Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Transcriptional Response According to Strength of Calorie Restriction in Saccharomyces cerevisiae

  • Lee, Yae-Lim (College of Life Sciences and Biotechnology, Korea University) ;
  • Lee, Cheol-Koo (College of Life Sciences and Biotechnology, Korea University)
  • Received : 2008.04.17
  • Accepted : 2008.05.22
  • Published : 2008.09.30
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Abstract

To characterize gene expression that is dependent on the strength of calorie restriction (CR), we obtained transcriptome at different levels of glucose, which is a major energy and carbon source for budding yeast. To faithfully mimic mammalian CR in yeast culture, we reconstituted and grew seeding yeast cells in fresh 2% YPD media before inoculating into 2%, 1%, 0.5% and 0.25% YPD media to reflect different CR strengths. We collected and characterized 160 genes that responded to CR strength based on the rigorous statistical analyses of multiple test corrected ANOVA (adjusted p value < 0.1 or raw p value < 0.0031) and Pearson correlation (|r| > 0.7). Based on the individual gene studies and the GO Term Finder analysis of 160 genes, we found that CR dose-dependently and gradually increased mitochondrial function at the transcriptional level. Therefore, we suggest these 160 genes are markers that respond to CR strength and that might be useful in elucidating CR mechanisms, especially how stronger CR extends life span more.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation

