Glycolytic Synchronization in Yeast Cells via ATP and Other Metabolites: Mathematical Analyses by Two-Dimensional Reaction-Diffusion Models
Affiliation(s)
Graduate School of Environment and Information Sciences, Yokohama National University, Yokohama, Japan.
Graduate School of Environment and Information Sciences, Yokohama National University, Yokohama, Japan.
ABSTRACT
Possibilities of synchronized oscillations in glycolysis mediated by various extracellular metabolites are investigated theoretically using two-dimensional reaction-diffusion systems, which originate from the existing seven-variable model. Our simulation results indicate the existence of alternative mediators such as ATP and 1,3-bisphosphoglycerate, in addition to already known acetaldehyde or pyruvate. Further, it is also suggested that the alternative intercellular communicator plays a more important role in the respect that these can synchronize oscillations instantaneously not only with difference phases but also with different periods. Relations between intercellular coupling and synchronization mechanisms are also analyzed and discussed by changing the values of parameters such as the diffusion coefficient and the cell density that can reflect in tercellular coupling strength.
Possibilities of synchronized oscillations in glycolysis mediated by various extracellular metabolites are investigated theoretically using two-dimensional reaction-diffusion systems, which originate from the existing seven-variable model. Our simulation results indicate the existence of alternative mediators such as ATP and 1,3-bisphosphoglycerate, in addition to already known acetaldehyde or pyruvate. Further, it is also suggested that the alternative intercellular communicator plays a more important role in the respect that these can synchronize oscillations instantaneously not only with difference phases but also with different periods. Relations between intercellular coupling and synchronization mechanisms are also analyzed and discussed by changing the values of parameters such as the diffusion coefficient and the cell density that can reflect in tercellular coupling strength.
KEYWORDS
Acetaldehyde, ATP, Glycolytic Oscillation, Intercellular Coupling, Reaction-Diffusion Model, Synchronization
Acetaldehyde, ATP, Glycolytic Oscillation, Intercellular Coupling, Reaction-Diffusion Model, Synchronization
Cite this paper
Serizawa, H. , Amemiya, T. and Itoh, K. (2014) Glycolytic Synchronization in Yeast Cells via ATP and Other Metabolites: Mathematical Analyses by Two-Dimensional Reaction-Diffusion Models. Natural Science, 6, 719-732. doi: 10.4236/ns.2014.610072.
Serizawa, H. , Amemiya, T. and Itoh, K. (2014) Glycolytic Synchronization in Yeast Cells via ATP and Other Metabolites: Mathematical Analyses by Two-Dimensional Reaction-Diffusion Models. Natural Science, 6, 719-732. doi: 10.4236/ns.2014.610072.
References
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Proceedings of the National Academy of Sciences of the United States of America, 104, 12732-12736. http://dx.doi.org/10.1073/pnas.0702560104 [9] Sel’kov, E.E. (1968) Self-Oscillations in Glycolysis. 1. A Simple Kinetic Model. European Journal of Biochemistry, 4, 79-86. [10] Goldbeter, A. and Lefever, R. (1972) Dissipative Structures for an Allosteric Model. Application to Glycolytic Oscillations. Biophysical Journal, 12, 1302-1315. http://dx.doi.org/10.1016/S0006-3495(72)86164-2 [11] Goldbeter, A. (1973) Patterns of Spatiotemporal Organizationin an Allosteric Enzyme Model. Proceedings of the National Academy of Sciences of the United States of America, 70, 3255-3259. http://dx.doi.org/10.1073/pnas.70.11.3255 [12] Zhang, L., Gao, Q., Wang, Q. and Zhang, X. (2007) Simple and Complex Spatiotemporal Structures in a Glycolytic Allosteric Enzyme Model. Biophysical Chemistry, 125, 112-116. http://dx.doi.org/10.1016/j.bpc.2006.07.004 [13] Straube, R., Vermeer, S., Nicola, E.M. and Mair, T. (2010) Inward Rotating Spiral Waves in Glycolysis. Biophysical- Journal, 99, L04-L06. http://dx.doi.org/10.1016/j.bpj.2010.04.018 [14] Lavrova, A.I., Bagyan, S., Mair, T., Hauser, M.J.B. and