Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae

Sara A. Zurita-Martinez, Rekha Puria, Xuewen Pan, Jef D. Boeke, Maria E. Cardenas

Research output: Contribution to journalArticle

Abstract

The Tor kinases regulate responses to nutrients and control cell growth. Unlike most organisms that only contain one Tor protein, Saccharomyces cerevisiae expresses two, Tor1 and Tor2, which are thought to share all of the rapamycin-sensitive functions attributable to Tor signaling. Here we conducted a genetic screen that defined the global TOR1 synthetic fitness or lethal interaction gene network. This screen identified mutations in distinctive functional categories that impaired vacuolar function, including components of the EGO/Gse and PAS complexes that reduce fitness. In addition, tor1 is lethal in combination with mutations in class C Vps complex components. We find that Tor1 does not regulate the known function of the class C Vps complex in protein sorting. Instead class C vps mutants fail to recover from rapamycin-induced growth arrest or to survive nitrogen starvation and have low levels of amino acids. Remarkably, addition of glutamate or glutamine restores viability to a tor1 pep3 mutant strain. We conclude that Tor1 is more effective than Tor2 at providing rapamycin-sensitive Tor signaling under conditions of amino acid limitation, and that an intact class C Vps complex is required to mediate intracellular amino acid homeostasis for efficient Tor signaling.

Original languageEnglish (US)
Pages (from-to)2139-2150
Number of pages12
JournalGenetics
Volume176
Issue number4
DOIs
StatePublished - Aug 2007

Fingerprint

Sirolimus
Protein C
Saccharomyces cerevisiae
Amino Acids
Lethal Genes
Saccharomyces cerevisiae Proteins
Mutation
Gene Regulatory Networks
Protein Transport
Growth
Starvation
Glutamine
Glutamic Acid
Homeostasis
Phosphotransferases
Nitrogen
Food

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

Cite this

Zurita-Martinez, S. A., Puria, R., Pan, X., Boeke, J. D., & Cardenas, M. E. (2007). Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. Genetics, 176(4), 2139-2150. https://doi.org/10.1534/genetics.107.072835

Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. / Zurita-Martinez, Sara A.; Puria, Rekha; Pan, Xuewen; Boeke, Jef D.; Cardenas, Maria E.

In: Genetics, Vol. 176, No. 4, 08.2007, p. 2139-2150.

Research output: Contribution to journalArticle

Zurita-Martinez, SA, Puria, R, Pan, X, Boeke, JD & Cardenas, ME 2007, 'Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae', Genetics, vol. 176, no. 4, pp. 2139-2150. https://doi.org/10.1534/genetics.107.072835
Zurita-Martinez, Sara A. ; Puria, Rekha ; Pan, Xuewen ; Boeke, Jef D. ; Cardenas, Maria E. / Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae. In: Genetics. 2007 ; Vol. 176, No. 4. pp. 2139-2150.
@article{089b7a4608be47758edea9935d519111,
title = "Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae",
abstract = "The Tor kinases regulate responses to nutrients and control cell growth. Unlike most organisms that only contain one Tor protein, Saccharomyces cerevisiae expresses two, Tor1 and Tor2, which are thought to share all of the rapamycin-sensitive functions attributable to Tor signaling. Here we conducted a genetic screen that defined the global TOR1 synthetic fitness or lethal interaction gene network. This screen identified mutations in distinctive functional categories that impaired vacuolar function, including components of the EGO/Gse and PAS complexes that reduce fitness. In addition, tor1 is lethal in combination with mutations in class C Vps complex components. We find that Tor1 does not regulate the known function of the class C Vps complex in protein sorting. Instead class C vps mutants fail to recover from rapamycin-induced growth arrest or to survive nitrogen starvation and have low levels of amino acids. Remarkably, addition of glutamate or glutamine restores viability to a tor1 pep3 mutant strain. We conclude that Tor1 is more effective than Tor2 at providing rapamycin-sensitive Tor signaling under conditions of amino acid limitation, and that an intact class C Vps complex is required to mediate intracellular amino acid homeostasis for efficient Tor signaling.",
author = "Zurita-Martinez, {Sara A.} and Rekha Puria and Xuewen Pan and Boeke, {Jef D.} and Cardenas, {Maria E.}",
year = "2007",
month = "8",
doi = "10.1534/genetics.107.072835",
language = "English (US)",
volume = "176",
pages = "2139--2150",
journal = "Genetics",
issn = "0016-6731",
publisher = "Genetics Society of America",
number = "4",

}

TY - JOUR

T1 - Efficient Tor signaling requires a functional class C Vps protein complex in Saccharomyces cerevisiae

AU - Zurita-Martinez, Sara A.

AU - Puria, Rekha

AU - Pan, Xuewen

AU - Boeke, Jef D.

AU - Cardenas, Maria E.

PY - 2007/8

Y1 - 2007/8

N2 - The Tor kinases regulate responses to nutrients and control cell growth. Unlike most organisms that only contain one Tor protein, Saccharomyces cerevisiae expresses two, Tor1 and Tor2, which are thought to share all of the rapamycin-sensitive functions attributable to Tor signaling. Here we conducted a genetic screen that defined the global TOR1 synthetic fitness or lethal interaction gene network. This screen identified mutations in distinctive functional categories that impaired vacuolar function, including components of the EGO/Gse and PAS complexes that reduce fitness. In addition, tor1 is lethal in combination with mutations in class C Vps complex components. We find that Tor1 does not regulate the known function of the class C Vps complex in protein sorting. Instead class C vps mutants fail to recover from rapamycin-induced growth arrest or to survive nitrogen starvation and have low levels of amino acids. Remarkably, addition of glutamate or glutamine restores viability to a tor1 pep3 mutant strain. We conclude that Tor1 is more effective than Tor2 at providing rapamycin-sensitive Tor signaling under conditions of amino acid limitation, and that an intact class C Vps complex is required to mediate intracellular amino acid homeostasis for efficient Tor signaling.

AB - The Tor kinases regulate responses to nutrients and control cell growth. Unlike most organisms that only contain one Tor protein, Saccharomyces cerevisiae expresses two, Tor1 and Tor2, which are thought to share all of the rapamycin-sensitive functions attributable to Tor signaling. Here we conducted a genetic screen that defined the global TOR1 synthetic fitness or lethal interaction gene network. This screen identified mutations in distinctive functional categories that impaired vacuolar function, including components of the EGO/Gse and PAS complexes that reduce fitness. In addition, tor1 is lethal in combination with mutations in class C Vps complex components. We find that Tor1 does not regulate the known function of the class C Vps complex in protein sorting. Instead class C vps mutants fail to recover from rapamycin-induced growth arrest or to survive nitrogen starvation and have low levels of amino acids. Remarkably, addition of glutamate or glutamine restores viability to a tor1 pep3 mutant strain. We conclude that Tor1 is more effective than Tor2 at providing rapamycin-sensitive Tor signaling under conditions of amino acid limitation, and that an intact class C Vps complex is required to mediate intracellular amino acid homeostasis for efficient Tor signaling.

UR - http://www.scopus.com/inward/record.url?scp=34548421080&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34548421080&partnerID=8YFLogxK

U2 - 10.1534/genetics.107.072835

DO - 10.1534/genetics.107.072835

M3 - Article

VL - 176

SP - 2139

EP - 2150

JO - Genetics

JF - Genetics

SN - 0016-6731

IS - 4

ER -