Cyclic AMP mediates the cell cycle dynamics of energy metabolism in Saccharomyces cerevisiae

Yeast

Volumn 20, Issue 4, 2003, Pages 351-367

  Müller, Dirk ^a   Exler, Simone ^a   Aguilera Vázquez, Luciano ^a   Guerrero Martín, Ester ^a   Reuss, Matthias ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

cAMP; Cell cycle; Energy metabolism; Oscillations; Synchronous cultures

Indexed keywords

CYCLIC AMP; GLUCOSE; GLYCOGEN; TREHALOSE;

ARTICLE; CELL CULTURE; CELL CYCLE; CELL GROWTH; CELL KINETICS; CELL LEVEL; CONTROLLED STUDY; ENERGY METABOLISM; MEASUREMENT; MODULATION; NONHUMAN; NUTRIENT SUPPLY; OSCILLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; YEAST CELL;

BIOREACTORS; CELL COUNT; CELL CYCLE; CELL DIVISION; CYCLIC AMP; ENERGY METABOLISM; GLYCOGEN; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TREHALOSE;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037338995     PISSN: 0749503X     EISSN: None     Source Type: Journal    
DOI: 10.1002/yea.967     Document Type: Article

References (90)

1. Alberghina L, Ranzi BM, Porro D, Martegani E. 1991. Flow cytometry and cell cycle kinetics in continuous and fed-batch fermentations of budding yeast. Biotechnol Prog 7: 299-304.
2. Alberghina L, Smeraldi C, Ranzi BM, Porro D. 1998. Control by nutrients of growth and cell cycle progression in budding yeast, analyzed by double-tag flow cytometry. J Bacteriol 180(15): 3864-3872.
3. Anghileri P, Branduardi P, Sternieri F, et al. 1999. Chromosome separation and exit from mitosis in budding yeast: dependence on growth revealed by cAMP-mediated inhibition. Exp Cell Res 250: 510-523.
4. Aon MA, Cortassa S, Westerhoff HV, et al. 1991. Dynamic regulation of yeast glycolytic oscillations by mitochondrial functions. J Cell Sci 99: 325-334.
5. App H, Holzer H. 1989. Purification and characterization of neutral trehalase from the yeast ABYS1 mutant. J Biol Chem 264(29): 17583-17588.
6. Ashe MP, De Long SK, Sachs AB. 2000. Glucose depletion rapidly inhibits translation initiation in yeast. Mol Biol Cell 11: 833-848.
7. Baldwin WW, Kubitschek HE. 1984. Buoyant density variation during the cell cycle of Saccharomyces cerevisiae. J Bacteriol 158(2): 701-704.
8. 1 cyclin expression by cyclic AMP in budding yeast. Nature 371: 339-342.
9. Becker JU. 1978. A method for glycogen determination in whole yeast cells. Anal Biochem 86(1): 56-64.
10. Boles E, Zimmermann FK, Thevelein JM. 1997. Metabolic signals. In Yeast Sugar Metabolism, Zimmermann FK, Entian KD (eds), Technomic: Basel; 379-407.
11. Cho RJ, Campbell MJ, Winzeler EA, et al. 1998. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2: 65-73.
12. Colombo S, Ma P, Cauwenberg L, et al. 1998. Involvement of distinct G-proteins, Gpa2 and Ras in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J 17(12): 3326-3341.
13. de Koning W, Groeneveld K, Oehlen LJWM, Berden JA, van Dam K. 1991. Changes in the activities of key enzymes of glycolysis during the cell cycle in yeast: a rectification. J Gen Microbiol 137: 971-976.
14. Dombek KM, Young ET. 1997. Cyclic AMP-dependent protein kinase inhibits ADH2 expression in part by decreasing expression of the transcription factor gene ADR1. Mol Cell Biol 17(3): 1450-1458.
15. Duboc P, Marison I, von Stockar U. 1996. Physiology of Saccharomyces cerevisiae during cell cycle oscillations. J Biotechnol 51: 57-72.
16. Estruch F. 2000. Stress-controlled transcription factors, stress-induced genes, and stress tolerance in budding yeast. FEMS Microbiol Rev 24(4): 469-486.
17. Francois J, Eraso P, Gancedo C. 1987. Changes in the concentration of cAMP, fructose-2,6-bisphosphate and related metabolites and enzymes in Saccharomyces cerevisiae during growth on glucose. Eur J Biochem 164(2): 369-373.
18. Francois J, Parrou JL. 2001. Reserve carbohydrate metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25: 125-145.
19. Frandsen S, Nielsen J, Villadsen J. 1994. Dynamics of Saccharomyces cerevisiae in continuous culture. In ECB6: Proceedings of the 6th European Congress on Biotechnology, Alberghina L, Frontali L, Sensi P (eds). Elsevier Science: Amsterdam; 887-890.
