Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-ATPases

Biophysical Journal

Volumn 96, Issue 9, 2009, Pages 3850-3861

  Olsen, Lars Folke ^a   Andersen, Ann Zahle ^a   Lunding, Anita ^a   Brasen, Jens Christian ^a   Poulsen, Allan K ^a,b  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b DANISH TECHNOLOGICAL INSTITUTE   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

3,3' DIETHYLOXACARBOCYANINE IODIDE; ADENINE NUCLEOTIDE TRANSLOCASE; ALCOHOL; ANTIPORTER; FLUORESCENT DYE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; DITHIAZANINE; ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE; OMEPRAZOLE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SACCHAROMYCES CEREVISIAE PROTEIN; UNCOUPLING PROTEIN;

ANAEROBIC METABOLISM; ARTICLE; AUTOFLUORESCENCE; CELL MEMBRANE; CELL PH; CONTROLLED STUDY; ELECTRON TRANSPORT; GLYCOLYSIS; HYDROLYSIS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OSCILLATION; SACCHAROMYCES CEREVISIAE; CELL MEMBRANE POTENTIAL; DRUG ANTAGONISM; FLUORESCENCE; METABOLISM; MITOCHONDRIAL MEMBRANE; OXYGEN CONSUMPTION; PERIODICITY; PH; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; CARBON DIOXIDE; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL MEMBRANE; DITHIAZANINE; ENZYME INHIBITORS; ETHANOL; FLUORESCENCE; GLYCOLYSIS; HYDROGEN-ION CONCENTRATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE POTENTIALS; MITOCHONDRIAL MEMBRANES; NAD; OMEPRAZOLE; OXYGEN CONSUMPTION; PERIODICITY; PROTON-TRANSLOCATING ATPASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UNCOUPLING AGENTS;

EID: 67650363728     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.026     Document Type: Article

References (56)

