What makes biochemical networks tick?

In view of the increasing number of reported concentration oscillations in living cells, methods are needed that can identify the causes of these oscillations. These causes always derive from the influences that concentrations have on reaction rates. The influences reach over many molecular reaction steps and are defined by the detailed molecular topology of the network. So-called 'autoinfluence paths', which quantify the influence of one molecular species upon itself through a particular path through the network, can have positive or negative values. The former bring a tendency towards instability. In this molecular context a new graphical approach is presented that enables the classification of network topologies into oscillophoretic and nonoscillophoretic, i.e. into ones that can and ones that cannot induce concentration oscillations. The network topologies are formulated in terms of a set of uni-molecular and bi-molecular reactions, organized into branched cycles of directed reactions, and presented as graphs. Subgraphs of the network topologies are then classified as negative ones (which can) and positive ones (which cannot) give rise to oscillations. A subgraph is oscillophoretic (negative) when it contains more positive than negative autoinfluence paths. Whether the former generates oscillations depends on the values of the other subgraphs, which again depend on the kinetic parameters. An example shows how this can be established. By following the rules of our new approach, various oscillatory kinetic models can be constructed and analyzed, starting from the classified simplest topologies and then working towards desirable complications. Realistic biochemical examples are analyzed with the new method, illustrating two new main classes of oscillophore topologies.

[1]  Markus Eiswirth,et al.  Mechanistic Classification of Chemical Oscillators and the Role of Species , 2007 .

[2]  B. Kholodenko,et al.  Negative feedback and ultrasensitivity can bring about oscillations in the mitogen-activated protein kinase cascades. , 2000, European journal of biochemistry.

[3]  E. L. King,et al.  A Schematic Method of Deriving the Rate Laws for Enzyme-Catalyzed Reactions , 1956 .

[4]  Anders Lansner,et al.  A model of phosphofructokinase and glycolytic oscillations in the pancreatic beta-cell. , 2003, Biophysical journal.

[5]  R Heinrich,et al.  Metabolic regulation and mathematical models. , 1977, Progress in biophysics and molecular biology.

[6]  Brian O'Rourke,et al.  Synchronized Whole Cell Oscillations in Mitochondrial Metabolism Triggered by a Local Release of Reactive Oxygen Species in Cardiac Myocytes* , 2003, Journal of Biological Chemistry.

[7]  Ursula Kummer,et al.  Mechanism of protection of peroxidase activity by oscillatory dynamics. , 2003, European journal of biochemistry.

[8]  M. Savageau Biochemical systems analysis. II. The steady-state solutions for an n-pool system using a power-law approximation. , 1969, Journal of theoretical biology.

[9]  B. Goldstein,et al.  Hormonal regulation of 6‐phosphofructo‐2‐kinase/fructose‐2,6‐bisphosphatase: Kinetic models , 1987, FEBS letters.

[10]  J. V. van Beek,et al.  Coordinated behavior of mitochondria in both space and time: a reactive oxygen species-activated wave of mitochondrial depolarization. , 2004, Biophysical journal.

[11]  R. Heinrich,et al.  Mathematical analysis of a mechanism for autonomous metabolic oscillations in continuous culture of Saccharomyces cerevisiae , 2001, FEBS letters.

[12]  Arthur R. Schulz Enzyme Kinetics: Biochemical systems theory , 1994 .

[13]  John J Tyson,et al.  Monitoring p53's pulse , 2004, Nature Genetics.

[14]  Boris N. Kholodenko,et al.  Control analysis of stationary forced oscillations. , 1999 .

[15]  Uri Alon,et al.  Dynamics of the p53-Mdm2 feedback loop in individual cells , 2004, Nature Genetics.

[16]  M. Volkenstein,et al.  Allosteric enzyme models and their analysis by the theory of graphs. , 1966, Biochimica et biophysica acta.

[17]  David Lloyd,et al.  Respiratory oscillations in yeast: clock‐driven mitochondrial cycles of energization , 2002, FEBS letters.

[18]  B. Hess,et al.  Control of Metabolic Oscillations: Unpredictability, Critical Slowing Down, Optimal Stability and Hysteresis , 1990 .

[19]  J. Tyson,et al.  Regulation of the eukaryotic cell cycle: molecular antagonism, hysteresis, and irreversible transitions. , 2001, Journal of theoretical biology.

[20]  Reinhart Heinrich,et al.  Transduction of intracellular and intercellular dynamics in yeast glycolytic oscillations. , 2000, Biophysical journal.

[21]  Peter Lipp,et al.  Calcium - a life and death signal , 1998, Nature.

[22]  A. Betz,et al.  Control of phosphofructokinase [PFK] activity in conditions simulating those of glycolysing yeast extract , 1969, FEBS letters.

[23]  B. Goldstein,et al.  Critical switch of the metabolic fluxes by phosphofructo‐2‐kinase:fructose‐2,6‐bisphosphatase. A kinetic model , 2002, FEBS letters.

[24]  Eberhard O. Voit,et al.  Biochemical systems theory and metabolic control theory: 2. the role of summation and connectivity relationships , 1987 .

[25]  H V Westerhoff The silicon cell, not dead but live! , 2001, Metabolic engineering.

[26]  B. Goldstein Analysis of cyclic enzyme reaction schemes by the graph-theoretic method. , 1983, Journal of theoretical biology.

[27]  B. N. Goldstein,et al.  A new method for solving the problems of the stationary kinetics of enzymological reactions , 1966 .

[28]  M. J. MacDonald,et al.  Citrate Oscillates in Liver and Pancreatic Beta Cell Mitochondria and in INS-1 Insulinoma Cells* , 2003, Journal of Biological Chemistry.

[29]  Stability of multienzyme systems with feedback regulation: a graph theoretical approach. , 1985, Journal of theoretical biology.

[30]  S. Schuster,et al.  Modelling of simple and complex calcium oscillations , 2002 .

[31]  Barbara M. Bakker,et al.  Acetaldehyde mediates the synchronization of sustained glycolytic oscillations in populations of yeast cells. , 1996, European journal of biochemistry.

[32]  B. Goldstein,et al.  Activity oscillations predicted for pyruvate dehydrogenase complexes , 1994, FEBS letters.

[33]  H. Kacser,et al.  The control of flux. , 1995, Biochemical Society transactions.

[34]  Grégoire Nicolis,et al.  Self-Organization in nonequilibrium systems , 1977 .

[35]  H. Westerhoff,et al.  Thermodynamics and Control of Biological Free-Energy Transduction , 1987 .

[36]  C Reder,et al.  Metabolic control theory: a structural approach. , 1988, Journal of theoretical biology.

[37]  J. Ross,et al.  Operational procedure toward the classification of chemical oscillators , 1991 .