The transcriptional response to alkaline pH in <i>Saccharomyces cerevisiae</i>: evidence for calcium‐mediated signalling

Serrano, Raquel; Ruiz, Amparo; Bernal, Dolores; Chambers, James R.; Ariño, Joaquı́n

doi:10.1046/j.1365-2958.2002.03246.x

Cited by 183 publications

(284 citation statements)

References 47 publications

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“…We verified this idea as we showed that activation of FKS2, a well established reporter gene of cell wall defects (6,17,29), in response to Calcofluor White or in a gas1 mutant was reduced upon the removal of the CDRE element present in the promoter of this gene. Interestingly, two recent papers reported the implication of calcium signaling in the tolerance of yeast to antifungal azoles (96) and in transcriptional induction of genes in response to alkaline pH (97). Altogether, these data demonstrate a major contribution of the calcium signaling in adaptation of yeast cells to various stresses.…”

Section: Discussionmentioning

confidence: 68%

Genome-wide Analysis of the Response to Cell Wall Mutations in the Yeast Saccharomyces cerevisiae

Lagorce

Hauser

Labourdette

et al. 2003

Journal of Biological Chemistry

240

280

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Perturbations of the yeast cell wall trigger a repair mechanism that reconfigures its molecular structure to preserve cell integrity. To investigate this mechanism, we compared the global gene expression in five mutant strains, each bearing a mutation (i.e. fks1, kre6, mnn9, gas1, and knr4 mutants) that affects in a different manner the cell wall construction. Altogether, 300 responsive genes were kept based on high stringency criteria during data processing. Functional classification of these differentially expressed genes showed a substantial subset of induced genes involved in cell wall construction and an enrichment of metabolic, energy generation, and cell defense categories, whereas families of genes belonging to transcription, protein synthesis, and cellular growth were underrepresented. Clustering methods isolated a single group of ϳ80 up-regulated genes that could be considered as the stereotypical transcriptional response of the cell wall compensatory mechanism. The in silico analysis of the DNA upstream region of these co-regulated genes revealed pairwise combinations of DNA-binding sites for transcriptional factors implicated in stress and heat shock responses (Msn2/4p and Hsf1p) with Rlm1p and Swi4p, two PKC1-regulated transcription factors involved in the activation genes related to cell wall biogenesis and G 1 /S transition. Moreover, this computational analysis also uncovered the 6-bp 5 -AGCCTC-3 CDRE (calcineurindependent response element) motif in 40% of the coregulated genes. This motif was recently shown to be the DNA binding site for Crz1p, the major effector of calcineurin-regulated gene expression in yeast. Taken altogether, the data presented here lead to the conclusion that the cell wall compensatory mechanism, as triggered by cell wall mutations, integrates three major regulatory systems: namely the PKC1-SLT2 mitogen-activated protein kinase-signaling module, the "global stress" response mediated by Msn2/4p, and the Ca 2؉ /calcineurindependent pathway. The relative importance of these regulatory systems in the cell wall compensatory mechanism is discussed.Yeast and fungi are surrounded by a cell wall that is a complex structure essential for maintenance of the cell shape, prevention of lysis, and protection against harmful environmental conditions. The yeast cell wall architecture has been determined in detail over the past decade (1). It is a layered structure that is composed of ␤-1,3-and ␤-1,6-glucan (50 -60% of the cell wall dry mass), mannoproteins (40 -50%), and chitin (2%). ␤-1,3-Glucan and chitin form a fibrillar network to which mannoproteins are anchored, mostly through ␤-1,6-glucan. Some cell wall proteins, like the PIR family, can be directly linked to ␤-1,3-glucan (reviewed in Ref.2). The cell wall is not a rigid structure, since it endures all of the changes that the cell undergoes during division, morphogenesis, and differentiation.To ensure continuous integrity of the wall in accordance with its plasticity, complex mechanisms must be operating, which need to be strictly ...

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Section: Discussionmentioning

confidence: 68%

Genome-wide Analysis of the Response to Cell Wall Mutations in the Yeast Saccharomyces cerevisiae

Lagorce

Hauser

Labourdette

et al. 2003

Journal of Biological Chemistry

240

280

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“…Possibly, Pho85-Pho80 regulates expression of the high-affinity phosphate transporter Pho89 under alkaline stress response (Serrano et al 2002). It was shown that increasing the extracellular pH to 7.6 leads to induction of PHO84 and PHO89, encoding the high-affinity phosphate transporters, and PHM1, PHM2 and PHM3, encoding the vacuolar polyphosphate synthases.…”

Section: The Protein Kinase Sch9mentioning

confidence: 99%

Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae

et al. 2010

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Cells of all living organisms contain complex signal transduction networks to ensure that a wide range of physiological properties are properly adapted to the environmental conditions. The fundamental concepts and individual building blocks of these signalling networks are generally well-conserved from yeast to man; yet, the central role that growth factors and hormones play in the regulation of signalling cascades in higher eukaryotes is executed by nutrients in yeast. Several nutrient-controlled pathways, which regulate cell growth and proliferation, metabolism and stress resistance, have been defined in yeast. These pathways are integrated into a signalling network, which ensures that yeast cells enter a quiescent, resting phase (G 0 ) to survive periods of nutrient scarceness and that they rapidly resume growth and cell proliferation when nutrient conditions become favourable again. A series of well-conserved nutrient-sensory protein kinases perform key roles in this signalling network: i.e. Snf1, PKA, Tor1 and Tor2, Sch9 and Pho85-Pho80. In this review, we provide a comprehensive overview on the current understanding of the signalling processes mediated via these kinases with a particular focus on how these individual pathways converge to signalling networks that ultimately ensure the dynamic translation of extracellular nutrient signals into appropriate physiological responses.