Schimansky-Geier, L. (2009) Modeling of Glycolytic Wave Propagation in an Open Spatial Reactor with Inhomogeneous Substrate Influx. BioSystems, 97, 127-133. http://dx.doi.org/10.1016/j.biosystems.2009.04.005 [15] Bier, M., Bakker, B.M. and Westerhoff, H.V. (2000) How Yeast Cells Synchronize Their Glycolytic Oscillations: A Perturbation Analytic Treatment. Biophysical Journal, 78, 1087-1093. http://dx.doi.org/10.1016/S0006-3495(00)76667-7 [16] Wolf, J. and Heinrich, R. (2000) Effect of Cellular Interaction on Glycolytic Oscillation in Yeast: A Theoretical Investigation. Biochemical Journal, 345, 321-334. http://dx.doi.org/10.1042/0264-6021:3450321 [17] Henson, M.A., Müller, D. and Reuss, M. (2002) Cell Population Modelling of Yeast Glycolytic Oscillations. Biochemical Journal, 368, 433-466. http://dx.doi.org/10.1042/BJ20021051 [18] Zhong, X., Malhotra, R. and Guidotti, G. (2003) ATP Uptake in the Golgi and Extracellular Release Require Mcd4 Protein and the Vacuolar H+-ATPase. Journal of Biological Chemistry, 278, 33436-33444. http://dx.doi.org/10.1074/jbc.M305785200 [19] Boyum, R. and Guidotti, G. (1997) Glucose-Dependent, cAMP-Mediated ATP Efflux from Saccharomyces Cerevisiae. Microbiology, 143, 1901-1908. http://dx.doi.org/10.1099/00221287-143-6-1901 [20] Jakubowski, H. and Goldman, E. (1988) Evidence for Cooperation between Cells during Sporulation of the Yeast Saccharomyces cerevisiae. Molecular andCellularBiology, 8, 5166-5178. [21] Schütze, J., Mair, T., Hauser, M.J.B., Falcke, M. and Wolf, J. (2011) Metabolic Synchronization by Traveling Waves in Yeast Cell Layers. Biophysical Journal, 100, 809-813. http://dx.doi.org/10.1016/j.bpj.2010.12.3704 [22] Weber, A., Prokazov, Y., Zuschratter, W. and Hauser, M.J.B. (2012) Desynchronisation of Glycolytic Oscillations in Yeast Cell Populations. PLoS ONE, 7, Article ID: e43276. [23] De Monte, S., d’Ovidio, F., Dan?, S. and S?rensen, P.G. (2007) Dynamical Quorum Sensing: Population Density Encodedin Cellular Dynamics. Proceedings of the National Academy of Sciences of the United States of America, 104, 18377-18381. http://dx.doi.org/10.1073/pnas.0706089104 [24] Tinsley, M.R., Taylor, A.F., Huang, Z. and Showalter, K. (2009) Emergence of Collective Behavior in Groups of Excitable Catalyst-Loaded Particles: Spatiotemporal Dynamical Quorum Sensing. Physical Review Letters, 102, Article ID: 158301. http://dx.doi.org/10.1103/PhysRevLett.102.158301 [25] Taylor, A.F., Tinsley, M.R., Wang, F., Huang, Z. and Showalter, K. (2009) Dynamical Quorum Sensing and Synchronization in Large Populations of Chemical Oscillators. Science, 323, 614-617. http://dx.doi.org/10.1126/science.1166253
[1] Buck, J. and Buck, E. (1968) Mechanism of Rhythmic Synchronous Flashing of Fireflies. Fireflies of Southeast Asia May Use Anticipatory Time-Measuring in Synchronizing Their Flashing. Science, 159, 1319-1327. http://dx.doi.org/10.1126/science.159.3821.1319 [2] Ramírez ávila, G.M., Deneubourg, J.-L., Guisset, J.-L., Wessel, N. and Kurths, J. (2011) Firefly Courtship as the Basis of the Synchronization-Response Principle. Europhysics Letters, 94, Article ID: 60007. http://dx.doi.org/10.1209/0295-5075/94/60007 [3] Betz, A. and Chance, B. (1965) Phase Relationship of Glycolytic Intermediates in Yeast Cells with Oscillatory Metabolic Control. Archives of Biochemistry and Biophysics, 109, 585-594. [4] Hess, B. and Boiteux, A. (1968) Mechanism of Glycolytic Oscillation in Yeast. I. Aerobic and Anaerobic Growth Conditions for Obtaining Glycolytic Oscillation. Hoppe-Seyler’s Zeitschriftfürphysiologische Chemie, 349, 1567-1574. http://dx.doi.org/10.1515/bchm2.1968.349.2.1567 [5] Aon, M.A., Cortassa, S., Westerhoff, H.V. and van Dam, K. (1992) Synchrony and Mutual Stimulation of Yeast Cells during Fast Glycolytic Oscillations. Journal of General Microbiology, 138, 2219-2227. [6] Richard, P., Bakker, B.M., Teusink, B., van Dam, K. and Westerhoff, H.V. (1996) Acetaldehyde Mediatesthe Synchronization of Sustained Glycolytic Oscillations in Populations of Yeast Cells. European Journal of Biochemistry, 235, 238-241. http://dx.doi.org/10.1111/j.1432-1033.1996.00238.x [7] Richard, P. (2003) The Rhythm of Yeast. FEMS Microbiology Reviews, 27, 547-557. http://dx.doi.org/10.1016/S0168-6445(03)00065-2 [8] Dan?, S., Madsen, M.F. and S?rensen, P.G. (2007) Quantitative Characterization of Cell Synchronization in Yeast. Proceedings of the National Academy of Sciences of the United States of America, 104, 12732-12736. http://dx.doi.org/10.1073/pnas.0702560104 [9] Sel’kov, E.E. (1968) Self-Oscillations in Glycolysis. 