Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast

Molecular Biology of the Cell

Volumn 19, Issue 1, 2008, Pages 352-367

  Brauer, Matthew J ^a,d   Huttenhower, Curtis ^a,b   Airoldi, Edoardo M ^a,b   Rosenstein, Rachel ^a,c   Matese, John C ^a   Gresham, David ^a   Boer, Viktor M ^a   Troyanskaya, Olga G ^a,b   Botstein, David ^a  

^a PRINCETON UNIVERSITY   (United States)

^b Princeton University   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; GLUCOSE; LEUCINE; PHOSPHATE; SULFATE; URACIL;

ANIMAL CELL; ARTICLE; AUXOTROPHY; CELL CULTURE; CELL CYCLE; CELL FRACTIONATION; CELL FUNCTION; CELL GROWTH; CONTROLLED STUDY; FUNGAL GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC CODE; GLUCOSE INTAKE; GLUCOSE METABOLISM; NONHUMAN; NUTRIENT; PEROXISOME; PRIORITY JOURNAL; RIBOSOME; STEADY STATE; STRESS; YEAST;

CELL CYCLE; CLUSTER ANALYSIS; CULTURE MEDIA; ETHANOL; FOOD; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GLUCOSE; MODELS, BIOLOGICAL; REGRESSION ANALYSIS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

EID: 38749112941     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-08-0779     Document Type: Article

References (63)

