Characterization of Differentiated Quiescent and Nonquiescent Cells in Yeast Stationary-Phase Cultures

Aragon, Anthony D.; Rodriguez, Angelina L.; Meirelles, Osorio; Roy, Sushmita; Davidson, George S.; Tapia, Phillip H.; Allen, Chris; Joe, Ray; Benn, Don; Werner‐Washburne, Margaret

doi:10.1091/mbc.e07-07-0666

Cited by 131 publications

(207 citation statements)

References 67 publications

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“…We found no requirement for several chromatin factors implicated in expression memory, including the deacetylase SIR2, the Pho23p subunit of the Rpd3-large histone deacetylase complex, or the histone variant H2A.z (Q. Guan and A. P. Gasch, unpublished data). We also found no significant differences in transcript abundance after cells had re-acclimated to stress-free medium, nor evidence of a sequestered pool of nontranslated, stored mRNAs (Aragon et al 2008) (data not shown). These negative results are consistent with the dispensability of nascent protein synthesis in maintaining the memory of H 2 O 2 tolerance.…”

Section: Mechanism Of Cellular Memory Of Stress Resistancementioning

confidence: 71%

Cellular Memory of Acquired Stress Resistance inSaccharomyces cerevisiae

et al. 2012

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Cellular memory of past experiences has been observed in several organisms and across a variety of experiences, including bacteria "remembering" prior nutritional status and amoeba "learning" to anticipate future environmental conditions. Here, we show that Saccharomyces cerevisiae maintains a multifaceted memory of prior stress exposure. We previously demonstrated that yeast cells exposed to a mild dose of salt acquire subsequent tolerance to severe doses of H 2 O 2 . We set out to characterize the retention of acquired tolerance and in the process uncovered two distinct aspects of cellular memory. First, we found that H 2 O 2 resistance persisted for four to five generations after cells were removed from the prior salt treatment and was transmitted to daughter cells that never directly experienced the pretreatment. Maintenance of this memory did not require nascent protein synthesis after the initial salt pretreatment, but rather required long-lived cytosolic catalase Ctt1p that was synthesized during salt exposure and then distributed to daughter cells during subsequent cell divisions. In addition to and separable from the memory of H 2 O 2 resistance, these cells also displayed a faster gene-expression response to subsequent stress at .1000 genes, representing transcriptional memory. The faster gene-expression response requires the nuclear pore component Nup42p and serves an important function by facilitating faster reacquisition of H 2 O 2 tolerance after a second cycle of salt exposure. Memory of prior stress exposure likely provides a significant advantage to microbial populations living in ever-changing environments. N ATURAL environments are complex and often vary significantly in space and time, posing challenges for the organisms living within them. Single-cell organisms are particularly vulnerable, since variation in external conditions can directly impact internal homeostasis. Therefore, preparing for environmental change after early signs of fluctuation would present a significant advantage for cells growing in the wild. Indeed, many organisms can become tolerant to severe stress after an initial mild pretreatment with the same or a different stressor. This response, termed "acquired stress resistance," has been observed in microbes such as bacteria and yeast as well as in multicellular organisms including worms, plants, mammals, and even humans (Lu et al. 1993;Davies et al. 1995;Lewis et al. 1995;Lou and Yousef 1997;Swan and Watson 1999;Chi and Arneborg 2000;Schenk et al. 2000;Durrant and Dong 2004;Kandror et al. 2004;Scholz et al. 2005;Hecker et al. 2007;Kensler et al. 2007;Matsumoto et al. 2007). The conservation of this response suggests that it plays an important role in surviving environmental stress in diverse species.We previously conducted a systematic analysis of acquired stress resistance in Saccharomyces cerevisiae and found that the response is common, but not universal, for all pairs of stress treatments (Berry and Gasch 2008). The level and duration of mild-stress pretreatme...

