Exploring the genetic control of glycolytic oscillations in Saccharomyces Cerevisiae

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  Williamson, Thomas ^a   Adiamah, Delali ^a   Schwartz, Jean Marc ^a   Stateva, Lubomira ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

cAMP PKA signal transduction pathway; deletion mutants; Glycolytic oscillations; Saccharomyces cerevisiae

Indexed keywords

SACCHAROMYCES CEREVISIAE;

6 PHOSPHOFRUCTOKINASE; CYCLIC AMP; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOKINASE; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; BIOLOGICAL MODEL; CYTOLOGY; ENZYMOLOGY; GENE DELETION; GENETICS; GLYCOLYSIS; METABOLISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

CYCLIC AMP; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GLYCOLYSIS; HEXOKINASE; ISOENZYMES; MODELS, GENETIC; NAD; PHOSPHOFRUCTOKINASES; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

EID: 84865300881     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-108     Document Type: Article

References (63)

1. Richard P, Teusink B, Hemker MB, Van Dam K, Westerhoff HV. Sustained oscillations in free-energy state and hexose phosphates in yeast. Yeast 1996, 12:731-740. 10.1002/(SICI)1097-0061(19960630)12:8<731::AID-YEA961>3.0.CO;2-Z, 8813760.
2. Andersen AZ, Poulsen AK, Brasen JC, Olsen LF. On-line measurements of oscillating mitochondrial membrane potential in glucose-fermenting Saccharomyces cerevisiae. Yeast 2007, 24:731-739. 10.1002/yea.1508, 17568453.
3. Ghosh A, Chance B. Oscillations of glycolytic intermediates in yeast cells. Biochem Biophys Res Commun 1964, 16:174-181. 10.1016/0006-291X(64)90357-2, 4224521.
4. Chance B, Estabrook RW, Ghosh A. Damped sinusoidal oscillations of cytoplasmic reduced pyridine nucleotide in yeast cells. Proc Natl Acad Sci USA 1964, 51:1244-1251. 10.1073/pnas.51.6.1244, 300244, 14215650.
5. Lushchak OV, Müller SC, Mair T. Comparison of glycolytic NADH oscillations in yeasts Saccharomyces cerevisiae and Saccharomyces carlsbergensis. Ukr Biokhim Zh 2006, 78:22-28.
6. Tornheim K, Lowenstein JM. The purine nucleotide cycle. Control of phosphofructokinase and glycolytic oscillations in muscle extracts. J Biol Chem 1975, 250:6304-6314.
7. Nilsson T, Schultz V, Berggren PO, Corkey BE, Tornheim K. Temporal patterns of changes in ATP/ADP ratio, glucose 6-phosphate and cytoplasmic free Ca2+ in glucose-stimulated pancreatic beta-cells. Biochem J 1996, 314:91-94. 1217056, 8660314.
8. Escalante R, Vicente JJ. Dictyostelium discoideum: a model system for differentiation and patterning. Int J Dev Biol 2000, 44:819-835.
9. Vitaterna MH, Takahashi JS, Turek FW. Overview of circadian rhythms. Alcohol Res Health 2001, 2001(25):85-93.
10. Berridge MJ, Bootman MD, Lipp P. 1998 Calcium-a life and death signal. Nature 1998, 395:645-648. 10.1038/27094, 9790183.
11. Tyson JJ, Novak B. Regulation of the eukaryotic cell cycle: molecular antagonism, hysteresis, and irreversible transitions. J Theor Biol 2001, 210:249-263. 10.1006/jtbi.2001.2293, 11371178.
12. Mair T, Warnke C, Tsuji K, Müller SC. Control of glycolytic oscillations by temperature. Biophys J 2005, 88:639-646. 10.1529/biophysj.104.043398, 1305041, 15489309.
13. De Monte S, D' Ovidio F, Danø S, Sørensen PG. Dynamical quorum sensing: Population density encoded in cellular dynamics. Proc Natl Acad Sci USA 2007, 104:18377-18381. 10.1073/pnas.0706089104, 2141785, 18003917.
