Extending the linear-noise approximation to biochemical systems influenced by intrinsic noise and slow lognormally distributed extrinsic noise.

It is well known that the kinetics of an intracellular biochemical network is stochastic. This is due to intrinsic noise arising from the random timing of biochemical reactions in the network as well as due to extrinsic noise stemming from the interaction of unknown molecular components with the network and from the cell's changing environment. While there are many methods to study the effect of intrinsic noise on the system dynamics, few exist to study the influence of both types of noise. Here we show how one can extend the conventional linear-noise approximation to allow for the rapid evaluation of the molecule numbers statistics of a biochemical network influenced by intrinsic noise and by slow lognormally distributed extrinsic noise. The theory is applied to simple models of gene regulatory networks and its validity confirmed by comparison with exact stochastic simulations. In particular, we consider three important biological examples. First, we investigate how extrinsic noise modifies the dependence of the variance of the molecule number fluctuations on the rate constants. Second, we show how the mutual information between input and output of a network motif is affected by extrinsic noise. And third, we study the robustness of the ubiquitously found feed-forward loop motifs when subjected to extrinsic noise.

[1]  Lubomír Brancík,et al.  Simulation of multiconductor transmission lines with random parameters via stochastic differential equations approach , 2016, Simul..

[2]  Philipp Thomas,et al.  How accurate are the nonlinear chemical Fokker-Planck and chemical Langevin equations? , 2011, The Journal of chemical physics.

[3]  P. Alam ‘A’ , 2021, Composites Engineering: An A–Z Guide.

[4]  P. Alam ‘S’ , 2021, Composites Engineering: An A–Z Guide.

[5]  David F Anderson,et al.  A modified next reaction method for simulating chemical systems with time dependent propensities and delays. , 2007, The Journal of chemical physics.

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

[7]  R. Grima,et al.  An effective rate equation approach to reaction kinetics in small volumes: theory and application to biochemical reactions in nonequilibrium steady-state conditions. , 2010, The Journal of chemical physics.

[8]  Fabrizio Gabbiani,et al.  Coding of time-varying signals in spike trains of linear and half-wave rectifying neurons. , 1996, Network.

[9]  Vahid Shahrezaei,et al.  Analytical distributions for stochastic gene expression , 2008, Proceedings of the National Academy of Sciences.

[10]  Johan Paulsson,et al.  Models of stochastic gene expression , 2005 .

[11]  Fabian J. Theis,et al.  Inference for Stochastic Chemical Kinetics Using Moment Equations and System Size Expansion , 2016, PLoS Comput. Biol..

[12]  S. Mangan,et al.  Structure and function of the feed-forward loop network motif , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Hespanha,et al.  Optimal feedback strength for noise suppression in autoregulatory gene networks. , 2009, Biophysical journal.

[14]  Philipp Thomas,et al.  Stochastic Simulation of Biomolecular Networks in Dynamic Environments , 2015, PLoS Comput. Biol..

[15]  Dan S. Tawfik,et al.  The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. , 2011, Biochemistry.

[16]  Nacho Molina,et al.  Mammalian Genes Are Transcribed with Widely Different Bursting Kinetics , 2011, Science.

[17]  Eric Jones,et al.  SciPy: Open Source Scientific Tools for Python , 2001 .

[18]  Deena R. Schmidt,et al.  Steady-state fluctuations of a genetic feedback loop: an exact solution. , 2012, The Journal of chemical physics.

[19]  D. Sherrington Stochastic Processes in Physics and Chemistry , 1983 .

[20]  Uri Alon,et al.  Environmental selection of the feed-forward loop circuit in gene-regulation networks , 2005, Physical biology.

[21]  Javier Macía,et al.  Specialized or flexible feed-forward loop motifs: a question of topology , 2009, BMC Systems Biology.

[22]  Kunihiko Kaneko,et al.  Ubiquity of log-normal distributions in intra-cellular reaction dynamics , 2005, Biophysics.

[23]  F. Tostevin,et al.  Mutual information between input and output trajectories of biochemical networks. , 2009, Physical review letters.

[24]  Elijah Roberts,et al.  Dynamics of simple gene-network motifs subject to extrinsic fluctuations. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[25]  P. Swain,et al.  Gene Regulation at the Single-Cell Level , 2005, Science.

[26]  L. Gerace,et al.  The size-wise nucleus: nuclear volume control in eukaryotes , 2007, The Journal of cell biology.

[27]  Haidong Feng,et al.  Stochastic expression dynamics of a transcription factor revealed by single-molecule noise analysis , 2012, Nature Structural &Molecular Biology.

[28]  Philipp Thomas,et al.  System size expansion using Feynman rules and diagrams , 2014, 1409.1439.

[29]  Margaritis Voliotis,et al.  The magnitude and colour of noise in genetic negative feedback systems , 2012, Nucleic acids research.