1. A Simple Kinetic Model. European Journal of Biochemistry, 4, 79-86. [10] Goldbeter, A. and Lefever, R. (1972) Dissipative Structures for an Allosteric Model. Application to Glycolytic Oscillations. Biophysical Journal, 12, 1302-1315. http://dx.doi.org/10.1016/S0006-3495(72)86164-2 [11] Goldbeter, A. (1973) Patterns of Spatiotemporal Organizationin an Allosteric Enzyme Model. Proceedings of the National Academy of Sciences of the United States of America, 70, 3255-3259. http://dx.doi.org/10.1073/pnas.70.11.3255 [12] Zhang, L., Gao, Q., Wang, Q. and Zhang, X. (2007) Simple and Complex Spatiotemporal Structures in a Glycolytic Allosteric Enzyme Model. Biophysical Chemistry, 125, 112-116. http://dx.doi.org/10.1016/j.bpc.2006.07.004 [13] Straube, R., Vermeer, S., Nicola, E.M. and Mair, T. (2010) Inward Rotating Spiral Waves in Glycolysis. Biophysical- Journal, 99, L04-L06. http://dx.doi.org/10.1016/j.bpj.2010.04.018 [14] Lavrova, A.I., Bagyan, S., Mair, T., Hauser, M.J.B. and Schimansky-Geier, L. (2009) Modeling of Glycolytic Wave Propagation in an Open Spatial Reactor with Inhomogeneous Substrate Influx. BioSystems, 97, 127-133. http://dx.doi.org/10.1016/j.biosystems.2009.04.005 [15] Bier, M., Bakker, B.M. and Westerhoff, H.V. (2000) How Yeast Cells Synchronize Their Glycolytic Oscillations: A Perturbation Analytic Treatment. Biophysical Journal, 78, 1087-1093. http://dx.doi.org/10.1016/S0006-3495(00)76667-7 [16] Wolf, J. and Heinrich, R. (2000) Effect of Cellular Interaction on Glycolytic Oscillation in Yeast: A Theoretical Investigation. Biochemical Journal, 345, 321-334. http://dx.doi.org/10.1042/0264-6021:3450321 [17] Henson, M.A., Müller, D. and Reuss, M. (2002) Cell Population Modelling of Yeast Glycolytic Oscillations. Biochemical Journal, 368, 433-466. http://dx.doi.org/10.1042/BJ20021051 [18] Zhong, X., Malhotra, R. and Guidotti, G. (2003) ATP Uptake in the Golgi and Extracellular Release Require Mcd4 Protein and the Vacuolar H+-ATPase. Journal of Biological Chemistry, 278, 33436-33444. http://dx.doi.org/10.1074/jbc.M305785200 [19] Boyum, R. and Guidotti, G. (1997) Glucose-Dependent, cAMP-Mediated ATP Efflux from Saccharomyces Cerevisiae. Microbiology, 143, 1901-1908. http://dx.doi.org/10.1099/00221287-143-6-1901 [20] Jakubowski, H. and Goldman, E. (1988) Evidence for Cooperation between Cells during Sporulation of the Yeast Saccharomyces cerevisiae. Molecular andCellularBiology, 8, 5166-5178. [21] Schütze, J., Mair, T., Hauser, M.J.B., Falcke, M. and Wolf, J. (2011) Metabolic Synchronization by Traveling Waves in Yeast Cell Layers. Biophysical Journal, 100, 809-813. http://dx.doi.org/10.1016/j.bpj.2010.12.3704 [22] Weber, A., Prokazov, Y., Zuschratter, W. and Hauser, M.J.B. (2012) Desynchronisation of Glycolytic Oscillations in Yeast Cell Populations. PLoS ONE, 7, Article ID: e43276. [23] De Monte, S., d’Ovidio, F., Dan?, S. and S?rensen, P.G. (2007) Dynamical Quorum Sensing: Population Density Encodedin Cellular Dynamics. Proceedings of the National Academy of Sciences of the United States of America, 104, 18377-18381. http://dx.doi.org/10.1073/pnas.0706089104 [24] Tinsley, M.R., Taylor, A.F., Huang, Z. and Showalter, K. (2009) Emergence of Collective Behavior in Groups of Excitable Catalyst-Loaded Particles: Spatiotemporal Dynamical Quorum Sensing. Physical Review Letters, 102, Article ID: 158301. http://dx.doi.org/10.1103/PhysRevLett.102.158301 [25] Taylor, A.F., Tinsley, M.R., Wang, F., Huang, Z. and Showalter, K. (2009) Dynamical Quorum Sensing and Synchronization in Large Populations of Chemical Oscillators. Science, 323, 614-617. http://dx.doi.org/10.1126/science.1166253