20. Futcher B. 1996. Cyclins and the wiring of the yeast cell cycle. Yeast 12(16): 1635-1646.
21. Futcher B. 1999. Cell cycle synchronization. Methods Cell Sci 21: 79-86.
22. Geymonat M, Wang L, Garreau H, Jacquet M. 1998. Ssa1p chaperone interacts with the guanine nucleotide exchange factor of Ras Cdc25p and controls the cAMP pathway in Saccharomyces cerevisiae. Mol Microbial 30(4): 855-864.
23. Gonzalez B, Francois J, Renaud M. 1997. A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol. Yeast 14: 1347-1355.
24. Grauslund M, Lopes JM, Rønnow B. 1999. Expression of GUT1, which encodes glycerol kinase in Saccharomyces cerevisiae, is controlled by the positive regulators Adr1p, Ino2p and Ino4p and the negative regulator Opi1p in a carbon source-dependent fashion. Nucleic Acids Res 27(22): 4391-4398.
25. Hall DD, Markwardt DD, Parviz F, Heideman W. 1998. Regulation of the Cln3-Cdc28 kinase by cAMP in Saccharomyces cerevisiae. EMBO J 17(15): 4370-4378.
26. Haney SA, Broach SR. 1994. Cdc25p, the guanine nucleotide exchange factor for the Ras proteins of Saccharomyces cerevisiae, promotes exchange by stabilizing Ras in a nucleotide-free state. J Biol Chem 269(24): 16541-16548.
27. Harashima T, Heitman J. 2002. The Gα protein Gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gβ subunits. Mol Cell 10: 163-173.
28. Hartwell LH. 1970. Periodic density fluctuation during the yeast cell cycle and the selection of synchronous cultures. J Bacteriol 104(3): 1280-1285.
29. Hirimburegama K, Durnez P, Keleman J, et al. 1992. Nutrient-induced activation of trehalase in nutrient-starved cells of the yeast Saccharomyces cerevisiae: cAMP is not involved as second messenger. J Gen Microbiol 138: 2035-2043.
30. Hjortsø MA, Nielsen J. 1995. Population balance models of autonomous microbial oscillations. J Biotechnol 42(3): 255-269.
31. Hofmann E, Bedri A, Kessler R, Kretschmer M, Schellenberger W. 1989. 6-phosphofructo-2-kinase and fructose-2,6-bisphosphatase from Saccharomyces cerevisiae. Adv Enzyme Regul 28: 283-306.
32. Irniger S, Bäumer M, Braus GH. 2000. Glucose and Ras activity influence the ubiquitin ligases APC/C and SCF in Saccharomyces cerevisiae. Genetics 154: 1509-1521.
33. Kaplon T, Jacquet M. 1995. The cellular content of Cdc25p, the Ras exchange factor in Saccharomyces cerevisiae, is regulated by destabilization through a cyclin destruction box. J Biol Chem 270(35): 20742-20747.
34. Kessler R, Schellenberger W, Nissler K, Hofmann E. 1988. Binding of fructose-2,6-bisphosphate to yeast phosphofructokinase. Biomed Biochim Acta 47: 221-225.
35. Kotani S, Tugendreich S, Fujii M, et al. 1998. PKA and MPF-activated polo-like kinase regulate anaphase-promoting complex activity and mitosis progression. Mol Cell 1: 371-380.
36. Kotani S, Tanaka H, Yasuda H, Todokoro K. 1999. Regulation of APC activity by phosphorylation and regulatory factors. J Cell Biol 146(4): 791-800.
37. Kraakman L, Lemaire K, Ma P, et al. 1999a. A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose. Mol Microbiol 32(5): 1002-1012.
38. Kraakman L, Winderickx J, Thevelein JM, de Winde JH. 1999b. Structure-function analysis of yeast hexokinase: structural requirements for triggering cAMP signalling and catabolite repression. Biochem J 343: 159-168.
39. Küenzi MT, Fiechter A. 1969. Changes in carbohydrate composition and trehalase activity during the budding cycle of Saccharomyces cerevisiae. Arch Mikrobiol 64: 396-407.
40. Kunst A, Draeger B, Ziegenhorn J. 1984. UV methods with hexokinase and glucose-6-phosphate dehydrogenase. In Methods of Enzymatic Analysis, vol VI, Metabolites 1: Carbohydrates, 3rd edn, Bergmeyer HU (ed.). VCH: Weinheim; 163-172.
41. Liao H, Thorner J. 1980. Yeast mating pheromone α-factor inhibits adenylate cyclase. Proc Natl Acad Sci USA 77: 1898-1902.
42. Lorenz MC, Pan X, Harashima T, et al. 2000. The G protein-coupled receptor Gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154: 609-622.
