Trehalose Is a Versatile and Long-Lived Chaperone for Desiccation Tolerance

Tapia, Hugo; Koshland, Douglas

doi:10.1016/j.cub.2014.10.005

Cited by 214 publications

(221 citation statements)

References 38 publications

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“…With respect to desiccation, we found that trehalose has no protective effect when wild type cells are subjected to this stress. This is in line with results from Calahan et al (53) showing that mutants defective in trehalose biosynthesis retained wild type levels of desiccation tolerance, whereas a more recent report from the same group (54) proposed that trehalose is only needed for survival during long term (Ͼ2 days) desiccation. Our results also agreed with a previous work of Ratnakumar and Tunnacliffe (52) that pointed out a lack of correlation between trehalose levels and survival of the yeast S. cerevisiae during short-term desiccation.…”

Section: Discussionsupporting

confidence: 90%

Yeast Tolerance to Various Stresses Relies on the Trehalose-6P Synthase (Tps1) Protein, Not on Trehalose

Petitjean

Teste

François

et al. 2015

Journal of Biological Chemistry

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Background: Decades of observations strengthened the idea that trehalose is a chemical chaperone. Results: A catalytically inactive variant of the trehalose-6P synthase (Tps1) maintains cell survival and energy homeostasis under stress exposure. Conclusion: The Tps1 protein itself, not trehalose, is crucial for cell integrity. Significance: This work provides unbiased evidence for an alternative function of Tps1, a new "moonlighting" protein.

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Section: Discussionsupporting

confidence: 90%

Yeast Tolerance to Various Stresses Relies on the Trehalose-6P Synthase (Tps1) Protein, Not on Trehalose

Petitjean

Teste

François

et al. 2015

Journal of Biological Chemistry

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“…Trehalose is abundant in many, but not all, organisms that survive anhydrobiosis, an ametabolic state incurred by desiccation, oxidation, freezing, and heat, and all survived by Artemia during diapause and quiescence (Crowe et al 1992;Singer and Lindquist 1998a, b;Tunnacliffe et al 2005;Ratnakumar and Tunnacliffe 2006;Hengherr et al 2008;Erkut et al 2011Erkut et al , 2013Morano 2014;Tapia and Koshland 2014). Trehalose preserves membranes by blocking fusion, thus averting leakiness, and by lowering transition temperature (T m ), the latter proposed to come about by different but overlapping processes as follows (Crowe et al 1987(Crowe et al , 1992Clegg and Trotman 2002;Crowe 2007;Erkut et al 2011;Hengherr et al 2011).…”

Section: Trehalose and Stress Tolerance In Artemia Cystsmentioning

confidence: 99%

“…Stabilization favors protein renaturation by Hsp104 which, with trehalose, is strongly induced in moderately stressed and stationary-phase yeast. Hsp104, an energyrequiring molecular chaperone, promotes short-term dehydration tolerance in yeast (Tapia and Koshland 2014). Conversely, trehalose maintains both short-and long-term protein homeostasis by an energy-independent mechanism effective even when organisms experience metabolic depression, desiccation, and ATP limitation, as occur in Artemia cysts during diapause and quiescence (Crowe et al 1987;Tapia and Koshland 2014).…”

Section: Trehalose and Stress Tolerance In Artemia Cystsmentioning

confidence: 99%

“…Hsp104, an energyrequiring molecular chaperone, promotes short-term dehydration tolerance in yeast (Tapia and Koshland 2014). Conversely, trehalose maintains both short-and long-term protein homeostasis by an energy-independent mechanism effective even when organisms experience metabolic depression, desiccation, and ATP limitation, as occur in Artemia cysts during diapause and quiescence (Crowe et al 1987;Tapia and Koshland 2014). Trehalose protects proteins if the chaperone system is overwhelmed or when there is insufficient energy for ATP-dependent chaperones to operate.…”

Section: Trehalose and Stress Tolerance In Artemia Cystsmentioning

confidence: 99%

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Stress tolerance during diapause and quiescence of the brine shrimp, Artemia