References

  1. Anderson, R.M., Bitterman, K.J., Wood, J.G., Medvedik, O., and Sinclair, D.A. (2003). Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cervisiae. Nature 423, 181-185 https://doi.org/10.1038/nature01578
  2. Askwith, C., Eide, D., Van Ho, A., Bernard, P.S., Li, L., Davis- Kaplan, S., Sipe, D.M., and Kaplan, J. (1994). The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76, 403-410 https://doi.org/10.1016/0092-8674(94)90346-8
  3. Bedalov, A., Hirao, M., Posakony, J., Nelson, M., and Simon, J.A. (2003). NAD+-dependent deacetylase Hst1p controls biosynthesis and cellular NAD+ levels in Saccharomyces cervisiae. Mol. Cell. Biol. 23, 7044-7054 https://doi.org/10.1128/MCB.23.19.7044-7054.2003
  4. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. Royal Statistical Soc. Series B-Methodological 57, 289-300
  5. Bianconi, M.L. (2003). Calorimetric determination of thermodynamic parameters of reaction reveals different enthalpic compensations of the yeast hexokinase isozymes. J. Biol. Chem. 278, 18709-18713 https://doi.org/10.1074/jbc.M211103200
  6. Bonawitz, N.D., Chatenay-Lapointe, M., Pan, Y., and Shadel, G.S. (2007). Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab. 5, 265-277 https://doi.org/10.1016/j.cmet.2007.02.009
  7. Boyle, E.I., Weng, S., Gollub, J., Jin, H., Botstein, D., Cherry, J.M., and Sherlock, G. (2004). GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 20, 3710-3715 https://doi.org/10.1093/bioinformatics/bth456
  8. Clifton, D., Walsh, R.B., and Fraenkel, D.G. (1993). Functional studies of yeast glucokinase. J. Bacteriol. 175, 3289-3294 https://doi.org/10.1128/jb.175.11.3289-3294.1993
  9. Diderich, J.A., Schuurmans, J.M., Van Gaalen, M.C., Kruckeberg, A.L., and Van Dam, K. (2001). Functional analysis of the hexose transporter homologue HXT5 in Saccharomyces cervisiae. Yeast 18, 1515-1524 https://doi.org/10.1002/yea.779
  10. Do, J.H., and Choi, D.K. (2006). Normalization of microarray data: single-labeled and dual-labeled arrays. Mol. Cells 22, 254-261
  11. Fabrizio, P., Gattazzo, C., Battistella, L., Wei, M., Cheng, C., McGrew, K., and Longo, V.D. (2005). Sir2 blocks extreme lifespan extension. Cell 123, 655-667 https://doi.org/10.1016/j.cell.2005.08.042
  12. Haurie, V., Boucherie, H., and Sagliocco, F. (2003). The Snf1 protein kinase controls the induction of genes of the iron uptake pathway at the diauxic shift in Saccharomyces cervisiae. J. Biol. Chem. 278, 45391-45396 https://doi.org/10.1074/jbc.M307447200
  13. Kaeberlein, M., McVey, M., and Guarente, L. (1999). The SIR2/3/4 complex and SIR2 alone promote longevity inSaccharomyces cervisiae by two different mechanisms. Genes Dev. 13, 2570-2580 https://doi.org/10.1101/gad.13.19.2570
  14. Kaeberlein, M., Kirkland, K.T., Fields, S., and Kennedy, B.K. (2004). Sir2-independent life span extension by calorie restriction in yeast. PLoS Biol. 2, E296 https://doi.org/10.1371/journal.pbio.0020296
  15. Kim, J.H., Polish, J., and Johnston, M. (2003). Specificity and regulation of DNA binding by the yeast glucose transporter gene repressor Rgt1. Mol. Cell. Biol. 23, 5208-5216 https://doi.org/10.1128/MCB.23.15.5208-5216.2003
  16. Kresnowati, M.T., van Winden, W.A., Almering, M.J., ten Pierick, A., Ras, C., Knijnenburg, T.A., Daran-Lapujade, P., Pronk, J.T., Heijnen, J.J., and Daran, J.M. (2006). When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol. Syst. Biol. 2, 49
  17. Lin, S.J., Defossez, P.A., and Guarente, L. (2000). Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cervisiae. Science 289, 2126-2128 https://doi.org/10.1126/science.289.5487.2126
  18. Lin, S.J., Kaeberlein, M., Andalis, A.A., Sturtz, L.A., Defossez, P.A., Culotta, V.C., Fink, G.R., and Guarente, L. (2002). Calorie restriction extends Saccharomyces cervisiae lifespan by increasing respiration. Nature. 418, 344-348 https://doi.org/10.1038/nature00829
  19. Lin, S.J., Ford, E., Haigis, M., Liszt, G., and Guarente, L. (2004). Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev. 18, 12-16 https://doi.org/10.1101/gad.1164804
  20. Moriya, H., and Johnston, M. (2004). Glucose sensing and signaling in Saccharomyces cerevisiae through the Rgt2 glucose sensor and casein kinase I. Proc. Natl. Acad. Sci. USA 101, 1572-1577
  21. Mosley, A.L., Lakshmanan, J., Aryal, B.K., and Ozcan, S. (2003). Glucose-mediated phosphorylation converts the transcription factor Rgt1 from a repressor to an activator. J. Biol. Chem. 278, 10322-10327 https://doi.org/10.1074/jbc.M212802200
  22. Nadon, R., and Shoemaker, J. (2002). Statistical issues with microarrays: processing and analysis. Trends Genet. 18, 265-271 https://doi.org/10.1016/S0168-9525(02)02665-3
  23. Ozcan, S., and Johnston, M. (1995). Three different regulatory mechanisms enable yeast hexose transporter (HXT) genes to be induced by different levels of glucose. Mol. Cell. Biol.15, 1564-1572 https://doi.org/10.1128/MCB.15.3.1564
  24. Ozcan, S., and Johnston, M. (1999). Function and regulation of yeast hexose transporters. Microbiol. Mol. Biol. Rev. 63, 554-569
  25. Park, S.K., and Prolla, T.A. (2005). Lessons learned from gene expression profile studies of aging and caloric restriction. Ageing Res. Rev.4, 55-65 https://doi.org/10.1016/j.arr.2004.09.003
  26. Philpott, C.C., Protchenko, O., Kim, Y.W., Boretsky, Y., and Shakoury-Elizeh, M. (2002). The response to iron deprivation in Saccharomyces cervisiae: expression of siderophore-based systems of iron uptake. Biochem. Soc. Trans. 30, 698-702 https://doi.org/10.1042/BST0300698
  27. Protchenko, O., and Philpott, C.C. (2003). Regulation of intracellular heme levels by HMX1, a homologue of heme oxygenase, in Saccharomyces cervisiae. J. Biol. Chem. 278, 36582-36587 https://doi.org/10.1074/jbc.M306584200
  28. Reifenberger, E., Boles, E., and Ciriacy, M. (1997). Kinetic characterization of individual hexose transporters of Saccharomyces cervisiae and their relation to the triggering mechanisms of glucose repression. Eur. J. Biochem. 245, 324-333 https://doi.org/10.1111/j.1432-1033.1997.00324.x
  29. Ronen, M., and Botstein, D. (2006). Transcriptional response of steady-state yeast cultures to transient perturbations in carbon source. Proc. Natl. Acad. Sci. USA 103, 389-394
  30. Shakoury-Elizeh, M., Tiedeman, J., Rashford, J., Ferea, T., Demeter, J., Garcia, E., Rolfes, R., Brown, P.O., Botstein, D., and Philpott, C.C. (2004). Transcriptional remodeling in response to iron deprivation in Saccharomyces cervisiae. Mol. Biol. Cell. 15, 1233-1243 https://doi.org/10.1091/mbc.E03-09-0642
  31. Speakman, J.R., and Hambly, C. (2007). Starving for life: what animal studies can and cannot tell us about the use of caloric restriction to prolong human lifespan. J. Nutr. 137, 1078-1086
  32. Stearman, R., Yuan, D.S., Yamaguchi-Iwai, Y., Klausner, R.D., and Dancis, A. (1996). A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271, 1552-1557 https://doi.org/10.1126/science.271.5255.1552
  33. Thon, V.J., Vigneron-Lesens, C., Marianne-Pepin, T., Montreuil, J., Decq, A., Rachez, C., Ball, S.G., and Cannon, J.F. (1992). Coordinate regulation of glycogen metabolism in the yeast Saccharomyces cervisiae. Induction of glycogen branching enzyme. J. Biol. Chem.267, 15224-15228.
  34. Tissenbaum, H.A., and Guarente, L. (2001). Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410, 227-230 https://doi.org/10.1038/35065638
  35. Walsh, R.B., Kawasaki, G., and Fraenkel, D.G. (1983). Cloning of genes that complement yeast hexokinase and glucokinase mutants. J. Bacteriol. 154, 1002-1004
  36. Yang, H., Yang, T., Baur, J.A., Perez, E., Matsui, T., Carmona, J.J., Lamming, D.W., Souza-Pinto, N.C., Bohr, V.A., Rosenzweig, A., et al. (2007). Nutrient-sensitive mitochondrial NAD(+) levels dictate cell survival. Cell 130, 1095-1107 https://doi.org/10.1016/j.cell.2007.07.035
  37. Yin, Z., Wilson, S., Hauser, N.C., Tournu, H., Hoheisel, J.D., and Brown, A.J. (2003). Glucose triggers different global responses in yeast, depending on the strength of the signal, and transiently stabilizes ribosomal protein mRNAs. Mol. Microbiol. 48, 713-724 https://doi.org/10.1046/j.1365-2958.2003.03478.x
  38. Yun, C.W., Bauler, M., Moore, R.E., Klebba, P.E., and Philpott, C.C. (2001). The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cervisiae. J. Biol. Chem. 276, 10218-10223 https://doi.org/10.1074/jbc.M010065200