14. Olsen LF, Andersen AZ, Lunding A, Brasen JC, Poulsen AK. Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-ATPases. Biophys J 2009, 96:3850-3861. 10.1016/j.bpj.2009.02.026, 2711425, 19413991.
15. Richard P, Bakker BM, Teusink B, Van Dam K, Westerhoff HV. Acetaldehyde mediates the synchronization of sustained glycolytic oscillations in populations of yeast cells. Eur J Biochem 1996, 235:238-241. 10.1111/j.1432-1033.1996.00238.x, 8631335.
16. Bier M, Bakker BM, Westerhoff HV. How yeast cells synchronize their glycolytic oscillations: a perturbation analytic treatment. Biophys J 2000, 78:1087-1093. 10.1016/S0006-3495(00)76667-7, 1300712, 10692299.
17. Poulsen AK, Petersen M, Olsen LF. Single cell studies and simulation of cell-cell interactions using oscillating glycolysis in yeast cells. Biophys Chem 2007, 125:275-280. 10.1016/j.bpc.2006.08.009, 16997454.
18. Wolf J, Passarge J, Somsen OJ, Snoep JL, Heinrich R, Westerhoff HV. Transduction of intracellular and intercellular dynamics in yeast glycolytic oscillations. Biophys J 2000, 78:1145-1153. 10.1016/S0006-3495(00)76672-0, 1300717, 10692304.
19. Goldbeter A, Lefever R. Dissipative structures for an allosteric model. Application to glycolytic oscillations. Biophys J 1972, 12:1302-1315. 10.1016/S0006-3495(72)86164-2, 1484224, 4263005.
20. Teusink B, Passarge J, Reijenga CA, Esgalhado E, van der Weijden CC, Schepper M, et al. Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur J Biochem 2000, 267:5313-5329. 10.1046/j.1432-1327.2000.01527.x, 10951190.
21. Reijenga KA, Snoep JL, Diderich JA, van Verseveld HW, Westerhoff HV, Teusink B. Control of glycolytic dynamics by hexose transport in Saccharomyces cerevisiae. Biophys J 2001, 80:626-634. 10.1016/S0006-3495(01)76043-2, 1301262, 11159431.
22. Reijenga KA, van Megen Y, Kooi BW, Bakker BM, Snoep JL, van Verseveld HW, et al. Yeast glycolytic oscillations that are not controlled by a single oscillophore: a new definition of oscillophore strength. J Theor Biol 2005, 232:385-398. 10.1016/j.jtbi.2004.08.019, 15572063.
23. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998, 14:115-132. 10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2, 9483801.
24. Sherman F, Fink G, Hicks J. Methods in yeast genetics: A laboratory manual 1986, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
25. Poulsen AK, Lauritsen FR, Olsen LF. Sustained glycolytic oscillations-no need for cyanide. FEMS Microbiol Lett 2004, 236:261-266.
26. Poulsen AK, Andersen AZ, Brasen JC, Scharff-Poulsen AM, Olsen LF. Probing glycolytic and membrane potential oscillations in Saccharomyces cerevisiae. Biochemistry 2008, 47:7477-7484. 10.1021/bi800396e, 18558716.
27. Schmidt H, Jirstrand M. Systems Biology Toolbox for MATLAB: a computational platform for research in systems biology. Bioinformatics 2006, 22:514-515. 10.1093/bioinformatics/bti799, 16317076.
28. Stelling J, Gilles ED, Doyle FJ. Robustness properties of circadian clock architectures. Proc Natl Acad Sci USA 2004, 101:13210-13215. 10.1073/pnas.0401463101, 516549, 15340155.
29. Higgins J. A chemical mechanism for oscillation of glycolytic intermediates in yeast cells. Proc Natl Acad Sci USA 1964, 51:989-994. 10.1073/pnas.51.6.989, 300199, 14215656.
30. Madsen MF, Danø S, Sørensen PG. On the mechanisms of glycolytic oscillations in yeast. FEBS J 2005, 272:648-2660.
