Determinants and Regulation of Protein Turnover in Yeast

Overview

Journal Cell Syst

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2017 Sep 18

PMID 28918244

Citations 59

Authors

Miguel Martin-Perez

Judit Villen

Affiliations

Soon will be listed here.

Abstract

Protein turnover maintains the recycling needs of the proteome, and its malfunction has been linked to aging and age-related diseases. However, not all proteins turnover equally, and the factors that contribute to accelerate or slow down turnover are mostly unknown. We measured turnover rates for 3,160 proteins in exponentially growing yeast and analyzed their dependence on physical, functional, and genetic properties. We found that functional characteristics, including protein localization, complex membership, and connectivity, have greater effect on turnover than sequence elements. We also found that protein turnover and mRNA turnover are correlated. Analysis under nutrient perturbation and osmotic stress revealed that protein turnover highly depends on cellular state and is faster when proteins are being actively used. Finally, stress-induced changes in protein and transcript abundance correlated with changes in protein turnover. This study provides a resource of protein turnover rates and principles to understand the recycling needs of the proteome under basal conditions and perturbation.

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References

Thayer N, Leverich C, Fitzgibbon M, Nelson Z, Henderson K, Gafken P . Identification of long-lived proteins retained in cells undergoing repeated asymmetric divisions. Proc Natl Acad Sci U S A. 2014; 111(39):14019-26. PMC: 4191815. DOI: 10.1073/pnas.1416079111. View

Liu Z, Yuan F, Ren J, Cao J, Zhou Y, Yang Q . GPS-ARM: computational analysis of the APC/C recognition motif by predicting D-boxes and KEN-boxes. PLoS One. 2012; 7(3):e34370. PMC: 3315528. DOI: 10.1371/journal.pone.0034370. View

Hammond D, Claydon A, Simpson D, Edward D, Stockley P, Hurst J . Proteome Dynamics: Tissue Variation in the Kinetics of Proteostasis in Intact Animals. Mol Cell Proteomics. 2016; 15(4):1204-19. PMC: 4824850. DOI: 10.1074/mcp.M115.053488. View

Cambridge S, Gnad F, Nguyen C, Lorenzo Bermejo J, Kruger M, Mann M . Systems-wide proteomic analysis in mammalian cells reveals conserved, functional protein turnover. J Proteome Res. 2011; 10(12):5275-84. DOI: 10.1021/pr101183k. View

Petti A, Crutchfield C, Rabinowitz J, Botstein D . Survival of starving yeast is correlated with oxidative stress response and nonrespiratory mitochondrial function. Proc Natl Acad Sci U S A. 2011; 108(45):E1089-98. PMC: 3215077. DOI: 10.1073/pnas.1101494108. View

Rappsilber J, Mann M, Ishihama Y . Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc. 2007; 2(8):1896-906. DOI: 10.1038/nprot.2007.261. View

Hsieh E, Shulman N, Dai D, Vincow E, Karunadharma P, Pallanck L . Topograph, a software platform for precursor enrichment corrected global protein turnover measurements. Mol Cell Proteomics. 2012; 11(11):1468-74. PMC: 3494182. DOI: 10.1074/mcp.O112.017699. View

Soto T, Nunez A, Madrid M, Vicente J, Gacto M, Cansado J . Transduction of centrifugation-induced gravity forces through mitogen-activated protein kinase pathways in the fission yeast Schizosaccharomyces pombe. Microbiology (Reading). 2007; 153(Pt 5):1519-1529. DOI: 10.1099/mic.0.2006/004283-0. View

Geisberg J, Moqtaderi Z, Fan X, Ozsolak F, Struhl K . Global analysis of mRNA isoform half-lives reveals stabilizing and destabilizing elements in yeast. Cell. 2014; 156(4):812-24. PMC: 3939777. DOI: 10.1016/j.cell.2013.12.026. View

10.

Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z . GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009; 10:48. PMC: 2644678. DOI: 10.1186/1471-2105-10-48. View

11.

Cherry J, Hong E, Amundsen C, Balakrishnan R, Binkley G, Chan E . Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 2011; 40(Database issue):D700-5. PMC: 3245034. DOI: 10.1093/nar/gkr1029. View

12.

Gawron D, Ndah E, Gevaert K, Van Damme P . Positional proteomics reveals differences in N-terminal proteoform stability. Mol Syst Biol. 2016; 12(2):858. PMC: 4770386. DOI: 10.15252/msb.20156662. View

13.

Vincow E, Merrihew G, Thomas R, Shulman N, Beyer R, MacCoss M . The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc Natl Acad Sci U S A. 2013; 110(16):6400-5. PMC: 3631677. DOI: 10.1073/pnas.1221132110. View

14.

Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D . Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13(11):2498-504. PMC: 403769. DOI: 10.1101/gr.1239303. View

15.

Lee M, Topper S, Hubler S, Hose J, Wenger C, Coon J . A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol Syst Biol. 2011; 7:514. PMC: 3159980. DOI: 10.1038/msb.2011.48. View

16.

Gracy R, Talent J, Zvaigzne A . Molecular wear and tear leads to terminal marking and the unstable isoforms of aging. J Exp Zool. 1998; 282(1-2):18-27. View

17.

Csardi G, Franks A, Choi D, Airoldi E, Drummond D . Accounting for experimental noise reveals that mRNA levels, amplified by post-transcriptional processes, largely determine steady-state protein levels in yeast. PLoS Genet. 2015; 11(5):e1005206. PMC: 4423881. DOI: 10.1371/journal.pgen.1005206. View

18.

Mishima Y, Tomari Y . Codon Usage and 3' UTR Length Determine Maternal mRNA Stability in Zebrafish. Mol Cell. 2016; 61(6):874-85. DOI: 10.1016/j.molcel.2016.02.027. View

19.

Gibbs D, Bacardit J, Bachmair A, Holdsworth M . The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends Cell Biol. 2014; 24(10):603-11. DOI: 10.1016/j.tcb.2014.05.001. View

20.

Wilkinson D, Ramsdale M . Proteases and caspase-like activity in the yeast Saccharomyces cerevisiae. Biochem Soc Trans. 2011; 39(5):1502-8. DOI: 10.1042/BST0391502. View