1. Airoldi, E. M., Huttenhower, C., Gresham, D., Botstein, D., and Troyanskaya, O. G. (2007). Growth-specific programs of gene expression. Proceedings of the Problems and Methods in Computational Biology Workshop. NIPS 2007.
2. Alexander, M., and Jeffries, T. (1990). Respiratory efficiency and metabolite partitioning as regulatory phenomena in yeasts. Enzyme Microb. Technol. 12, 2-19.
3. Alter, O., Brown, P. O., and Botstein, D. (2000). Singular value decomposition for genome-wide expression data processing and modeling. Proc. Natl. Acad. Sci. USA 97, 10101-10106.
4. Ashburner, M. et al. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.
5. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289-300.
6. Bloom, J., and Cross, F. R. (2007). Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. 8, 149-160.
7. Boer, V. M., de Winde, J. H., Pronk, J. T., and Piper, M. D. (2003). The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. J. Biol. Chem. 278, 3265-3274.
8. 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.
9. Brauer, M. J., Saldanha, A. J., Dolinski, K., and Botstein, D. (2005). Homeostatic adjustment and metabolic remodeling in glucose-limited yeast cultures. Mol. Biol. Cell 16, 2503-2517.
10. Castrillo, J. I. et al. (2007). Growth control of the eukaryote cell: a systems biology study in yeast. J. Biol. 6, 4.
11. Chen, Z., Odstrcil, E. A., Tu, B. P., and McKnight, S. L. (2007). Restriction of DNA replication to the reductive phase of the metabolic cycle protects genome integrity. Science 316, 1916-1919.
12. Cho, R. J. et al. (1998). A genome-wide transcriptional analysis of the mitotic cell cycle. Mol. Cell 2, 65-73.
13. De Virgilio, C., and Loewith, R. (2006a). Cell growth control: little eukaryotes make big contributions. Oncogene 25, 6392-6415.
14. De Virgilio, C., and Loewith, R. (2006b). The TOR signalling network from yeast to man. Int. J. Biochem. Cell Biol. 38, 1476-1481.
15. DeRisi, J. L., Iyer, V. R., and Brown, P. O. (1997). Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278, 680-686.
16. Efron, B. (1993). An Introduction to the Bootstrap, New York: Chapman & Hall.
17. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95, 14863-14868.
18. Elliott, B., and Futcher, B. (1993). Stress resistance of yeast cells is largely independent of cell cycle phase. Yeast 9, 33-42.
19. Futcher, B. (2002). Transcriptional regulatory networks and the yeast cell cycle. Curr. Opin. Cell Biol. 14, 676-683.
20. Futcher, B. (2006). Metabolic cycle, cell cycle, and the finishing kick to Start. Genome Biol. 7, 107.
21. Gasch, A. P., Huang, M., Metzner, S., Botstein, D., Elledge, S. J., and Brown, P. O. (2001). Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell 12, 2987-3003.
22. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., and Brown, P. O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257.
23. Grigull, J., Mnaimneh, S., Pootoolal, J., Robinson, M. D., and Hughes, T. R. (2004). Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24, 5534-5547.
24. Guo, J., Bryan, B. A., and Polymenis, M. (2004). Nutrient-specific effects in the coordination of cell growth with cell division in continuous cultures of Saccharomyces cerevisiae. Arch. Microbiol. 182, 326-330.
25. Hartwell, L. H. (1974). Saccharomyces cerevisiae cell cycle. Bacteriol. Rev. 38, 164-198.
26. Hartwell, L. H., Culotti, J., Pringle, J. R., and Reid, B. J. (1974). Genetic control of the cell division cycle in yeast. Science 183, 46-51.
27. Hoskisson, P. A., and Hobbs, G. (2005). Continuous culture-making a comeback? Microbiology 151, 3153-3159.
28. Jorgensen, P., Rupes, I., Sharom, J. R., Schneper, L., Broach, J. R., and Tyers, M. (2004). A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev. 18, 2491-2505.
29. Jorgensen, P., and Tyers, M. (2004). How cells coordinate growth and division. Curr. Biol. 14, R1014-R1027.
30. Kasper von Meyenburg, H. (1969). Energetics of the Budding Cycle of Saccharomyces cerevisiae. Arch. Mikrobiol. 66, 289-303.
31. Kim, J., and Klionsky, D. J. (2000). Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu. Rev. Biochem. 69, 303-342.
32. Kim, J. W., and Dang, C. V. (2006). Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 66, 8927-8930.
33. Klevecz, R. R., Bolen, J., Forrest, G., and Murray, D. B. (2004). A genomewide oscillation in transcription gates DNA replication and cell cycle. Proc. Natl. Acad. Sci. USA101, 1200-1205.
34. Kubitschek, H. E. (1970). Introduction to Research with Continuous Cultures, Englewood Cliffs, NJ: Prentice Hall.
35. Kudlicki, A., Rowicka, M., and Otwinowski, Z. (2007). SCEPTRANS: an online tool for analyzing periodic transcription in yeast. Bioinformatics 23, 1559-1561.
36. Kuenzi, M. T., and Fiechter, A. (1969). Changes in carbohydrate composition and trehalase-activity during the budding cycle of Saccharomyces cerevisiae. Arch. Mikrobiol. 64, 396-407.
37. Laabs, T. L., Markwardt, D. D., Slattery, M. G., Newcomb, L. L., Stillman, D. J., and Heideman, W. (2003). ACE2 is required for daughter cell-specific G1 delay in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 100, 10275-10280.
38. Maaloe, O., and Kjeldgaard, N. O. (1966). Control of macromolecular synthesis, New York: W. A. Benjamin, Inc.
39. Monastyrska, I., and Klionsky, D. J. (2006). Autophagy in organelle homeostasis: peroxisome turnover. Mol. Aspects Med. 27, 483-494.
40. Monod, J. (1950). La technique de culture continue, theorie et applications. Ann. Inst. Pasteur 79, 390-410.
41. Nomura, M. (1999). Regulation of ribosome biosynthesis in Escherichia coli and Saccharomyces cerevisiae: diversity and common principles. J. Bacteriol. 181, 6857-6864.
42. Novick, A., and Szilard, L. (1950). Description of the chemostat. Science 112, 715-716.
43. Postma, E., Verduyn, C., Sceffers, W. A., and Van Dijken, J. P. (1989). Enzymic Analysis of the Crabtree Effect in Glucose-Limited Chemostat Cultures of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 55, 468-477.
44. Pramila, T., Wu, W., Miles, S., Noble, W. S., and Breeden, L. L. (2006). The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev. 20, 2266-2278.
45. Pringle, J. R., and Hartwell, L. H. (1981). The Saccharomyces cerevisiae cell cycle. In: The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance, ed. J. N. Strathern, E. W. Jones, and J. R. Broach, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
46. R Development Core Team (2007). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.r-project.org.
47. Regenberg, B., Grotkjaer, T., Winther, O., Fausboll, A., Akesson, M., Bro, C., Hansen, L. K., Brunak, S., and Nielsen, J. (2006). Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae. Genome Biol. 7, R107.
48. Rivin, C. J., and Fangman, W. L. (1980). Cell cycle phase expansion in nitrogen-limited cultures of Saccharomyces cerevisiae. J. Cell Biol. 85, 96-107.
49. Rottensteiner, H., and Theodoulou, F. L. (2006). The ins and outs of peroxisomes: co-ordination of membrane transport and peroxisomal metabolism. Biochim. Biophys. Acta 1763, 1527-1540.
50. Saldanha, A. J., Brauer, M. J., and Botstein, D. (2004). Nutritional homeostasis in batch and steady-state culture of yeast. Mol. Biol. Cell 15, 4089-4104.
51. Schneider, B. L., Zhang, J., Markwardt, J., Tokiwa, G., Volpe, T., Honey, S., and Futcher, B. (2004). Growth rate and cell size modulate the synthesis of, and requirement for, G1-phase cyclins at start. Mol. Cell. Biol. 24, 10802-10813.
52. Slattery, M. G., and Heideman, W. (2007). Coordinated regulation of growth genes in Saccharomyces cerevisiae. Cell Cycle 6, 1210-1219.
53. Spellman, P. T., Sherlock, G., Zhang, M. Q., Iyer, V. R., Anders, K., Eisen, M. B., Brown, P. O., Botstein, D., and Futcher, B. (1998). Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9, 3273-3297.
54. Troyanskaya, O., Cantor, M., Sherlock, G., Brown, P., Hastie, T., Tibshirani, R., Botstein, D., and Altman, R. B. (2001). Missing value estimation methods for DNA microarrays. Bioinformatics 17, 520-525.
55. Tu, B. P., Kudlicki, A., Rowicka, M., and McKnight, S. L. (2005). Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310, 1152-1158.
56. Unger, M. W., and Hartwell, L. H. (1976). Control of cell division in Saccharomyces cerevisiae by methionyl-tRNA. Proc. Natl. Acad. Sci. USA 73, 1664-1668.
57. van Dijken, J. P. et al. (2000). An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains. Enzyme Microb. Technol. 26, 706-714.
58. van Roermund, C. W., Waterham, H. R., Ijlst, L., and Wanders, R. J. (2003). Fatty acid metabolism in Saccharomyces cerevisiae. Cell Mol. Life Sci. 60, 1838-1851.
59. Verges, E., Colomina, N., Gari, E., Gallego, C., and Aldea, M. (2007). Cyclin Cln3 is retained at the ER and released by the J chaperone Ydj1 in late G1 to trigger cell cycle entry. Mol. Cell 26, 649-662.
60. Wanders, R. J., and Waterham, H. R. (2006). Peroxisomal disorders: the single peroxisomal enzyme deficiencies. Biochim. Biophys. Acta 1763, 1707-1720.
61. Warburg, O. (1956). On respiratory impairment in cancer cells. Science 124, 269-270.
62. Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440.
63. Zhao, Y., Sohn, J. H., and Warner, J. R. (2003). Autoregulation in the biosynthesis of ribosomes. Mol. Cell. Biol. 23, 699-707.