1. Goldbeter, A. 1996. Biochemical Oscillations and Cellular Rhythms: The Molecular Basis of Periodic and Chaotic Behaviour. Cambridge University Press, Cambridge, UK.
2. Aon, M. A., S. Cortassa, E. Marbán, and B. O'Rourke. 2003. Synchronized whole cell oscillations in mitochondrial metabolism triggered by a local release of reactive oxygen species in cardiac myocytes. J. Biol. Chem. 278:44735-44744.
3. Chou, H. F., N. Berman, and E. Ipp. 1992. Oscillations of lactate released from islets of Langerhans - evidence for oscillatory glycolysis in b-cells. Am. J. Physiol. 262:E800-E805.
4. Lloyd, D. D. B. M. 2006. The temporal architecture of eukaryotic growth. FEBS Lett. 580:2830-2835.
5. Weiss, J. N., L. Yang, and Z. Qu. 2006. Systems biology approaches to metabolic and cardiovascular disorders: network perspectives of cardiovascular metabolism. J. Lipid Res. 47:2355-2366.
6. Richard, P. 2003. The rhythm of yeast. FEMS Microbiol. Rev. 27: 547-557.
7. Wymann, M. P., P. Kernen, D. A. Deranleau, and M. Baggiolini. 1989. Respiratory burst oscillations in human neutrophils and their correlation with fluctuations in apparent cell shape. J. Biol. Chem. 264:15829-15834.
8. Fossati, G., D. A. Moulding, D. G. Spiller, R. J. Moots, M. R. H. White, et al. 2003. The mitochondrial network of human neutrophils: role in chemotaxis, phagocytosis, respiratory burst activation, and commitment to apoptosis. J. Immunol. 170:1964-1972.
9. Maianski, N. A., J. Geissler, S. M. Srinivasula, E. S. Alnemri, D. Roos, et al. 2004. Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ. 11:143-153.
10. Tintinger, G., H. C. Steel, and R. Anderson. 2005. Taming the neutrophil: calcium clearance and influx mechanisms as novel targets for pharmacological control. Clin. Exp. Immunol. 141:191-200.
11. 2+, NAD(P)H and membrane potential changes in pancreatic β-cells by methyl succinate: comparison with glucose. Biochem. J. 403: 197-205.
12. Andersen, A. Z., A. K. Poulsen, J. C. Brasen, and L. F. Olsen. 2007. On-line measurements of oscillating mitochondrial membrane potential in glucose-fermenting Saccharomyces cerevisiae. Yeast. 24:731-739.
13. Poulsen, A. K., A. Z. Andersen, J. C. Brasen, A. M. Scharff-Poulsen, and L. F. Olsen. 2008. Probing glycolytic and membrane potential oscillations in Saccharomyces cerevisiae. Biochemistry. 47:7477-7484.
14. Satroutdinov, A. D., H. Kuriyama, and H. Kobayashi. 1992. Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. FEMS Microbiol. Lett. 98:261-267.
15. Murray, D. B., S. Roller, H. Kuriyama, and D. Lloyd. 2001. Clock control of ultradian respiratory oscillation found during yeast continuous culture. J. Bacteriol. 183:7253-7259.
16. Lloyd, D. 2008. Respiratory oscillations in yeast. In Cellular Oscillatory Mechanisms. Advances in Experimental Medicine and Biology, Vol. 641. M. Maroto and N. A. M. Monk, editors. Springer, Berlin. 118-140.
17. Murray, D. B., M. Beckmann, and H. Kitano. 2007. Regulation of yeast oscillatory dynamics. Proc. Natl. Acad. Sci. USA. 104:2241-2246.
18. Duysens, L. N. M., and J. Amesz. 1957. Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the nearultravioloet and visible region. Biochim. Biophys. Acta. 24:19-26.
19. Chance, B., R. W. Estabrook, and A. Ghosh. 1964. Damped sinusoidal oscillations of cytoplasmic reduced pyridine nucleotide in yeast cells. Proc. Natl. Acad. Sci. USA. 51:1244-1251.
20. Betz, A., and B. Chance. 1965. Influence of inhibitors and temperature on oscillation of reduced pyridine nucleotides in yeast cells. Arch. Biochem. Biophys. 109:579-584.
21. Poulsen, A. K., F. R. Lauritsen, and L. F. Olsen. 2004. Sustained glycolytic oscillations - no need for cyanide. FEMS Microbiol. Lett. 236:261-266.
22. Poulsen, A. K., M. Ø. Petersen, and L. F. Olsen. 2007. Single cell studies and simulation of cell-cell interactions using oscillating glycolysis in yeast cells. Biophys. Chem. 125:275-280.
23. De Monte, S., F. d'Ovidio, S. Danø, and P. G. Sørensen. 2007. Dynamical quorum sensing: population density encoded in cellular dynamics. Proc. Natl. Acad. Sci. USA. 104:18377-18381.
24. Aon, M. A., S. Cortassa, K. M. Lemar, A. J. Hayes, and D. Lloyd. 2007. Single and cell population respiratory oscillations in yeast: a 2-photon scanning laser microscopy study. FEBS Lett. 581:8-14.
25. Aon, M. A., S. Cortassa, and B. O'Rourke. 2008. Mitochondrial oscillations in physiology and pathophysiology. In Cellular Oscillatory Mechanisms. Advances in Experimental Medicine and Biology, Vol. 641. M. Maroto and N. A. M. Monk, editors. Springer, Berlin. 98-117.
26. Winkler, H. H., F. L. Bygrave, and A. L. Lehninger. 1968. Characterization of the atractyloside-sensitive adenine nucleotide transport system in rat liver mitochondria. J. Biol. Chem. 243:20-28.