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Section: Mechanism Of Cellular Memory Of Stress Resistancementioning

confidence: 71%

Cellular Memory of Acquired Stress Resistance inSaccharomyces cerevisiae

et al. 2012

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“…Although potentially interesting, it is not yet clear why only half of the cells in these stationary-phase cultures appear to be able to form cytoplasmic granules. One interesting possibility is suggested by previous work indicating that only 50% of the cells in stationary-phase cultures exhibit the ability to remain viable for long periods of time (Allen et al 2006;Aragon et al 2008). These cells have been termed the Q, or quiescent, fraction of this population and may correspond to those cells that have a focus in our studies here.…”

Section: Resultsmentioning

confidence: 92%

Protein Kinases Are Associated with Multiple, Distinct Cytoplasmic Granules in Quiescent Yeast Cells

Shah¹,

Nostramo²,

Zhang³

et al. 2014

Genetics

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The cytoplasm of the eukaryotic cell is subdivided into distinct functional domains by the presence of a variety of membrane-bound organelles. The remaining aqueous space may be further partitioned by the regulated assembly of discrete ribonucleoprotein (RNP) complexes that contain particular proteins and messenger RNAs. These RNP granules are conserved structures whose importance is highlighted by studies linking them to human disorders like amyotrophic lateral sclerosis. However, relatively little is known about the diversity, composition, and physiological roles of these cytoplasmic structures. To begin to address these issues, we examined the cytoplasmic granules formed by a key set of signaling molecules, the protein kinases of the budding yeast Saccharomyces cerevisiae. Interestingly, a significant fraction of these proteins, almost 20%, was recruited to cytoplasmic foci specifically as cells entered into the G 0 -like quiescent state, stationary phase. Colocalization studies demonstrated that these foci corresponded to eight different granules, including four that had not been reported previously. All of these granules were found to rapidly disassemble upon the resumption of growth, and the presence of each was correlated with cell viability in the quiescent cultures. Finally, this work also identified new constituents of known RNP granules, including the well-characterized processing body and stress granule. The composition of these latter structures is therefore more varied than previously thought and could be an indicator of additional biological activities being associated with these complexes. Altogether, these observations indicate that quiescent yeast cells contain multiple distinct cytoplasmic granules that may make important contributions to their long-term survival.

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“…This suggests that biological heterogeneity is still somehow triggered by genetic heterogeneity. This is also supported by the fact that Aragon et al (2008) identified mutations affecting reproductive capacity and/or viability.…”

Section: Discussionmentioning

confidence: 73%

“…Weinberger et al (2007) showed that yeast cells more efficiently able to arrest in G1 phase when entering into stationary phase exhibited longer chronological lifespans than cells arrested in S phase. The study of gene expression in quiescent and nonquiescent cells (Aragon et al, 2008) showed that nonquiescent cells seemed unable to arrest growth. In contrast, quiescent cells exhibited gene expression showing they had the capacity to survive prolonged starvation and to respond quickly if conditions became favorable to growth.…”

Section: Discussionmentioning

confidence: 99%

Plasticity of death rates in stationary phase in Saccharomyces cerevisiae

et al. 2009

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SummaryFor the species that have been most carefully studied, mortality rises with age and then plateaus or declines at advanced ages, except for yeast. Remarkably, mortality for yeast can rise, fall and rise again. In the present study we investigated (i) if this complicated shape could be modulated by environmental conditions by measuring mortality with different food media and temperature; (ii) if it is triggered by biological heterogeneity by measuring mortality in stationary phase in populations fractionated into subpopulations of young, virgin cells, and replicatively older, non-virgin cells. We also discussed the results of a staining method to measure viability instead of measuring the number of cells able to exit stationary phase and form a colony. We showed that different shapes of age-specific death rates were observed and that their appearance depended on the environmental conditions. Furthermore, biological heterogeneity explained the shapes of mortality with homogeneous populations of young, virgin cells exhibiting a simple shape of mortality in conditions under which more heterogeneous populations of older cells or unfractionated populations displayed complicated death rates. Finally, the staining method suggested that cells lost the capacity to exit stationary phase and to divide long before they died in stationary phase. These results explain a phenomenon that was puzzling because it appeared to reflect a radical departure from mortality patterns observed for other species.

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Characterization of Differentiated Quiescent and Nonquiescent Cells in Yeast Stationary-Phase Cultures

Cited by 131 publications

References 67 publications

Cellular Memory of Acquired Stress Resistance inSaccharomyces cerevisiae

Cellular Memory of Acquired Stress Resistance inSaccharomyces cerevisiae

Protein Kinases Are Associated with Multiple, Distinct Cytoplasmic Granules in Quiescent Yeast Cells

Plasticity of death rates in stationary phase in Saccharomyces cerevisiae

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