxidative stress. However, multiple lines of genetic and pharmacological evidence support that a ROS-activated mitogen-activated protein kinase (MAPK), p38α, is required for the motility inhibition. Furthermore, anchoring mitochondria directly to kinesins without involvement of the physiological adaptors between the organelles and the motor protein prevents the H2O2-induced decrease in mitochondrial motility. Thus, ROS engage p38α and the motor adaptor complex to exert changes in mitochondrial motility, which likely has both physiological and pathophysiological relevance.

Keywords: Miro; TRAK; calcium; mitochondria; movement; p38; permeability transition; reactive oxygen species.

MeSH terms

  • Animals
  • Anthracenes / pharmacology
  • Calcium / metabolism
  • Cells, Cultured
  • Cyclosporine / pharmacology
  • Hydrogen Peroxide / pharmacology
  • MAP Kinase Kinase Kinase 5 / metabolism
  • MAP Kinase Kinase Kinases / metabolism
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Microscopy, Fluorescence
  • Mitochondria / drug effects
  • Mitochondria / physiology*
  • Mitochondrial Dynamics / drug effects
  • Neurons / cytology
  • Neurons / metabolism
  • Rats
  • Reactive Oxygen Species / metabolism*
  • Superoxide Dismutase / metabolism
  • Time-Lapse Imaging
  • Vitamin K 3 / pharmacology
  • p38 Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • p38 Mitogen-Activated Protein Kinases / genetics
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Anthracenes
  • Reactive Oxygen Species
  • pyrazolanthrone
  • Vitamin K 3
  • Cyclosporine
  • Hydrogen Peroxide
  • Superoxide Dismutase
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5
  • MAP Kinase Kinase Kinases
  • Calcium