The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures

Davidson, George S.; Joe, Ray; Roy, Sushmita; Meirelles, Osorio; Allen, Chris; Wilson, Melissa R.; Tapia, Phillip H.; Manzanilla, Elaine; Dodson, Anne E.; Chakraborty, Swagata; Carter, Mark; Young, Susan; Edwards, Bruce S.; Sklar, Larry A.; Werner‐Washburne, Margaret

doi:10.1091/mbc.e10-06-0499

Cited by 90 publications

(139 citation statements)

References 56 publications

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“…However, by determining the replicative age, we found that these groups are not identical, as the subpopulation of cells with dynamic actin consisted not only of daughter cells but also of mother cells. This situation resembles a new model for the differentiation of Q and NQ cells (61). This recent model shows that cell fate is decided at or before glucose exhaustion.…”

Section: Fig 11mentioning

confidence: 75%

The Stationary-Phase Cells of Saccharomyces cerevisiae Display Dynamic Actin Filaments Required for Processes Extending Chronological Life Span

Vašicová

Lejskova

Malcová

et al. 2015

Molecular and Cellular Biology

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Stationary-growth-phase Saccharomyces cerevisiae yeast cultures consist of nondividing cells that undergo chronological aging. For their successful survival, the turnover of proteins and organelles, ensured by autophagy and the activation of mitochondria, is performed. Some of these processes are engaged in by the actin cytoskeleton. In S. cerevisiae stationary-phase cells, F actin has been shown to form static aggregates named actin bodies, subsequently cited to be markers of quiescence. Our in vivo analyses revealed that stationary-phase cultures contain cells with dynamic actin filaments, besides the cells with static actin bodies. The cells with dynamic actin displayed active endocytosis and autophagy and well-developed mitochondrial networks. Even more, stationary-phase cell cultures grown under calorie restriction predominantly contained cells with actin cables, confirming that the presence of actin cables is linked to successful adaptation to stationary phase. Cells with actin bodies were inactive in endocytosis and autophagy and displayed aberrations in mitochondrial networks. Notably, cells of the respiratory activity-deficient cox4⌬ strain displayed the same mitochondrial aberrations and actin bodies only. Additionally, our results indicate that mitochondrial dysfunction precedes the formation of actin bodies and the appearance of actin bodies corresponds to decreased cell fitness. We conclude that the F-actin status reflects the extent of damage that arises from exponential growth.O nce glucose and other external nutrients are exhausted, cell division stops and Saccharomyces cerevisiae cells are able to survive for extended periods of time. This period of survival has been termed chronological aging and has become a model for aging of postmitotic tissues (1, 2). The cells in these nondividing stationary-phase cell cultures are often termed quiescent (Q) cells (3, 4). Some authors claim that stationary-phase yeast cell populations are heterogeneous and only a portion of them have characteristics of quiescence (5, 6). The ability to survive the period of scarcity of external nutrition and reproduce again upon refeeding is influenced by several life span-extending genetic and environmental interventions. One of the most cited is calorie restriction (CR) (7).In general, cells that are in a nutrient-poor environment activate processes that help them to efficiently utilize inner resources and thus prolong the life span. A catabolic process that has a positive impact on chronological aging is autophagy, which provides nutrients by the vacuolar degradation of damaged or superfluous macromolecules and organelles (8, 9). In addition, Fabrizio et al. demonstrated that the deletion of several genes encoding endosomal functions also shortens the life span (8). Note that some of them have not been directly implicated in autophagy (8). The efficient utilization of resources is ensured by the activation of mitochondrial respiration. It has been proved that the utilization of carbohydrate stores by respiration instead...

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Section: Fig 11mentioning

confidence: 75%

The Stationary-Phase Cells of Saccharomyces cerevisiae Display Dynamic Actin Filaments Required for Processes Extending Chronological Life Span

Vašicová

Lejskova

Malcová

et al. 2015

Molecular and Cellular Biology

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“…In starved batch cultures, yeast CLS depends on respiration, not fermentation (67), as long-lived quiescent cells respire nonfermentable carbon that arises from autophagous nonquiescent cells (68). Immobilized yeast under calorie-unrestricted conditions exhibits long CLS in the absence of respiration, which is precluded in ICRs by glucose repression and low O 2 tension.…”

Section: Two-class Sam Reveals Immobilization-specific Changes In Genmentioning

confidence: 99%

Uncoupling reproduction from metabolism extends chronological lifespan in yeast

Nagarajan

Kruckeberg

Schmidt

et al. 2014

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

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Studies of replicative and chronological lifespan in Saccharomyces cerevisiae have advanced understanding of longevity in all eukaryotes. Chronological lifespan in this species is defined as the agedependent viability of nondividing cells. To date this parameter has only been estimated under calorie restriction, mimicked by starvation. Because postmitotic cells in higher eukaryotes often do not starve, we developed a model yeast system to study cells as they age in the absence of calorie restriction. Yeast cells were encapsulated in a matrix consisting of calcium alginate to form ∼3 mm beads that were packed into bioreactors and fed ad libitum. Under these conditions cells ceased to divide, became heat shock and zymolyase resistant, yet retained high fermentative capacity. Over the course of 17 d, immobilized yeast cells maintained >95% viability, whereas the viability of starving, freely suspended (planktonic) cells decreased to <10%. Immobilized cells exhibited a stable pattern of gene expression that differed markedly from growing or starving planktonic cells, highly expressing genes in glycolysis, cell wall remodeling, and stress resistance, but decreasing transcription of genes in the tricarboxylic acid cycle, and genes that regulate the cell cycle, including master cyclins CDC28 and CLN1. Stress resistance transcription factor MSN4 and its upstream effector RIM15 are conspicuously up-regulated in the immobilized state, and an immobilized rim15 knockout strain fails to exhibit the long-lived, growth-arrested phenotype, suggesting that altered regulation of the Rim15-mediated nutrient-sensing pathway plays an important role in extending yeast chronological lifespan under calorie-unrestricted conditions. cell longevity | Ca-alginate encapsulation U nicellular microbes senesce and die (for reviews, see refs.

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“…Peptide N-glycanase activity is difficult to detect in exponentially growing yeast and increases during post-diauxic growth (22), and Png1p abundance is higher in stationary cells than in exponentially growing cells (23). Likewise, Ams1p-dependent p-nitrophenyl-Man hydrolyzing activity is low in exponential yeast cultures and increases during post-diauxic growth (24).…”

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confidence: 99%

Endoplasmic Reticulum-associated Degradation (ERAD) and Free Oligosaccharide Generation in Saccharomyces cerevisiae

Chantret

Kodali

Lahmouich

et al. 2011

Journal of Biological Chemistry

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Background: Yeast free oligosaccharides (fOS) are cleaved from glycoproteins during ER-associated degradation of proteins (ERAD), but factors underlying their control remain to be explored. Results: Only one-half of fOS are regulated by known ERAD processes, and fOS generation and demannosylation are growth-dependent. Conclusion: Additional complexity of ERAD processes is revealed. Significance: This is the first demonstration of growth-dependent fOS regulation.

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The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures

Cited by 90 publications

References 56 publications

The Stationary-Phase Cells of Saccharomyces cerevisiae Display Dynamic Actin Filaments Required for Processes Extending Chronological Life Span

The Stationary-Phase Cells of Saccharomyces cerevisiae Display Dynamic Actin Filaments Required for Processes Extending Chronological Life Span

Uncoupling reproduction from metabolism extends chronological lifespan in yeast

Endoplasmic Reticulum-associated Degradation (ERAD) and Free Oligosaccharide Generation in Saccharomyces cerevisiae

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