[30]  I. Nemenman,et al.  Information Transduction Capacity of Noisy Biochemical Signaling Networks , 2011, Science.

[31]  Markus Ritter,et al.  Altered cell volume regulation in ras oncogene expressing NIH fibroblasts , 1992, Pflügers Archiv.

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

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

[34]  B. Ingalls,et al.  Estimations of intrinsic and extrinsic noise in models of nonlinear genetic networks. , 2006, Chaos.

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

[36]  T. Zhou,et al.  Physical limits of feedback noise-suppression in biological networks , 2009, Physical biology.

[37]  P. Alam ‘O’ , 2021, Composites Engineering: An A–Z Guide.

[38]  J. Raser,et al.  Control of Stochasticity in Eukaryotic Gene Expression , 2004, Science.

[39]  Daniel T Gillespie,et al.  Stochastic simulation of chemical kinetics. , 2007, Annual review of physical chemistry.

[40]  J. Herskowitz,et al.  Proceedings of the National Academy of Sciences, USA , 1996, Current Biology.

[41]  J. Timmer,et al.  Signatures of nonlinearity in single cell noise-induced oscillations. , 2013, Journal of theoretical biology.

[42]  Ramon Grima,et al.  Approximation and inference methods for stochastic biochemical kinetics—a tutorial review , 2016, 1608.06582.

[43]  E. Cox,et al.  Real-Time Kinetics of Gene Activity in Individual Bacteria , 2005, Cell.

[44]  Zhixing Cao,et al.  Accuracy of parameter estimation for auto-regulatory transcriptional feedback loops from noisy data , 2019, Journal of the Royal Society Interface.

[45]  Bruce Tidor,et al.  Combined Model of Intrinsic and Extrinsic Variability for Computational Network Design with Application to Synthetic Biology , 2013, PLoS Comput. Biol..

[46]  王丹,et al.  Plos Computational Biology主编关于论文获得发表的10条简单法则的评析 , 2009 .

[47]  R. Grima,et al.  Linear mapping approximation of gene regulatory networks with stochastic dynamics , 2018, Nature Communications.

[48]  J. Elf,et al.  Transcription factor binding kinetics constrain noise suppression via negative feedback , 2013, Nature Communications.

[49]  M. Selbach,et al.  Global quantification of mammalian gene expression control , 2011, Nature.

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

[51]  Ramon Grima,et al.  A study of the accuracy of moment-closure approximations for stochastic chemical kinetics. , 2012, The Journal of chemical physics.

[52]  J. Raser,et al.  Noise in Gene Expression: Origins, Consequences, and Control , 2005, Science.

[53]  T. Elston,et al.  Stochasticity in gene expression: from theories to phenotypes , 2005, Nature Reviews Genetics.

[54]  Emma M. Keizer,et al.  Stochastic gene expression in Arabidopsis thaliana , 2017, Nature Communications.

[55]  Andy R. Terrel,et al.  SymPy: Symbolic computing in Python , 2017, PeerJ Prepr..

[56]  E. Marcotte,et al.  Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation , 2007, Nature Biotechnology.

[57]  Ramon Grima,et al.  Linear-noise approximation and the chemical master equation agree up to second-order moments for a class of chemical systems. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  Benjamin Lindner,et al.  A frequency-resolved mutual information rate and its application to neural systems. , 2015, Journal of neurophysiology.

[59]  N. Kampen,et al.  a Power Series Expansion of the Master Equation , 1961 .

[60]  Konstantinos Michalodimitrakis,et al.  Noise in transcription negative feedback loops: simulation and experimental analysis , 2006, Molecular systems biology.

[61]  P. Rorsman,et al.  Gene expression profiling in single cells from the pancreatic islets of Langerhans reveals lognormal distribution of mRNA levels. , 2005, Genome research.

[62]  Diego A Oyarzún,et al.  Noise propagation in synthetic gene circuits for metabolic control. , 2015, ACS synthetic biology.

[63]  Jörg Stelling,et al.  Counter-intuitive stochastic behavior of simple gene circuits with negative feedback. , 2010, Biophysical journal.

[64]  Iain G. Johnston,et al.  Mitochondrial Variability as a Source of Extrinsic Cellular Noise , 2011, PLoS Comput. Biol..

[65]  U. Alon,et al.  Negative autoregulation speeds the response times of transcription networks. , 2002, Journal of molecular biology.

[66]  Gorjan Alagic,et al.  #p , 2019, Quantum information & computation.

[67]  Niraj Kumar,et al.  Exact distributions for stochastic gene expression models with bursting and feedback. , 2014, Physical review letters.

[68]  S. Swain Handbook of Stochastic Methods for Physics, Chemistry and the Natural Sciences , 1984 .