Hygromycin B hypersensitive (hhy) mutants implicate an intact trans-Golgi and late endosome interface in efficient Tor1 vacuolar localization and TORC1 function

Curr Genet. 2017 Jun;63(3):531-551. doi: 10.1007/s00294-016-0660-9. Epub 2016 Nov 3.

Abstract

Saccharomyces cerevisiae vacuoles are functionally analogous to mammalian lysosomes. Both also serve as physical platforms for Tor Complex 1 (TORC1) signal transduction, the master regulator of cellular growth and proliferation. Hygromycin B is a eukaryotic translation inhibitor. We recently reported on hygromycin B hypersensitive (hhy) mutants that fail to grow at subtranslation inhibitory concentrations of the drug and exhibit vacuolar defects (Banuelos et al. in Curr Genet 56:121-137, 2010). Here, we show that hhy phenotype is not due to increased sensitivity to translation inhibition and establish a super HHY (s-HHY) subgroup of genes comprised of ARF1, CHC1, DRS2, SAC1, VPS1, VPS34, VPS45, VPS52, and VPS54 that function exclusively or inclusively at trans-Golgi and late endosome interface. Live cell imaging of s-hhy mutants revealed that hygromycin B treatment disrupts vacuolar morphology and the localization of late endosome marker Pep12, but not that of late endosome-independent vacuolar SNARE Vam3. This, along with normal post-late endosome trafficking of the vital dye FM4-64, establishes that severe hypersensitivity to hygromycin B correlates specifically with compromised trans-Golgi and late endosome interface. We also show that Tor1p vacuolar localization and TORC1 anabolic functions, including growth promotion and phosphorylation of its direct substrate Sch9, are compromised in s-hhy mutants. Thus, an intact trans-Golgi and late endosome interface is a requisite for efficient Tor1 vacuolar localization and TORC1 function.

Keywords: Hygromycin hypersensitive mutants; TORC1 regulation; Trans-Golgi and late endosome interface; Yeast; hhy mutants.

MeSH terms

  • Endosomes / drug effects
  • Endosomes / genetics
  • Golgi Apparatus / drug effects
  • Golgi Apparatus / genetics
  • Hygromycin B / pharmacology*
  • Mechanistic Target of Rapamycin Complex 1 / genetics
  • Phosphatidylinositol 3-Kinases / genetics*
  • Protein Biosynthesis / drug effects
  • Protein Serine-Threonine Kinases / genetics*
  • Protein Serine-Threonine Kinases / metabolism
  • Qa-SNARE Proteins / genetics
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Vacuoles / drug effects
  • Vacuoles / genetics

Substances

  • Qa-SNARE Proteins
  • Saccharomyces cerevisiae Proteins
  • VAM3 protein, S cerevisiae
  • Hygromycin B
  • TOR1 protein, S cerevisiae
  • Mechanistic Target of Rapamycin Complex 1
  • Protein Serine-Threonine Kinases
  • SCH9 protein, S cerevisiae