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“…␤-Galactosidase Assays-The wild type DBY746 strain and its derivatives RSC46 (yvc1⌬), RSC28 (mid1⌬), and RSC31 (cch1⌬) were transformed with the reporter plasmids pAMS366 (10), pMRK212 (14), or pPHO89-lacZ (14). Cultures were centrifuged (5 min at 750 ϫ g), and cells were resuspended in YPD, 50 mM TAPS adjusted to pH 8.0 (containing 10 mM EGTA when required for chelating calcium cations), and incubated for 60 min (pAMS366 and pMRK212) or 90 min (pPHO89-lacZ).…”

Section: Strains and Growthmentioning

confidence: 99%

“…We showed (14) that a significant part of the alkaline response of the ENA1 promoter, and most of the PHO89 response, was blocked by the calcineurin inhibitor FK506 as well as by the absence of Cnb1 or Crz1/Tcn1, suggesting that the transcriptional response of certain genes to alkalinization of the medium could be, at least in part, dependent on calcineurin. These findings led us to speculate the possibility that exposure to alkaline pH could trigger a burst in cytoplasmic calcium, which in turn would activate the phosphatase.…”

mentioning

confidence: 96%

“…Recent evidence from our laboratory (14) supports early data (15,16) showing that calcineurin might be involved in the tolerance to alkaline pH. We showed (14) that a significant part of the alkaline response of the ENA1 promoter, and most of the PHO89 response, was blocked by the calcineurin inhibitor FK506 as well as by the absence of Cnb1 or Crz1/Tcn1, suggesting that the transcriptional response of certain genes to alkalinization of the medium could be, at least in part, dependent on calcineurin.…”

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confidence: 99%

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Characterization of the Calcium-mediated Response to Alkaline Stress in Saccharomyces cerevisiae

Viladevall¹,

Serrano²,

Ruiz³

et al. 2004

Journal of Biological Chemistry

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188

212

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Exposure of the yeast Saccharomyces cerevisiae to alkaline stress resulted in adaptive changes that involved remodeling the gene expression. Recent evidence suggested that the calcium-activated protein phosphatase calcineurin could play a role in alkaline stress signaling. By using an aequorin luminescence reporter, we showed that alkaline stress resulted in a sharp and transient rise in cytoplasmic calcium. This increase was largely abolished by addition of EGTA to the medium or in cells lacking Mid1 or Cch1, components of the high affinity cell membrane calcium channel. Under these circumstances, the alkaline response of different calcineurin-sensitive transcriptional promoters was also blocked. Therefore, exposure to alkali resulted in entry of calcium from the external medium, and this triggered a calcineurin-mediated response. The involvement of calcineurin and Crz1/Tcn1, the transcription factor activated by the phosphatase, in the transcriptional response triggered by alkalinization has been globally assessed by DNA microarray analysis in a time course experiment using calcineurin-deficient (cnb1) and crz1 mutants. We found that exposure to pH 8.0 increased at least 2-fold the mRNA levels of 266 genes. In many cases (60%) the response was rather early (peak after 10 min). The transcriptional response of 27 induced genes (10%) was reduced or fully abolished in cnb1 cells. In general, the response of crz1 mutants was similar to that of calcineurin-deficient cells. By analysis of a systematic deletion library, we found 48 genes whose mutation resulted in increased sensitivity to the calcineurin inhibitor FK506. Twenty of these mutations (42%) also provoked alkaline pH sensitivity. In conclusion, our results demonstrated that calcium signaling and calcineurin activation represented a significant component of the yeast response to environmental alkalinization.Calcium-mediated signaling mechanisms are used by virtually every eukaryotic cell to regulate a wide variety or cellular processes, including gene expression. Transient increases in cytosolic calcium results in activation of diverse enzymes, such as the protein phosphatase calcineurin. Calcineurin is a heterodimer of catalytic subunit and regulatory subunits. In the yeast Saccharomyces cerevisiae, the catalytic subunit is encoded by two genes, CNA1 and CNA2 (1), whereas a single gene, CNB1, encodes the regulatory subunit (2). Cells lacking the catalytic subunits, or the regulatory subunit, are deficient in calcineurin activity.Exposure of yeast cells to a number of signals, such as ␣-factor (3, 4), glucose (5), sphingosine (6), and certain stress conditions (7-9), triggers a rise in cytoplasmic calcium. This increase in calcium can be a consequence of external calcium influx or release from internal stores, such as the vacuole, and results in activation of calcineurin. For instance, hyperosmotic shock has been reported to provoke calcium release from vacuolar stores (8) through Yvc1, a member of the transient receptor potential channel family, and to trig...

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The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium‐mediated signalling

Cited by 183 publications

References 47 publications

Genome-wide Analysis of the Response to Cell Wall Mutations in the Yeast Saccharomyces cerevisiae

Genome-wide Analysis of the Response to Cell Wall Mutations in the Yeast Saccharomyces cerevisiae

Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae

Characterization of the Calcium-mediated Response to Alkaline Stress in Saccharomyces cerevisiae

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