Bounded noises as a natural tool to model extrinsic fluctuations in biomolecular networks

In the first part of this invited paper we review the role of both extrinsic and intrinsic stochasticity in shaping the dynamics of biomolecular networks. In particular, we stress the use of bounded stochastic processes as a model of extrinsic random perturbations. In the second part, we propose three examples of molecular circuits under the influence of external fluctuations modeled by means of bounded noises. The first two examples involve the linear decay of a protein with, respectively, large or low number of molecules, so to stress different modeling approaches. The third example concerns the spatio-temporal dynamics of proteins determining the chemotaxis-driven polarization of a cell. In these examples one can observe phenomena that are dependent on the specific class of employed bounded noise.

[1]  A. J. Homburg,et al.  BIFURCATIONS OF RANDOM DIFFERENTIAL EQUATIONS WITH BOUNDED NOISE ON SURFACES. , 2010, Topological methods in nonlinear analysis.

[2]  A. Coniglio,et al.  Diffusion-limited phase separation in eukaryotic chemotaxis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[3]  A. Macieira-Coelho,et al.  Asymmetric Cell Division , 2010 .

[4]  D. Gillespie The chemical Langevin equation , 2000 .

[5]  Lin Yk,et al.  Generation of non-Gaussian stationary stochastic processes. , 1996 .

[6]  V. Araújo Random Dynamical Systems , 2006, math/0608162.

[7]  S. Franciscis,et al.  Spatio-temporal sine-Wiener bounded noise and its effect on Ginzburg–Landau model , 2012, 1206.6020.

[8]  Gregory D. Smith,et al.  The capacity for multistability in small gene regulatory networks , 2009 .

[9]  Wei Guo,et al.  Transitions induced by time delays and cross-correlated sine-Wiener noises in a tumor–immune system interplay , 2012 .

[10]  N. Friedman,et al.  Stochastic protein expression in individual cells at the single molecule level , 2006, Nature.

[11]  V. M. Kenkre,et al.  Modern Challenges in Statistical Mechanics: Patterns, Noise, and the Interplay of Nonlinearity and Complexity , 2003 .

[12]  Anirvan M. Sengupta,et al.  Engineering aspects of enzymatic signal transduction: photoreceptors in the retina. , 2000, Biophysical journal.

[13]  P. Swain,et al.  Stochastic Gene Expression in a Single Cell , 2002, Science.

[14]  Jacques Demongeot,et al.  High-dimensional Switches and the Modeling of Cellular Differentiation 2.2 Mathematical Models , 2022 .

[15]  René Lefever,et al.  Noise-Induced Transitions: Theory and Applications in Physics, Chemistry, and Biology , 2007 .

[16]  L. Glass,et al.  The logical analysis of continuous, non-linear biochemical control networks. , 1973, Journal of theoretical biology.

[17]  Raul Toral,et al.  Effect of non-Gaussian noise sources in a noise-induced transition , 2004 .

[18]  M. Thattai,et al.  Attenuation of noise in ultrasensitive signaling cascades. , 2002, Biophysical journal.

[19]  Luca Ridolfi,et al.  Noise-Induced Phenomena in the Environmental Sciences , 2011 .

[20]  Matteo Semplice,et al.  A Bistable Model of Cell Polarity , 2012, PloS one.

[21]  Eduardo Sontag,et al.  Untangling the wires: A strategy to trace functional interactions in signaling and gene networks , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Gardiner Handbook of Stochastic Methods , 1983 .

[23]  Daniel T. Gillespie,et al.  Approximating the master equation by Fokker–Planck‐type equations for single‐variable chemical systems , 1980 .

[24]  W. Schieve,et al.  Stochastic model of linear, continuous protein synthesis in bacterial populations. , 1977, Journal of theoretical biology.

[25]  Claude Desplan,et al.  Stochasticity and Cell Fate , 2008, Science.

[26]  Alexandra Jilkine,et al.  Wave-pinning and cell polarity from a bistable reaction-diffusion system. , 2008, Biophysical journal.