31. Heinisch J, Boles E, Timple C. A yeast phosphofructokinase insensitive to the allosteric activator fructose 2,6-bisphosphate. J Biol Chem 1996, 171:15928-15933.
32. McAlister L, Holland MJ. Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 1985, 260:15019-15027.
33. McAlister L, Holland MJ. Isolation and characterization of yeast strains carrying mutations in the glyceraldehyde-3-phosphate dehydrogenase genes. J Biol Chem 1985, 260:15013-15018.
34. Delgado ML, O'Connor JE, Azorín I, Renau-Piqueras J, Gil ML, Gozalbo D. The glyceraldehyde-3-phosphate dehydrogenase polypeptides encoded by the Saccharomyces cerevisiae TDH1, TDH2 and TDH3 genes are also cell wall proteins. Microbiol (Reading, Engl.) 2001, 147:411-417.
35. Rodicio R, Heinisch J. Isolation of the yeast phosphoglyceromutase gene and construction of deletion mutants. Mol Gen Genet 1987, 206:133-140. 10.1007/BF00326548, 3033435.
36. Heinisch JJ, Müller S, Schlüter E, Jacoby J, Rodicio R. Investigation of two yeast genes encoding putative isoenzymes of phosphoglycerate mutase. Yeast 1998, 14:203-213. 10.1002/(SICI)1097-0061(199802)14:3<203::AID-YEA205>3.0.CO;2-8, 9544241.
37. Brewer JM, Glover CV, Holland MJ, Lebioda L. Effect of site-directed mutagenesis of His373 of yeast enolase on some of its physical and enzymatic properties. Biochim Biophys Acta 1997, 1340:88-96. 10.1016/S0167-4838(97)00029-0, 9217018.
38. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Véronneau S, et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 2002, 418:387-391. 10.1038/nature00935, 12140549.
39. Hynne F, Danø S, Sørensen PG. Full-scale model of glycolysis in Saccharomyces cerevisiae. Biophys Chem 2001, 94:121-163. 10.1016/S0301-4622(01)00229-0, 11744196.
40. Brusch L, Cuniberti G, Bertau M. Model evaluation for glycolytic oscillations in yeast biotransformations of xenobiotics. Biophys Chem 2004, 109:413-426. 10.1016/j.bpc.2003.12.004, 15110938.
41. Jones DL, Petty J, Hoyle DC, Hayes A, Ragni E, Popolo L, Oliver SG, Stateva L. Transcriptome profiling of a Saccharomyces cerevisiae mutant with a constitutively activated Ras/cAMP pathway. Physiol Genomics 2003, 16:107-118. 10.1152/physiolgenomics.00139.2003, 14570984.
42. Sass P, Field J, Nikawa J, Toda T, Wigler M. Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1986, 83:9303-9307. 10.1073/pnas.83.24.9303, 387126, 3025832.
43. Williamson T. Systems studies of the cAMP pathway and glycolytic oscillations in yeast 2009, UK: University of Manchester, Faculty of Life Sciences, PhD Thesis.
44. Nikawa J, Sass P, Wigler M. Cloning and characterization of the low-affinity cyclic AMP phosphodiesterase gene of Saccharomyces cerevisiae. Mol Cell Biol 1987, 7:3629-3636. 368017, 2824992.
45. Xue Y, Batlle M, Hirsch JP. GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p Galpha subunit and functions in a Ras-independent pathway. EMBO J 1998, 17:1996-2007. 10.1093/emboj/17.7.1996, 1170545, 9524122.
46. Nakafuku M, Obara T, Kaibuchi K, Miyajima I, Miyajima A, Itoh H, et al. Isolation of a second yeast Saccharomyces cerevisiae gene (GPA2) coding for guanine nucleotide-binding regulatory protein: studies on its structure and possible functions. Proc Natl Acad Sci USA 1988, 85:1374-1378. 10.1073/pnas.85.5.1374, 279773, 2830616.
