Roles for ROS and hydrogen sulfide in the longevity response to germline loss in Caenorhabditis elegans

Proc Natl Acad Sci U S A. 2016 May 17;113(20):E2832-41. doi: 10.1073/pnas.1524727113. Epub 2016 May 2.

Abstract

In Caenorhabditis elegans, removing germ cells slows aging and extends life. Here we show that transcription factors that extend life and confer protection to age-related protein-aggregation toxicity are activated early in adulthood in response to a burst of reactive oxygen species (ROS) and a shift in sulfur metabolism. Germline loss triggers H2S production, mitochondrial biogenesis, and a dynamic pattern of ROS in specific somatic tissues. A cytoskeletal protein, KRI-1, plays a key role in the generation of H2S and ROS. These kri-1-dependent redox species, in turn, promote life extension by activating SKN-1/Nrf2 and the mitochondrial unfolded-protein response, respectively. Both H2S and, remarkably, kri-1-dependent ROS are required for the life extension produced by low levels of the superoxide-generator paraquat and by a mutation that inhibits respiration. Together our findings link reproductive signaling to mitochondria and define an inducible, kri-1-dependent redox-signaling module that can be invoked in different contexts to extend life and counteract proteotoxicity.

Keywords: Aβ; KRIT1; Nrf2; SKN-1; hormesis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Aging*
  • Animals
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism
  • DNA-Binding Proteins / metabolism
  • Germ Cells / physiology
  • Hydrogen Sulfide / metabolism*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Longevity
  • Mitochondrial Dynamics
  • Organelle Biogenesis
  • Oxidation-Reduction
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction
  • Transcription Factors / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • KRI-1 protein, C elegans
  • Reactive Oxygen Species
  • Transcription Factors
  • skn-1 protein, C elegans
  • Hydrogen Sulfide