[27]  Alberto d’Onofrio,et al.  Bounded Noises in Physics, Biology, and Engineering , 2013 .

[28]  J. M. Sancho,et al.  A nonequilibrium phase transition with colored noise , 1992 .

[29]  Lisa Borland,et al.  Ito-Langevin equations within generalized thermostatistics , 1998 .

[30]  Alberto d'Onofrio,et al.  Multifaceted kinetics of immuno-evasion from tumor dormancy. , 2013, Advances in Experimental Medicine and Biology.

[31]  Benjamin B. Kaufmann,et al.  Contributions of low molecule number and chromosomal positioning to stochastic gene expression , 2005, Nature Genetics.

[32]  B. Kholodenko,et al.  Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades , 2004, The Journal of cell biology.

[33]  Z Simon,et al.  Multi-steady-state model for cell differentiation. , 1965, Journal of theoretical biology.

[34]  J. Griffith Mathematics of cellular control processes. II. Positive feedback to one gene. , 1968, Journal of theoretical biology.

[35]  Vladimir P. Zhdanov,et al.  Interplay of bistable kinetics of gene expression during cellular growth , 2009 .

[36]  J. Hasty,et al.  Noise-based switches and amplifiers for gene expression. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Giancarlo Mauri,et al.  NoisySim: exact simulation of stochastic chemically reacting systems with extrinsic bounded noises (WIP) , 2013, SpringSim.

[38]  B. Mandelbrot The Variation of Certain Speculative Prices , 1963 .

[39]  R. Thomas,et al.  Logical analysis of systems comprising feedback loops. , 1978, Journal of theoretical biology.

[40]  Pablo A Iglesias,et al.  Navigating through models of chemotaxis. , 2008, Current opinion in cell biology.

[41]  Cai,et al.  Generation of non-Gaussian stationary stochastic processes. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[42]  Pablo A. Iglesias,et al.  Control Theory and Systems Biology , 2009 .

[43]  G. Cai,et al.  On Bounded Stochastic Processes , 2013 .

[44]  Vladimir P. Zhdanov,et al.  Periodic perturbation of the bistable kinetics of gene expression , 2011 .

[45]  A. Turing,et al.  The chemical basis of morphogenesis. 1953. , 1990, Bulletin of mathematical biology.

[46]  D. Gillespie A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions , 1976 .

[47]  E. O’Shea,et al.  Global analysis of protein expression in yeast , 2003, Nature.

[48]  G. Vinnicombe,et al.  Fundamental limits on the suppression of molecular fluctuations , 2010, Nature.

[49]  A. J. Homburg,et al.  Bifurcations of random differential equations , 2013 .

[50]  Alberto d'Onofrio,et al.  Bounded-noise-induced transitions in a tumor-immune system interplay. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[51]  Hannah H. Chang,et al.  Multistable and multistep dynamics in neutrophil differentiation , 2006, BMC Cell Biology.

[52]  A. Arkin,et al.  Stochastic amplification and signaling in enzymatic futile cycles through noise-induced bistability with oscillations. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[53]  A. Turing The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[54]  Julien F. Ollivier,et al.  Colored extrinsic fluctuations and stochastic gene expression , 2008, Molecular systems biology.

[55]  Darren J. Wilkinson Stochastic Modelling for Systems Biology , 2006 .

[56]  Giulio Caravagna,et al.  Investigating the Relation between Stochastic Differentiation, Homeostasis and Clonal Expansion in Intestinal Crypts via Multiscale Modeling , 2014, PloS one.

[57]  Bernhard O. Palsson,et al.  Systems Biology: Simulation of Dynamic Network States , 2011 .

[58]  L. Ramírez-Piscina,et al.  Generation of spatiotemporal colored noise. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[59]  S. Kauffman Metabolic stability and epigenesis in randomly constructed genetic nets. , 1969, Journal of theoretical biology.

[60]  C. Rao,et al.  Control, exploitation and tolerance of intracellular noise , 2002, Nature.