27. Kovac, L., T. Galeotti, and B. Hess. 1968. Oligomycin-like inhibition of yeast respiration by N,N'-dicyclohexylcarbodiimide and nature of energy coupling in intact yeast cells. Biochim. Biophys. Acta. 153:715-717.
28. Beattie, D. S., and A. Villalobo. 1982. Energy transduction by the reconstituted b-c1 complex from yeast mitochondria. Inhibitory effects of dicyclohexylcarbodiimide. J. Biol. Chem. 257:14745-14752.
29. +-ATPase by dicyclohexylcarbodiimide: binding stoichiometry and effect of nucleophiles. Arch. Biochem. Biophys. 346:294-302.
30. Halm, M., T. Hornbæk, N. Arneborg, S. Sefa-Dedeh, and L. Jespersen. 2004. Lactic acid tolerance determined by measurement of intracellular pH of single cells of Candida kruesei and Sachharomyces cerevisiae isolated from fermented maize dough. Int. J. Food Microbiol. 94: 97-103.
31. +-ATPase. J. Microbiol. Methods. 31:113-125.
32. Gonzales, B., J. Francios, and M. Reneaud. 1997. A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol. Yeast. 13:1347-1356.
33. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:265-275.
34. 13C-NMR spectroscopy. Eur. J. Biochem. 218:221-228.
35. Webb, J. 1966. Enzyme and. . Metabolic Inhibitors., Vol. 3. Academic Press, New York.
36. Tran-Dinh, S., M. Hervé, O. Lebourguais, M. Jerome, and J. Wietzerbin. 1991. Effects of amphotericin B on the glucose metabolism in Saccharomyces cevevisiae cells: Studies by 13C-, 1H-NMR and biochemical methods. Eur. J. Biochem. 197:271-279.
37. Keilin, D., and E. F. Hartree. 1939. Cytochrome and cytochrome oxidase. Proc. R. Soc. Lond. B. Biol. Sci. 127:167-191.
38. Rosenfeld, E., B. Beauvoit, M. Rigoulet, and J. M. Salmon. 2002. Nonrespiratory oxygen consumption pathways in anaerobically-grown Saccharomyces cerevisiae: evidence and partial characterization. Yeast. 19:1299-1321.
39. 1-ATPase. Biochim. Biophys. Acta. 974:156-162.
40. Vanderhoff, B. T., and R. M. Tahboub. 2002. Proton pump inhibitors: an update. Am. Fam. Physician. 66:273-280.
41. Monk, B. C., A. B. Mason, G. Abramochkin, J. E. Haber, D. Seto-Young, et al. 1995. The yeast plasma membrane proton pumping ATPase is a viable antifungal target. I. Effects of the cysteine-modifying reagent omeprazole. Biochim. Biophys. Acta. 1239:81-90.
42. Larsson, C., A. Nielsson, A. Blomberg, and L. Gustafsson. 1997. Glycolytic flux is conditionally correlated with ATP concentration in Saccharomyces cerevisiae: a chemostat study under carbon- or nitrogen-limiting conditions. J. Bacteriol. 179:7243-7250.
43. Richard, P., B. Teusink, M. B. Hemker, K. Van Dam, and H. V. Westerhoff. 1996. Sustained oscillations in free-energy state and hexose phosphates in yeast. Yeast. 12:731-740.
44. Bracey, D., C. D. Holyoak, and P. J. Coote. 1998. Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae: is growth inhibition dependent on the intracellular pH? J. Appl. Microbiol. 85:1056-1066.
45. Aon, M. A., S. Cortassa, H. V. Westerhoff, J. A. Berden, E. Van Spronsen, et al. 1991. Dynamic regulation of yeast glycolytic oscillations by mitochondrial functions. J. Cell Sci. 99:325-334.
46. Chance, B., B. Hess, and A. Betz. 1964. DNPH oscillations in a cell-free extract of. S. carlsbergensis. Biochem. Biophys. Res. Commun. 16: 182-187.
47. Reijenga, K. A., J. L. Snoep, J. A. Diderich, H. W. van Verseveld, H. V. Westerhoff, et al. 2001. Control of glycolytic dynamics by hexose transport in Saccharomyces cerevisiae. Biophys. J. 80:626-634.
48. Ashcroft, F. M., D. E. Harrison, and S. J. Ashcroft. 1984. Glucose induces closure of single potassium channels in isolated rat pancreatic β-cells. Nature. 312:446-448.
49. + channels in pancreatic b-cells. Nature. 311:271-273.
50. Hopkins, W. F., S. Fatherazi, B. Peter-Riesch, B. E. Corkey, and D. L. Cook. 1992. Two sites for adenine-nucleotide regulation of ATP-sensitive potassium channels in mouse pancreatic β-cells and HIT cells. J. Membr. Biol. 129:287-295.
51. Misler, S., L. C. Falke, K. Gillis, and M. L. McDaniel. 1986. A metabolite-regulated potassium channel in rat pancreatic β-cells. Proc. Natl. Acad. Sci. USA. 83:7119-7123.
52. O'Rahilly, S., R. C. Turner, and D. R. Matthews. 1988. Impaired pulsatile secretion of insulin in relatives of patients with non-insulindependent diabetes. N. Engl. J. Med. 318:1225-1230.
53. Polonsky, K. S., B. D. Given, L. J. Hirsch, H. Tillil, E. T. Shapiro, et al. 1988. Abnormal patterns of insulin secretion in non-insulin-dependent diabetes mellitus. N. Engl. J. Med. 318:1231-1239.
54. Ashcroft, F. M., and P. Rorsman. 1989. Electrophysiology of the pancreatic β-cell. Prog. Biophys. Mol. Biol. 54:87-143.
55. 2+ in single islets of Langerhans. J. Biol. Chem. 275:6642-6650.
56. Danø, S., P. G. Sørensen, and F. Hynne. 1999. Sustained oscillations in living cells. Nature. 402:320-322.