Extension of chronological life span by reduced TOR signaling requires down-regulation of Sch9p and involves increased mitochondrial OXPHOS complex density

Aging (Albany NY). 2009 Jan 28;1(1):131-45. doi: 10.18632/aging.100016.

Abstract

The nutrient-sensing target of rapamycin (TOR) pathway appears to have a conserved role in regulating life span. This signaling network is complex, with many downstream physiological outputs, and thus the mechanisms underlying its age-related effects have not been elucidated fully. We demonstrated previously that reduced TOR signaling (intor1Delta strains) extends yeast chronological life span (CLS) by increasing mitochondrial oxygen consumption, in part, by up-regulating translation of mtDNA-encoded oxidative phosphorylation (OXPHOS) subunits. Here, we have examined in greater detail how TOR signaling influences mitochondrial function and CLS and the role of the Sch9p kinase in the TOR-mitochondria pathway. As is the case for oxygen consumption, mitochondrial translation is elevated in tor1Delta strains only during active growth and early stationary phase growth points. This is accompanied by a corresponding increase in the abundance of both mtDNA-encoded and nucleus-encoded OXPHOS subunits per mitochondrial mass. However, this increased OXPHOS complex density is not associated with more mitochondria/cell or cellular ATP and leads to an overall decrease in membrane potential, suggesting that TOR signaling may influence respiration uncoupling. Finally, we document that the Sch9p kinase is a key downstream effector of OXPHOS, ROS and CLS in the TOR-mitochondria pathway. Altogether, our results demonstrate that TOR signaling has a global role in regulating mitochondrial proteome dynamics and function that is important for its role in aging and provide compelling evidence for involvement of a "mitochondrial pre-conditioning" effect in CLS determination.

Keywords: ROS; SCH9; TOR signaling; TOR1; aging; life span; mitochondria; proteomics; respiration; translation.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Cell Proliferation / drug effects
  • Cell Survival / physiology
  • DNA-Directed RNA Polymerases / genetics
  • Down-Regulation / genetics
  • Electron Transport Chain Complex Proteins / genetics
  • Electron Transport Chain Complex Proteins / metabolism*
  • Electron Transport Complex IV / genetics
  • Electron Transport Complex IV / metabolism
  • Gene Deletion
  • Gene Expression / genetics
  • Longevity / physiology*
  • Membrane Potential, Mitochondrial / physiology
  • Membrane Proteins / metabolism
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Oxidative Phosphorylation
  • Oxygen Consumption / drug effects
  • Oxygen Consumption / physiology
  • Phosphatidylinositol 3-Kinases / genetics*
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Serine-Threonine Kinases / genetics*
  • Reactive Oxygen Species / metabolism
  • Ribosomal Proteins / metabolism
  • Saccharomyces cerevisiae / drug effects
  • Saccharomyces cerevisiae / physiology*
  • Saccharomyces cerevisiae Proteins / antagonists & inhibitors
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Signal Transduction / physiology*
  • Sirolimus / pharmacology
  • Up-Regulation / physiology

Substances

  • Electron Transport Chain Complex Proteins
  • Membrane Proteins
  • Mitochondrial Proteins
  • Phosphoinositide-3 Kinase Inhibitors
  • Reactive Oxygen Species
  • Ribosomal Proteins
  • Saccharomyces cerevisiae Proteins
  • VAR1 protein, S cerevisiae
  • Electron Transport Complex IV
  • TOR1 protein, S cerevisiae
  • Protein Serine-Threonine Kinases
  • SCH9 protein, S cerevisiae
  • DNA-Directed RNA Polymerases
  • RPO41 protein, S cerevisiae
  • Sirolimus