43. Ma P, Wera S, van Dijck P, Thevelein JM. 1999. The PDE1-encoded low affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function controlling agonist-induced cAMP signalling. Mol Biol Cell 10: 91-104.
44. Martegani E, Porro D, Ranzi BM, Alberghina L. 1990. Involvement of a cell size control mechanism in the induction and maintenance of oscillations in continuous cultures of budding yeast. Biotechnol Bioeng 36: 453-459.
45. Martínez-Pastor MT, Marchler G, Schüller C. 1996. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 15(9): 2227-2235.
46. Mösch HU, Roberts RL, Fink GR. 1996. Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93: 5352-5356.
47. Mösch HU, Fink GR. 1997. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 145: 671-684.
48. Münch T, Sonnleitner B, Fiechter A. 1992. The decisive role of the Saccharomyces cerevisiae cell cycle behaviour for dynamic growth characterization. J Biotechnol 22: 329-352.
49. Nielsen J, Villadsen J. 1994. Bioreaction Engineering Principles. Plenum Press: New York; 243-249.
50. Pan X, Heitman J. 1999. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 19(7): 4874-4887.
51. Pan X, Heitman J. 2002. Protein kinase A operates a molecular switch that governs yeast pseudohyphal differentiation. Mol Cell Biol 22(12): 3981-3993.
52. Pohlig G, Holzer H. 1985. Phosphorylation and inactivation of yeast fructose-1,6-bisphosphatase by cyclic AMP-dependent protein kinase from yeast. J Biol Chem 260(25): 13818-13823.
53. 1 cyclin CLN3 in yeast. Genes Dev 11: 2522-2531.
54. Porro D, Martegani E, Ranzi BM, Alberghina L. 1988. Oscillations in continuous cultures of budding yeast: a segregated parameter analysis. Biotechnol Bioeng 32: 411-417.
55. Pringle JR, Adams AEM, Drubin DG, Haarer BK. 1991. Immunofluorescence methods for yeast. In Guide to Yeast Genetics and Molecular Biology, Guthrie C, Fink G (eds). Methods in Enzymology, Academic Press: New York, 194; 565-602.
56. Quain DE. 1981. The determination of glycogen in yeasts. J Inst Brew 87: 289-291.
57. Reich JG, Sel'kov EE. 1981. Energy Metabolism of the Cell. Academic Press: London.
58. Reinders A, Bürckert N, Boller T, Wiemken A, De Virgilio C. 1998. Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. Genes Dev 12: 2943-2955.
59. Rolland F, de Winde JH, Lemaire K, et al. 2000. Glucose-induced cAMP signalling in yeast requires both a G-protein coupled receptor system for extracellular glucose detection and a separable hexokinase-dependent sensing process. Mol Microbiol 38(2): 348-358.
60. Rolland F, Wanke V, Cauwenberg L, et al. 2001. The role of hexose transport and phosphorylation in cAMP signalling in the yeast Saccharomyces cerevisiae. FEMS Yeast Res 1(1): 33-45.
61. Rolland F, Winderickx J, Thevelein JM. 2002. Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2(2): 183-201.
62. Rudoni S, Colombo S, Cocceti P, Martegani E. 2001. Role of guanine nucleotides in the regulation of the Ras/cAMP pathway in Saccharomyces cerevisiae. Biochim Biophys Acta 1538: 181-189.
63. Schulze U, Larsen ME, Villadsen J. 1995. Determination of intracellular trehalose and glycogen in Saccharomyces cerevisiae. Anal Biochem 228: 143-149.
64. 1 phase duration, cyclin expression and reserve carbohydrate metabolism in Saccharomyces cerevisiae. J Bacteriol 179(21): 6560-6565.
65. Simon MM, Pavlik P, Hartig A, et al. 1995. A C-terminal region of the Saccharomyces cerevisiae transcription factor ADR1 plays an important role in the regulation of peroxisome proliferation by fatty acids. Mol Gen Genet 249(3): 289-296.
66. Smith ME, Dickinson R, Wheals AE. 1990. Intracellular and extracellular levels of cyclic AMP during the cell cycle of Saccharomyces cerevisiae. Yeast 6: 53-60.
67. Sonnleitner B, Käppeli O. 1986. Growth of Saccharomyces cerevisiae is controlled by its limited respiratory capacity: formulation and verification of a hypothesis. Biotechnol Bioeng 28: 927-937.
