Stb3 Plays a Role in the Glucose-induced Transition from Quiescence to Growth in Saccharomyces Cerevisiae

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 2010 Apr 14

PMID 20385783

Citations 23

Authors

Dritan Liko

Michael K Conway

Douglas S Grunwald

Warren Heideman

Affiliations

Soon will be listed here.

Abstract

Addition of glucose to quiescent Saccharomyces cerevisiae cells causes the immediate induction of approximately 1000 genes. These genes include ribosomal proteins (RP) and non-RP genes needed for ribosome production and other growth processes. RRPE sequence elements are commonly found 5' of non-RP growth gene ORFs, and Stb3 has recently been identified as an RRPE binding protein. Stb3 overexpression (Stb3OE) produces a slow growth phenotype that is associated with reduced expression of non-RP genes and a drop in the rate of amino acid incorporation. Genes affected by Stb3 are associated with a TGAAAAA motif. Stb3 is restricted to the nucleus in quiescent cells and is immediately released into the cytoplasm after glucose repletion. The Stb3OE slow growth phenotype is reversed by loss of Hos2 histone deactylase activity, consistent with the idea that repression involves histone deacetylation. SCH9 overexpression or PPH22 deletion, mutations that activate target of rapamycin (Tor) nutrient sensing pathways, also reverse the Stb3OE phenotype. Inhibition of Tor signaling makes the phenotype more severe and restricts Stb3 to the nucleus. The results support a model in which Stb3 is one of the components that repress a large set of growth genes as nutrients are depleted. This repression is ended by glucose.

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References

Zhu C, Byers K, McCord R, Shi Z, Berger M, Newburger D . High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res. 2009; 19(4):556-66. PMC: 2665775. DOI: 10.1101/gr.090233.108. View

van Helden J . Regulatory sequence analysis tools. Nucleic Acids Res. 2003; 31(13):3593-6. PMC: 168973. DOI: 10.1093/nar/gkg567. View

Zaman S, Lippman S, Zhao X, Broach J . How Saccharomyces responds to nutrients. Annu Rev Genet. 2008; 42:27-81. DOI: 10.1146/annurev.genet.41.110306.130206. View

Zurita-Martinez S, Cardenas M . Tor and cyclic AMP-protein kinase A: two parallel pathways regulating expression of genes required for cell growth. Eukaryot Cell. 2005; 4(1):63-71. PMC: 544169. DOI: 10.1128/EC.4.1.63-71.2005. View

Hinnebusch A . Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol. 2005; 59:407-50. DOI: 10.1146/annurev.micro.59.031805.133833. View

Pijnappel W, Schaft D, Roguev A, Shevchenko A, Tekotte H, Wilm M . The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev. 2001; 15(22):2991-3004. PMC: 312828. DOI: 10.1101/gad.207401. View

Urban J, Soulard A, Huber A, Lippman S, Mukhopadhyay D, Deloche O . Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol Cell. 2007; 26(5):663-74. DOI: 10.1016/j.molcel.2007.04.020. View

Jagadish M, Carter B . Genetic control of cell division in yeast cultured at different growth rates. Nature. 1977; 269(5624):145-7. DOI: 10.1038/269145a0. View

Humphrey E, Shamji A, Bernstein B, Schreiber S . Rpd3p relocation mediates a transcriptional response to rapamycin in yeast. Chem Biol. 2004; 11(3):295-9. DOI: 10.1016/j.chembiol.2004.03.001. View

10.

Morano K, Thiele D . The Sch9 protein kinase regulates Hsp90 chaperone complex signal transduction activity in vivo. EMBO J. 1999; 18(21):5953-62. PMC: 1171661. DOI: 10.1093/emboj/18.21.5953. View

11.

Laabs T, Markwardt D, Slattery M, Newcomb L, Stillman D, Heideman W . ACE2 is required for daughter cell-specific G1 delay in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2003; 100(18):10275-80. PMC: 193551. DOI: 10.1073/pnas.1833999100. View

12.

Wullschleger S, Loewith R, Hall M . TOR signaling in growth and metabolism. Cell. 2006; 124(3):471-84. DOI: 10.1016/j.cell.2006.01.016. View

13.

Martinez M, Roy S, Archuletta A, Wentzell P, Anna-Arriola S, Rodriguez A . Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol Biol Cell. 2004; 15(12):5295-305. PMC: 532011. DOI: 10.1091/mbc.e03-11-0856. View

14.

Jiang Y, Broach J . Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J. 1999; 18(10):2782-92. PMC: 1171359. DOI: 10.1093/emboj/18.10.2782. View

15.

Robyr D, Suka Y, Xenarios I, Kurdistani S, Wang A, Suka N . Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell. 2002; 109(4):437-46. DOI: 10.1016/s0092-8674(02)00746-8. View

16.

Huber A, Bodenmiller B, Uotila A, Stahl M, Wanka S, Gerrits B . Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis. Genes Dev. 2009; 23(16):1929-43. PMC: 2725941. DOI: 10.1101/gad.532109. View

17.

Cherkasova V, Hinnebusch A . Translational control by TOR and TAP42 through dephosphorylation of eIF2alpha kinase GCN2. Genes Dev. 2003; 17(7):859-72. PMC: 196024. DOI: 10.1101/gad.1069003. View

18.

Shamji A, Kuruvilla F, Schreiber S . Partitioning the transcriptional program induced by rapamycin among the effectors of the Tor proteins. Curr Biol. 2001; 10(24):1574-81. DOI: 10.1016/s0960-9822(00)00866-6. View

19.

Wedaman K, Reinke A, Anderson S, Yates 3rd J, McCaffery J, Powers T . Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol Biol Cell. 2003; 14(3):1204-20. PMC: 151591. DOI: 10.1091/mbc.e02-09-0609. View

20.

Toda T, Cameron S, Sass P, Wigler M . SCH9, a gene of Saccharomyces cerevisiae that encodes a protein distinct from, but functionally and structurally related to, cAMP-dependent protein kinase catalytic subunits. Genes Dev. 1988; 2(5):517-27. DOI: 10.1101/gad.2.5.517. View