Withdrawal of essential amino acids increases autophagy by a pathway involving Ca2+/calmodulin-dependent kinase kinase-β (CaMKK-β)

J Biol Chem. 2012 Nov 9;287(46):38625-36. doi: 10.1074/jbc.M112.365767. Epub 2012 Oct 1.

Abstract

Autophagy is the main lysosomal catabolic process that becomes activated under stress conditions, such as amino acid starvation and cytosolic Ca(2+) upload. However, the molecular details on how both conditions control autophagy are still not fully understood. Here we link essential amino acid starvation and Ca(2+) in a signaling pathway to activate autophagy. We show that withdrawal of essential amino acids leads to an increase in cytosolic Ca(2+), arising from both extracellular medium and intracellular stores, which induces the activation of adenosine monophosphate-activated protein kinase (AMPK) via Ca(2+)/calmodulin-dependent kinase kinase-β (CaMKK-β). Furthermore, we show that autophagy induced by amino acid starvation requires AMPK, as this induction is attenuated in its absence. Subsequently, AMPK activates UNC-51-like kinase (ULK1), a mammalian autophagy-initiating kinase, through phosphorylation at Ser-555 in a process that requires CaMKK-β. Finally, the mammalian target of rapamycin complex C1 (mTORC1), a negative regulator of autophagy downstream of AMPK, is inhibited by amino acid starvation in a Ca(2+)-sensitive manner, and CaMKK-β appears to be important for mTORC1 inactivation, especially in the absence of extracellular Ca(2+). All these results highlight that amino acid starvation regulates autophagy in part through an increase in cellular Ca(2+) that activates a CaMKK-β-AMPK pathway and inhibits mTORC1, which results in ULK1 stimulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Amino Acids, Essential / chemistry
  • Animals
  • Autophagy
  • Autophagy-Related Protein-1 Homolog
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase / metabolism*
  • Cytosol / metabolism
  • HeLa Cells
  • Humans
  • Insulin / metabolism
  • Mechanistic Target of Rapamycin Complex 1
  • Mice
  • Models, Biological
  • Multiprotein Complexes / metabolism*
  • Phosphorylation
  • Protein Serine-Threonine Kinases / metabolism
  • RNA Interference
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Amino Acids, Essential
  • Insulin
  • Multiprotein Complexes
  • Autophagy-Related Protein-1 Homolog
  • Mechanistic Target of Rapamycin Complex 1
  • Protein Serine-Threonine Kinases
  • TOR Serine-Threonine Kinases
  • Ulk1 protein, mouse
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase