TY - JOUR
T1 - Saccharomyces cerevisiae is dependent on vesicular traffic between the Golgi apparatus and the vacuole when inositolphosphorylceramide synthase aur1 is inactivated
AU - Voynova, Natalia S
AU - Roubaty, Carole
AU - Vazquez, Hector M
AU - Mallela, Shamroop K
AU - Ejsing, Christer S
AU - Conzelmann, Andreas
N1 - Copyright © 2015, American Society for Microbiology. All Rights Reserved.
PY - 2015/11/30
Y1 - 2015/11/30
N2 - Inositolphosphorylceramide (IPC) and its mannosylated derivatives are the only complex sphingolipids of yeast. Their synthesis can be reduced by aureobasidin A (AbA), which specifically inhibits the IPC synthase Aur1. AbA reportedly, by diminishing IPC levels, causes endoplasmic reticulum (ER) stress, an increase in cytosolic calcium, reactive oxygen production, and mitochondrial damage leading to apoptosis. We found that when Aur1 is gradually depleted by transcriptional downregulation, the accumulation of ceramides becomes a major hindrance to cell survival. Overexpression of the alkaline ceramidase YPC1 rescues cells under this condition. We established hydroxylated C
26 fatty acids as a reliable hallmark of ceramide hydrolysis. Such hydrolysis occurs only when YPC1 is overexpressed. In contrast, overexpression of YPC1 has no beneficial effect when Aur1 is acutely repressed by AbA. A high-throughput genetic screen revealed that vesicle-mediated transport between Golgi apparatus, endosomes, and vacuole becomes crucial for survival when Aur1 is repressed, irrespective of the mode of repression. In addition, vacuolar acidification becomes essential when cells are acutely stressed by AbA, and quinacrine uptake into vacuoles shows that AbA activates vacuolar acidification. The antioxidant N-acetylcysteine does not improve cell growth on AbA, indicating that reactive oxygen radicals induced by AbA play a minor role in its toxicity. AbA strongly induces the cell wall integrity pathway, but osmotic support does not improve the viability of wild-type cells on AbA. Altogether, the data support and refine current models of AbA-mediated cell death and add vacuolar protein transport and acidification as novel critical elements of stress resistance.
AB - Inositolphosphorylceramide (IPC) and its mannosylated derivatives are the only complex sphingolipids of yeast. Their synthesis can be reduced by aureobasidin A (AbA), which specifically inhibits the IPC synthase Aur1. AbA reportedly, by diminishing IPC levels, causes endoplasmic reticulum (ER) stress, an increase in cytosolic calcium, reactive oxygen production, and mitochondrial damage leading to apoptosis. We found that when Aur1 is gradually depleted by transcriptional downregulation, the accumulation of ceramides becomes a major hindrance to cell survival. Overexpression of the alkaline ceramidase YPC1 rescues cells under this condition. We established hydroxylated C
26 fatty acids as a reliable hallmark of ceramide hydrolysis. Such hydrolysis occurs only when YPC1 is overexpressed. In contrast, overexpression of YPC1 has no beneficial effect when Aur1 is acutely repressed by AbA. A high-throughput genetic screen revealed that vesicle-mediated transport between Golgi apparatus, endosomes, and vacuole becomes crucial for survival when Aur1 is repressed, irrespective of the mode of repression. In addition, vacuolar acidification becomes essential when cells are acutely stressed by AbA, and quinacrine uptake into vacuoles shows that AbA activates vacuolar acidification. The antioxidant N-acetylcysteine does not improve cell growth on AbA, indicating that reactive oxygen radicals induced by AbA play a minor role in its toxicity. AbA strongly induces the cell wall integrity pathway, but osmotic support does not improve the viability of wild-type cells on AbA. Altogether, the data support and refine current models of AbA-mediated cell death and add vacuolar protein transport and acidification as novel critical elements of stress resistance.
KW - Alleles
KW - Biological Transport/drug effects
KW - Biosynthetic Pathways/drug effects
KW - Ceramides/metabolism
KW - Depsipeptides/pharmacology
KW - Doxycycline/pharmacology
KW - Epistasis, Genetic/drug effects
KW - Gene Deletion
KW - Gene Ontology
KW - Genetic Testing
KW - Glycosphingolipids/metabolism
KW - Golgi Apparatus/drug effects
KW - Hexosyltransferases/antagonists & inhibitors
KW - High-Throughput Screening Assays
KW - Hydrolysis
KW - Lipid Droplets/drug effects
KW - Mutation/genetics
KW - Quinacrine/metabolism
KW - Saccharomyces cerevisiae Proteins/metabolism
KW - Saccharomyces cerevisiae/cytology
KW - Sphingolipids/biosynthesis
KW - Transport Vesicles/drug effects
KW - Vacuoles/drug effects
U2 - 10.1128/EC.00117-15
DO - 10.1128/EC.00117-15
M3 - Journal article
C2 - 26432633
SN - 1535-9778
VL - 14
SP - 1203
EP - 1216
JO - Eukaryotic Cell
JF - Eukaryotic Cell
IS - 12
ER -