Import of extracellular ATP in yeast and man modulates AMPK and TORC1 signalling

J Cell Sci. 2019 Apr 3;132(7):jcs223925. doi: 10.1242/jcs.223925.

Abstract

AMP-activated kinase (AMPK) and target of rapamycin (TOR) signalling coordinate cell growth, proliferation, metabolism and cell survival with the nutrient environment of cells. The poor vasculature and nutritional stress experienced by cells in solid tumours raises the question: how do they assimilate sufficient nutrients to survive? Here, we show that human and fission yeast cells import ATP and AMP from their external environment to regulate AMPK and TOR signalling. Exposure of fission yeast (Schizosaccharomyces pombe) and human cells to external AMP impeded cell growth; however, in yeast this restraining impact required AMPK. In contrast, external ATP rescued the growth defect of yeast mutants with reduced TORC1 signalling; furthermore, exogenous ATP transiently enhanced TORC1 signalling in both yeast and human cell lines. Addition of the PANX1 channel inhibitor probenecid blocked ATP import into human cell lines suggesting that this channel may be responsible for both ATP release and uptake in mammals. In light of these findings, it is possible that the higher extracellular ATP concentration reported in solid tumours is both scavenged and recognized as an additional energy source beneficial for cell growth.

Keywords: AMP; AMPK; ATP; Fission yeast; Nutrient stress; Schizosaccharomyces pombe; Ssp2; TORC1; Tsc1; Tsc2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism*
  • Adenosine Triphosphate / metabolism*
  • Cell Proliferation
  • Connexins / metabolism
  • Gene Expression Regulation, Fungal
  • HEK293 Cells
  • Humans
  • Mechanistic Target of Rapamycin Complex 1 / genetics
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Nerve Tissue Proteins / metabolism
  • Phosphorylation
  • Schizosaccharomyces
  • Schizosaccharomyces pombe Proteins / genetics
  • Schizosaccharomyces pombe Proteins / metabolism
  • Signal Transduction*
  • Stress, Physiological

Substances

  • Connexins
  • Nerve Tissue Proteins
  • PANX1 protein, human
  • Schizosaccharomyces pombe Proteins
  • Adenosine Triphosphate
  • Mechanistic Target of Rapamycin Complex 1
  • AMP-Activated Protein Kinases