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Title: Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter

Abstract

Trehalose is a highly stable, nonreducing disaccharide of glucose. A large body of research exists implicating trehalose in a variety of cellular phenomena, notably response to stresses of various kinds. However, in very few cases has the role of trehalose been examined directly in vivo. Here, we describe the development and characterization of a system in Saccharomyces cerevisiae that allows us to manipulate intracellular trehalose concentrations independently of the biosynthetic enzymes and independently of any applied stress. We found that many physiological roles heretofore ascribed to intracellular trehalose, including heat resistance, are not due to the presence of trehalose per se. We also found that many of the metabolic and growth defects associated with mutations in the trehalose biosynthesis pathway are not abolished by providing abundant intracellular trehalose. Instead, we made the observation that intracellular accumulation of trehalose or maltose (another disaccharide of glucose) is growth-inhibitory in a carbon source-specific manner. We conclude that the physiological role of the trehalose pathway is fundamentally metabolic: i.e., more complex than simply the consequence of increased concentrations of the sugar and its attendant physical properties (with the exception of the companion paper where demonstrate a direct role for trehalose in protecting cells againstmore » desiccation).« less

Authors:
 [1];  [1];  [1];  [1];  [1]
  1. Princeton Univ., Princeton, NJ (United States)
Publication Date:
Research Org.:
Princeton Univ., NJ (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1347586
Grant/Contract Number:  
SC0012461
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 19; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; yeast; trehalose; AGT1; heat shock; carbon source

Citation Formats

Gibney, Patrick A., Schieler, Ariel, Chen, Jonathan C., Rabinowitz, Joshua D., and Botstein, David. Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter. United States: N. p., 2015. Web. doi:10.1073/pnas.1506289112.
Gibney, Patrick A., Schieler, Ariel, Chen, Jonathan C., Rabinowitz, Joshua D., & Botstein, David. Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter. United States. https://doi.org/10.1073/pnas.1506289112
Gibney, Patrick A., Schieler, Ariel, Chen, Jonathan C., Rabinowitz, Joshua D., and Botstein, David. Mon . "Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter". United States. https://doi.org/10.1073/pnas.1506289112. https://www.osti.gov/servlets/purl/1347586.
@article{osti_1347586,
title = {Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter},
author = {Gibney, Patrick A. and Schieler, Ariel and Chen, Jonathan C. and Rabinowitz, Joshua D. and Botstein, David},
abstractNote = {Trehalose is a highly stable, nonreducing disaccharide of glucose. A large body of research exists implicating trehalose in a variety of cellular phenomena, notably response to stresses of various kinds. However, in very few cases has the role of trehalose been examined directly in vivo. Here, we describe the development and characterization of a system in Saccharomyces cerevisiae that allows us to manipulate intracellular trehalose concentrations independently of the biosynthetic enzymes and independently of any applied stress. We found that many physiological roles heretofore ascribed to intracellular trehalose, including heat resistance, are not due to the presence of trehalose per se. We also found that many of the metabolic and growth defects associated with mutations in the trehalose biosynthesis pathway are not abolished by providing abundant intracellular trehalose. Instead, we made the observation that intracellular accumulation of trehalose or maltose (another disaccharide of glucose) is growth-inhibitory in a carbon source-specific manner. We conclude that the physiological role of the trehalose pathway is fundamentally metabolic: i.e., more complex than simply the consequence of increased concentrations of the sugar and its attendant physical properties (with the exception of the companion paper where demonstrate a direct role for trehalose in protecting cells against desiccation).},
doi = {10.1073/pnas.1506289112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 19,
volume = 112,
place = {United States},
year = {Mon Apr 27 00:00:00 EDT 2015},
month = {Mon Apr 27 00:00:00 EDT 2015}
}

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Cited by: 58 works
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Yeast metabolic and signaling genes are required for heat-shock survival and have little overlap with the heat-induced genes
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  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 46
  • DOI: 10.1073/pnas.1318100110

Growth Arrest by Trehalose-6-Phosphate: An Astonishing Case of Primary Metabolite Control over Growth by Way of the SnRK1 Signaling Pathway
journal, July 2011

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Composition and Functional Analysis of the Saccharomyces cerevisiae Trehalose Synthase Complex
journal, December 1998

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Immunological Properties of Trehalose Dimycolate (Cord Factor) and Other Mycotic Acid-Containing Glycolipids--A Review
journal, December 2001


Rapid Expansion and Functional Divergence of Subtelomeric Gene Families in Yeasts
journal, May 2010


Can Trehalose Prevent Neurodegeneration? Insights from Experimental Studies
journal, April 2014


Sugar signals and molecular networks controlling plant growth
journal, June 2010

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Works referencing / citing this record:

Osmolytes ameliorate the effects of stress in the absence of the heat shock protein Hsp104 in Saccharomyces cerevisiae
journal, September 2019


Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature
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Discrete roles of trehalose and Hsp104 in inhibition of protein aggregation in yeast cells
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Osmolytes ameliorate the effects of stress in the absence of the heat shock protein Hsp104 in Saccharomyces cerevisiae
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The trehalose protective mechanism during thermal stress in Saccharomyces cerevisiae: the roles of Ath1 and Agt1
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Common and divergent features of galactose-1-phosphate and fructose-1-phosphate toxicity in yeast
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