[61]  Lei Wang,et al.  Bistable switches control memory and plasticity in cellular differentiation , 2009, Proceedings of the National Academy of Sciences.

[62]  Giancarlo Mauri,et al.  The Interplay of Intrinsic and Extrinsic Bounded Noises in Biomolecular Networks , 2012, PloS one.

[63]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[64]  Jung,et al.  Dynamical systems: A unified colored-noise approximation. , 1987, Physical review. A, General physics.

[65]  J. Ferrell,et al.  A positive-feedback-based bistable ‘memory module’ that governs a cell fate decision , 2003, Nature.

[66]  L. Serrano,et al.  Engineering stability in gene networks by autoregulation , 2000, Nature.

[67]  M. Elowitz,et al.  Functional roles for noise in genetic circuits , 2010, Nature.

[68]  B. Mandlebrot The Variation of Certain Speculative Prices , 1963 .

[69]  M. Thattai,et al.  Intrinsic noise in gene regulatory networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. Antoniotti,et al.  Investigating the relation between stochastic differentiation and homeostasis in intestinal crypts via multiscale modeling , 2013, bioRxiv.

[71]  Henryk Gzyl,et al.  Noise-induced transitions: Theory and applications in physics, chemistry and biology , 1988 .

[72]  A. Chrzȩszczyk,et al.  Transitions in a Duffing oscillator excited by random noise , 2008 .

[73]  Peter Hänggi,et al.  Fluctuations in reversible chemical reactions , 1983 .

[74]  Giancarlo Mauri,et al.  Bounded Extrinsic Noises Affecting Biochemical Networks with Low Molecule Numbers , 2013 .

[75]  H. Meinhardt Orientation of chemotactic cells and growth cones: models and mechanisms. , 1999, Journal of cell science.

[76]  Alberto d'Onofrio,et al.  Spatiotemporal bounded noises and transitions induced by them in solutions of the real Ginzburg-Landau model. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[77]  J. Collins,et al.  Construction of a genetic toggle switch in Escherichia coli , 2000, Nature.

[78]  Mikhail F. Dimentberg,et al.  Statistical dynamics of nonlinear and time-varying systems , 1988 .

[79]  Vladimir P. Zhdanov,et al.  Periodic perturbation of genetic oscillations , 2012 .

[80]  A. d’Onofrio,et al.  Cellular polarization: interaction between extrinsic bounded noises and the wave-pinning mechanism. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[81]  Tsz-Leung To,et al.  Noise Can Induce Bimodality in Positive Transcriptional Feedback Loops Without Bistability , 2010, Science.

[82]  Georg R. Walther,et al.  Deterministic Versus Stochastic Cell Polarisation Through Wave-Pinning , 2012, Bulletin of mathematical biology.

[83]  M SUGITA,et al.  Functional analysis of chemical systems in vivo using a logical circuit equivalent. , 1966, Journal of theoretical biology.

[84]  Roman V. Bobryk,et al.  Transitions induced by bounded noise , 2005 .

[85]  P. Bork,et al.  Evolution of biomolecular networks — lessons from metabolic and protein interactions , 2009, Nature Reviews Molecular Cell Biology.

[86]  D. Gillespie Exact Stochastic Simulation of Coupled Chemical Reactions , 1977 .

[87]  H. Wio,et al.  Noise-Induced Phenomena: Effects of Noises Based on Tsallis Statistics , 2013 .

[88]  C. V. Rao,et al.  Calling heads from tails: the role of mathematical modeling in understanding cell polarization. , 2009, Current opinion in cell biology.

[89]  Alberto Gandolfi,et al.  Resistance to antitumor chemotherapy due to bounded-noise-induced transitions. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[90]  Martin Fussenegger,et al.  Hysteresis in a synthetic mammalian gene network. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Olaf Wolkenhauer,et al.  Stochastic approaches in systems biology , 2010, Wiley interdisciplinary reviews. Systems biology and medicine.

[92]  Kevin R. Sanft,et al.  Legitimacy of the stochastic Michaelis-Menten approximation. , 2011, IET systems biology.