Sfp1 is a Stress- and Nutrient-sensitive Regulator of Ribosomal Protein Gene Expression

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2004 Sep 9

PMID 15353587

Citations 199

Authors

Rosa M Marion

Aviv Regev

Eran Segal

Yoseph Barash

Daphne Koller

Nir Friedman

Erin K OShea

Affiliations

Soon will be listed here.

Abstract

Yeast cells modulate their protein synthesis capacity in response to physiological needs through the transcriptional control of ribosomal protein (RP) genes. Here we demonstrate that the transcription factor Sfp1, previously shown to play a role in the control of cell size, regulates RP gene expression in response to nutrients and stress. Under optimal growth conditions, Sfp1 is localized to the nucleus, bound to the promoters of RP genes, and helps promote RP gene expression. In response to inhibition of target of rapamycin (TOR) signaling, stress, or changes in nutrient availability, Sfp1 is released from RP gene promoters and leaves the nucleus, and RP gene transcription is down-regulated. Additionally, cells lacking Sfp1 fail to appropriately modulate RP gene expression in response to environmental cues. We conclude that Sfp1 integrates information from nutrient- and stress-responsive signaling pathways to help control RP gene expression.

Citing Articles

Regulated resource reallocation is transcriptionally hard wired into the yeast stress response.

Kocik R, Gasch A bioRxiv. 2024; .

PMID: 39677602 PMC: 11642900. DOI: 10.1101/2024.12.03.626567.

TUDCA modulates drug bioavailability to regulate resistance to acute ER stress in .

Chadwick S, Stack-Couture S, Berg M, Di Gregorio S, Lung B, Genereaux J Mol Biol Cell. 2024; 36(2):ar13.

PMID: 39661468 PMC: 11809307. DOI: 10.1091/mbc.E24-04-0147.

The transcription factor FgSfp1 orchestrates mycotoxin deoxynivalenol biosynthesis in Fusarium graminearum.

Sun S, Yu D, Guo M, Tang M, Yan Z, Sun W Commun Biol. 2024; 7(1):1584.

PMID: 39604708 PMC: 11603076. DOI: 10.1038/s42003-024-07265-4.

Engineering transcriptional regulatory networks for improving second-generation fuel ethanol production in .

Sun D, Wu L, Lu X, Li C, Xu L, Li H Synth Syst Biotechnol. 2024; 10(1):207-217.

PMID: 39558946 PMC: 11570414. DOI: 10.1016/j.synbio.2024.10.006.

RNAseq and targeted metabolomics implicate RIC8 in regulation of energy homeostasis, amino acid compartmentation, and asexual development in .

Quinn M, Carrillo A, Halilovic L, Borkovich K mBio. 2024; 15(12):e0313324.

PMID: 39555920 PMC: 11633382. DOI: 10.1128/mbio.03133-24.

References

Warner J . The economics of ribosome biosynthesis in yeast. Trends Biochem Sci. 1999; 24(11):437-40. DOI: 10.1016/s0968-0004(99)01460-7. View

Reinders A, Burckert N, Boller T, Wiemken A, de Virgilio C . Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev. 1998; 12(18):2943-55. PMC: 317170. DOI: 10.1101/gad.12.18.2943. View

Hardwick J, Kuruvilla F, Tong J, Shamji A, Schreiber S . Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc Natl Acad Sci U S A. 1999; 96(26):14866-70. PMC: 24739. DOI: 10.1073/pnas.96.26.14866. View

Cardenas M, Cutler N, Lorenz M, Di Como C, Heitman J . The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 2000; 13(24):3271-9. PMC: 317202. DOI: 10.1101/gad.13.24.3271. View

Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J . Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25(1):25-9. PMC: 3037419. DOI: 10.1038/75556. View

ROBERTSON L, Causton H, Young R, Fink G . The yeast A kinases differentially regulate iron uptake and respiratory function. Proc Natl Acad Sci U S A. 2000; 97(11):5984-8. PMC: 18545. DOI: 10.1073/pnas.100113397. View

Oldham S, Montagne J, Radimerski T, Thomas G, Hafen E . Genetic and biochemical characterization of dTOR, the Drosophila homolog of the target of rapamycin. Genes Dev. 2000; 14(21):2689-94. PMC: 317036. DOI: 10.1101/gad.845700. View

Zhang H, Stallock J, Ng J, Reinhard C, Neufeld T . Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes Dev. 2000; 14(21):2712-24. PMC: 317034. DOI: 10.1101/gad.835000. View

Komeili A, Wedaman K, OShea E, Powers T . Mechanism of metabolic control. Target of rapamycin signaling links nitrogen quality to the activity of the Rtg1 and Rtg3 transcription factors. J Cell Biol. 2000; 151(4):863-78. PMC: 2169436. DOI: 10.1083/jcb.151.4.863. View

10.

Gasch A, Spellman P, Kao C, Eisen M, Storz G, Botstein D . Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell. 2000; 11(12):4241-57. PMC: 15070. DOI: 10.1091/mbc.11.12.4241. View

11.

Riechmann J, Heard J, Martin G, Reuber L, Jiang C, Keddie J . Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000; 290(5499):2105-10. DOI: 10.1126/science.290.5499.2105. View

12.

ROBERTSON L, Fink G . The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci U S A. 1998; 95(23):13783-7. PMC: 24897. DOI: 10.1073/pnas.95.23.13783. View

13.

Powers T, Walter P . Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol Biol Cell. 1999; 10(4):987-1000. PMC: 25225. DOI: 10.1091/mbc.10.4.987. View

14.

Pan X, Heitman J . Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol. 1999; 19(7):4874-87. PMC: 84286. DOI: 10.1128/MCB.19.7.4874. View

15.

Causton H, Ren B, Koh S, Harbison C, Kanin E, Jennings E . Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell. 2001; 12(2):323-37. PMC: 30946. DOI: 10.1091/mbc.12.2.323. View

16.

Rohde J, Heitman J, Cardenas M . The TOR kinases link nutrient sensing to cell growth. J Biol Chem. 2001; 276(13):9583-6. DOI: 10.1074/jbc.R000034200. View

17.

Carroll A, Bishop A, DeRisi J, Shokat K, OShea E . Chemical inhibition of the Pho85 cyclin-dependent kinase reveals a role in the environmental stress response. Proc Natl Acad Sci U S A. 2001; 98(22):12578-83. PMC: 60096. DOI: 10.1073/pnas.211195798. View

18.

Cutler N, Pan X, Heitman J, Cardenas M . The TOR signal transduction cascade controls cellular differentiation in response to nutrients. Mol Biol Cell. 2001; 12(12):4103-13. PMC: 60779. DOI: 10.1091/mbc.12.12.4103. View

19.

Kanehisa M, Goto S, Kawashima S, Nakaya A . The KEGG databases at GenomeNet. Nucleic Acids Res. 2001; 30(1):42-6. PMC: 99091. DOI: 10.1093/nar/30.1.42. View

20.

Dilova I, Chen C, Powers T . Mks1 in concert with TOR signaling negatively regulates RTG target gene expression in S. cerevisiae. Curr Biol. 2002; 12(5):389-95. DOI: 10.1016/s0960-9822(02)00677-2. View