68. Spellman PT, Sherlock G, Zhang MQ, et al. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9: 3273-3297.
69. Spevak W, Keiper BD, Stratowa C, Castanón MJ. 1993. Saccharomyces cerevisiae cdc15 mutants arrested at a late stage in anaphase are rescued by Xenopus cDNAs encoding N-ras or a protein with β-transducin repeats. Mol Cell Biol 13(8): 4953-4966.
70. Strässle C, Sonnleitner B, Fiechter A. 1988. A predictive model for the spontaneous synchronization of Saccharomyces cerevisiae grown in continuous culture. I. Concept. J Biotechnol 7: 299-318.
71. Strässle C, Sonnleitner B, Fiechter A. 1989. A predictive model for the spontaneous synchronization of Saccharomyces cerevisiae grown in continuous culture. II. Experimental verification. J Biotechnol 9: 191-208.
72. Taylor WE, Young ET. 1990. cAMP-dependent phosphorylation and inactivation of yeast transcription factor ADR1 does not affect DNA binding. Proc Natl Acad Sci USA 87: 4098-4102.
73. Theobald U, Mailinger W, Reuss M, Rizzi M. 1993. In vivo analysis of glucose-induced fast changes in yeast adenine nucleotide pool applying a rapid sampling technique. Anal Biochem 214: 31-37.
74. Theobald U, Mailinger W, Baltes M, Rizzi M, Reuss M. 1997. In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae: I. Experimental observations. Biotech Bioeng 55(2): 305-316.
75. Thevelein JM. 1988. Regulation of trehalase activity by phosphorylation-dephosphorylation during developmental transitions in fungi. Exp Mycol 12: 1-12.
76. Thevelein JM. 1991. Fermentable sugars and intracellular acidification as specific activators of the RAS-adenylate cyclase pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol 5(6): 1301-1307.
77. Thevelein JM, de Winde JH. 1999. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33(5): 904-918.
78. Thevelein JM, Cauwenberg L, Colombo S, et al. 2000. Nutrient-induced signal transduction through the protein kinase A pathway and its role in the control of metabolism, stress resistance, and growth in yeast. Enzyme Microb Technol 26: 819-825.
79. 1 cyclin activity by the Ras-cAMP pathway in yeast. Nature 371: 343-345.
80. van der Plaat JB. 1974. Cyclic 3′,5′-adenosine monophosphate stimulates trehalose degradation in baker's yeast. Biochem Biophys Res Commun 56(3): 580-587.
81. van Doorn J, Scholte ME, Postma PW, van Driel R, van Dam K. 1988a. Regulation of trehalase activity during the cell cycle of Saccharomyces cerevisiae. J Gen Microbiol 134: 785-790.
82. van Doorn J, Valkenburg JAC, Scholte ME, et al. 1988b. Changes in activities of several enzymes involved in carbohydrate metabolism during the cell cycle of Saccharomyces cerevisiae. J Bacteriol 170: 4808-4815.
83. Vanoni M, Vai M, Popolo L, Alberghina L. 1983. Structural heterogeneity in populations of the budding yeast Saccharomyces cerevisiae. J Bacteriol 156(3): 1282-1291.
84. Vaseghi S. 2000. Modellgestützte Analyse der Dynamik des Phosphofructokinase-Systems in Saccharomyces cerevisiae. PhD Thesis, Universität Stuttgart, Stuttgart, Germany.
85. Vaseghi S, Macherhammer F, Zibek S, Reuss M. 2001. Signal transduction dynamics of the protein kinase A-phosphofructokinase-2 system in Saccharomyces cerevisiae. Metab Eng 3: 163-172.
86. Versele M, de Winde JH, Thevelein JM. 1999. A novel regulator of G protein signalling in yeast, Rgs2, downregulates glucose activation of the cAMP pathway through direct inhibition of Gpa2. EMBO J 18(20): 5577-5591.
87. Vidan S, Mitchell AP. 1997. Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p. Mol Cell Biol 17(5): 2688-2697.
88. von Meyenburg HK. 1969. Energetics of the budding cycle of Saccharomyces cerevisiae during glucose limited aerobic growth, Arch Mikrobiol 66: 289-303.
89. Watson CD, Berry DR. 1977. Fluctuations in cAMP levels during the cell cycle of Saccharomyces cerevisiae. FEMS Microbiol Lett 1: 175-177.
90. Woldringh CL, Huls PG, Vischer NOE. 1993. Volume growth of daughter and parent cells during the cell cycle of Saccharomyces cerevisiae a/α as determined by image cytometry. J Bacteriol 175(10): 3174-3181.