47. Toda T, Cameron S, Sass P, Zoller M, Wigler M. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell 1987, 50:277-287. 10.1016/0092-8674(87)90223-6, 3036373.
48. Tanaka K, Nakafuku M, Tamanoi F, Kaziro Y, Matsumoto K, Toh-e A. IRA2, a second gene of Saccharomyces cerevisiae that encodes a protein with a domain homologous to mammalian ras GTPase-activating protein. Mol Cell Biol 1990, 10:4303-4313. 360976, 2164637.
49. Nikawa J, Cameron S, Toda T, Ferguson KM, Wigler M. Rigorous feedback control of cAMP levels in Saccharomyces cerevisiae. Gen Dev 1987, 1:931-937.
50. Arvanitidis A, Heinisch JJ. Studies on the function of yeast phosphofructokinase subunits by in vitro mutagenesis. J Biol Chem 1994, 269:8911-8918.
51. Rodicio R, Strauß A, Heinisch JJ. Single point mutations in either gene encoding the subunits of the heterooctameric yeast phopshofructokinase abolish allosteric inhibition by ATP. J Biol Chem 2000, 29:40952-40960.
52. Tijane MN, Chaffotte AF, Seydoux FJ, Roucous C, Laurent M. Sulfhydryl groups of yeast phosphofructokinase-specific localization on beta subunits of fructose 6-phosphate binding sites as demonstrated by a differential chemical labeling study. J Biol Chem 1980, 255:10188-10193.
53. Danø S, Sørensen PG, Hynne F. Sustained oscillations in living cells. Nature 1999, 402:320-322. 10.1038/46329, 10580506.
54. De Winde JH, Crauwels M, Hohmann S, Thevelein JM, Winderickx J. Differential requirement of the yeast sugar kinases for sugar sensing in establishing the catabolite-repressed state. Eur J Biochem 1996, 241:633-643. 10.1111/j.1432-1033.1996.00633.x, 8917466.
55. De Risi JL, Iyer VR, Brown PO. Exploring the metabolic and genetic control of gene expression on a genomic scale. Sci 1997, 278:680-686.
56. Reijenga K, Westerhoff HV, Kholodenko BN, Snoep JL. Control analysis for autonomously oscillating biochemical networks. Biophys J 2002, 82:99-108. 10.1016/S0006-3495(02)75377-0, 1302452, 11751299.
57. Tseng YY, Hunt SM, Heintzen C, Crosthwaite SK, Schwartz JM. Comprehensive modelling of the Neurospora circadian clock and its temperature compensation. PLoS Comput Biol 2012, 8:e1002437. 10.1371/journal.pcbi.1002437, 3320131, 22496627.
58. Ihekwaba AE, Broomhead DS, Grimley RL, Benson N, Kell DB. Sensitivity analysis of parameters controlling oscillatory signalling in the NF-κB pathway: the roles of IKK and IκBα. Syst Biol 2004, 1:93-103.
59. Kim TH, Shin SY, Choo SM, Cho KH. Dynamical analysis of the calcium signaling pathway in cardiac myocytes based on logarithmic sensitivity analysis. Biotechnol J 2008, 3:639-647. 10.1002/biot.200700247, 18246569.
60. Nielsen K, Sørensen PG, Hynne F, Busse HG. Sustained oscillations in glycolysis: an experimental and theoretical study of chaotic and complex periodic behaviour and of quenching of simple oscillations. Biophys Chem 1998, 72:49-62. 10.1016/S0301-4622(98)00122-7, 17029704.
61. Richard P. The rhythm of yeast. FEMS Microbiol Rev 2003, 27:547-557. 10.1016/S0168-6445(03)00065-2, 14550945.
62. Kloster A, Olsen LF. Oscillations in glycolysis in Saccharomyces cerevisiae: The role of autocatalysis and intracellular ATPase activity. Biophys Chem 2012, 165-166:39-77.
63. Ytting CK, Fugslang AT, Hiltunen JK, Kastaniotis AJ, Özalp VC, Nielsen LJ, Olsen LF. Measurements of intracellular ATP provide new insight into the regulation of glycolysis in the yeast Saccharomyces cerevisiae. Integr Biol 2012, 4:99-107.