MacRae

2016

Cell Stress and Chaperones

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Oviparously developing embryos of the brine shrimp, Artemia, arrest at gastrulation and are released from females as cysts before entering diapause, a state of dormancy and stress tolerance. Diapause is terminated by an external signal, and growth resumes if conditions are permissible. However, if circumstances are unfavorable, cysts enter quiescence, a dormant stage that continues as long as adverse conditions persist. Artemia embryos in diapause and quiescence are remarkably resistant to environmental and physiological stressors, withstanding desiccation, cold, heat, oxidation, ultraviolet radiation, and years of anoxia at ambient temperature when fully hydrated. Cysts have adapted to stress in several ways; they are surrounded by a rigid cell wall impermeable to most chemical compounds and which functions as a shield against ultraviolet radiation. Artemia cysts contain large amounts of trehalose, a non-reducing sugar thought to preserve membranes and proteins during desiccation by replacing water molecules and/or contributing to vitrification. Late embryogenesis abundant proteins similar to those in seeds and other anhydrobiotic organisms are found in cysts, and they safeguard cell organelles and proteins during desiccation. Artemia cysts contain abundant amounts of p26, a small heat shock protein, and artemin, a ferritin homologue, both ATPindependent molecular chaperones important in stress tolerance. The evidence provided in this review supports the conclusion that it is the interplay of these protective elements that make Artemia one of the most stress tolerant of all metazoan organisms.

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“…However, in saturated cultures, yeast cells accumulate high levels of a number of stress effectors, including extremely high levels of trehalose (up to 15% of dry cell mass) (6,7). We recently showed that high levels of trehalose are necessary for yeast cells in saturated cultures to survive weeks to months of desiccation (long term), but not a few days (short term) (9). Trehalose dispensability during short-term desiccation is due in part to overlapping functions with the heat shock factor Hsp104.…”

mentioning

confidence: 99%

Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae

Tapia

Young

Fox³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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154

132

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Diverse organisms capable of surviving desiccation, termed anhydrobiotes, include species from bacteria, yeast, plants, and invertebrates. However, most organisms are sensitive to desiccation, likely due to an assortment of different stresses such as protein misfolding and aggregation, hyperosmotic stress, membrane fracturing, and changes in cell volume and shape leading to an overcrowded cytoplasm and metabolic arrest. The exact stress(es) that cause lethality in desiccation-sensitive organisms and how the lethal stresses are mitigated in desiccation-tolerant organisms remain poorly understood. The presence of trehalose in anhydrobiotes has been strongly correlated with desiccation tolerance. In the yeast Saccharomyces cerevisiae, trehalose is essential for survival after long-term desiccation. Here, we establish that the elevation of intracellular trehalose in dividing yeast by its import from the media converts yeast from extreme desiccation sensitivity to a high level of desiccation tolerance. This trehalose-induced tolerance is independent of utilization of trehalose as an energy source, de novo synthesis of other stress effectors, or the metabolic effects of trehalose biosynthetic intermediates, indicating that a chemical property of trehalose is directly responsible for desiccation tolerance. Finally, we demonstrate that elevated intracellular maltose can also make dividing yeast tolerant to short-term desiccation, indicating that other disaccharides have stress effector activity. However, trehalose is much more effective than maltose at conferring tolerance to long-term desiccation. The effectiveness and sufficiency of trehalose as an antagonizer of desiccation-induced damage in yeast emphasizes its potential to confer desiccation tolerance to otherwise sensitive organisms.trehalose | desiccation | yeast | anhydrobiosis | stress

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Trehalose Is a Versatile and Long-Lived Chaperone for Desiccation Tolerance

Abstract: Our results suggest that trehalose is both a more stable and more versatile protectant than protein chaperones, explaining its important role in desiccation tolerance and emphasizing the translational potential of small chemical chaperones as stress effectors.

Cited by 214 publications

References 38 publications

Yeast Tolerance to Various Stresses Relies on the Trehalose-6P Synthase (Tps1) Protein, Not on Trehalose

Yeast Tolerance to Various Stresses Relies on the Trehalose-6P Synthase (Tps1) Protein, Not on Trehalose

Stress tolerance during diapause and quiescence of the brine shrimp, Artemia

Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae

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