Identifiability analysis for stochastic differential equation models in systems biology

Mathematical models are routinely calibrated to experimental data, with goals ranging from building predictive models to quantifying parameters that cannot be measured. Whether or not reliable parameter estimates are obtainable from the available data can easily be overlooked. Such issues of parameter identifiability have important ramifications for both the predictive power of a model, and the mechanistic insight that can be obtained. Identifiability analysis is well-established for deterministic, ordinary differential equation (ODE) models, but there are no commonly-adopted methods for analysing identifiability in stochastic models. We provide an accessible introduction to identifiability analysis and demonstrate how existing ideas for analysis of ODE models can be applied to stochastic differential equation (SDE) models through four practical case studies. To assess structural identifiability, we study ODEs that describe the statistical moments of the stochastic process using open-source software tools. Using practically-motivated synthetic data and Markov-chain Monte Carlo (MCMC) methods, we assess parameter identifiability in the context of available data. Our analysis shows that SDE models can often extract more information about parameters than deterministic descriptions. All code used to perform the analysis is available on Github.

[1]  Umberto Picchini Inference for SDE Models via Approximate Bayesian Computation , 2012, 1204.5459.

[2]  Michael A. Gibson,et al.  Efficient Exact Stochastic Simulation of Chemical Systems with Many Species and Many Channels , 2000 .

[3]  Eric A. Sobie,et al.  Parameter sensitivity analysis of stochastic models provides insights into cardiac calcium sparks. , 2013, Biophysical journal.

[4]  S. Isaacson Relationship between the reaction–diffusion master equation and particle tracking models , 2008 .

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

[6]  Andrea Facchinetti,et al.  Continuous Glucose Monitoring Sensors: Past, Present and Future Algorithmic Challenges , 2016, Sensors.

[7]  Paul D. W. Kirk,et al.  MEANS: python package for Moment Expansion Approximation, iNference and Simulation , 2016, Bioinform..

[8]  Julio R. Banga,et al.  SUPPLEMENTARY FILE: Full observability and estimation of unknown inputs, states, and parameters of nonlinear biological models , 2019 .

[9]  K. Burrage,et al.  High strong order explicit Runge-Kutta methods for stochastic ordinary differential equations , 1996 .

[10]  Robert Kohn,et al.  Particle Methods for Stochastic Differential Equation Mixed Effects Models , 2019, 1907.11017.

[11]  Heyrim Cho,et al.  Mathematical modeling with single-cell sequencing data , 2019, bioRxiv.

[12]  Marisa C. Eisenberg,et al.  Parameter estimation for multistage clonal expansion models from cancer incidence data: A practical identifiability analysis , 2017, PLoS Comput. Biol..

[13]  Kevin Burrage,et al.  Modeling ion channel dynamics through reflected stochastic differential equations. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  Christopher M. Baker,et al.  Persistence as an optimal hedging strategy , 2019, bioRxiv.

[15]  Antonis Papachristodoulou,et al.  Structural Identifiability of Dynamic Systems Biology Models , 2016, PLoS Comput. Biol..

[16]  I. Simon,et al.  Studying and modelling dynamic biological processes using time-series gene expression data , 2012, Nature Reviews Genetics.

[17]  R. Miura,et al.  A Model of β -Cell Mass, Insulin, and Glucose Kinetics: Pathways to Diabetes , 2000 .

[18]  J. Banga,et al.  Structural Identifiability of Systems Biology Models: A Critical Comparison of Methods , 2011, PloS one.

[19]  Kevin Burrage,et al.  Stochastic simulation in systems biology , 2014, Computational and structural biotechnology journal.

[20]  David Welch,et al.  Approximate Bayesian computation scheme for parameter inference and model selection in dynamical systems , 2009, Journal of The Royal Society Interface.

[21]  E. Heyer,et al.  Social transmission of reproductive behavior increases frequency of inherited disorders in a young-expanding population. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  K R Godfrey,et al.  The structural identifiability and parameter estimation of a multispecies model for the transmission of mastitis in dairy cows. , 2001, Mathematical biosciences.

[23]  D. Gillespie Approximate accelerated stochastic simulation of chemically reacting systems , 2001 .

[24]  Matthew J Simpson,et al.  Simulation and inference algorithms for stochastic biochemical reaction networks: from basic concepts to state-of-the-art , 2018, Journal of the Royal Society Interface.

[25]  Andrew Gelman,et al.  General methods for monitoring convergence of iterative simulations , 1998 .

[26]  J. Timmer,et al.  Local Riemannian geometry of model manifolds and its implications for practical parameter identifiability , 2019, PloS one.

[27]  Maria Pia Saccomani,et al.  Parameter identifiability of nonlinear systems: the role of initial conditions , 2003, Autom..

[28]  D. L. Sean McElwain,et al.  Estimating cell diffusivity and cell proliferation rate by interpreting IncuCyte ZOOM™ assay data using the Fisher-Kolmogorov model , 2015, BMC Systems Biology.

[29]  Eric Deleersnijder,et al.  A high-order conservative Patankar-type discretisation for stiff systems of production-destruction equations , 2003 .

[30]  Stefan Engblom,et al.  Computing the moments of high dimensional solutions of the master equation , 2006, Appl. Math. Comput..

[31]  U. Alon,et al.  Dynamical compensation in physiological circuits , 2016, Molecular systems biology.

[32]  G. Maruyama Continuous Markov processes and stochastic equations , 1955 .

[33]  Jens Timmer,et al.  Joining forces of Bayesian and frequentist methodology: a study for inference in the presence of non-identifiability , 2012, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[34]  R. Kohn,et al.  Speeding Up MCMC by Efficient Data Subsampling , 2014, Journal of the American Statistical Association.

[35]  Sten Bay Jørgensen,et al.  Parameter estimation in stochastic grey-box models , 2004, Autom..

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

[37]  Maria Pia Saccomani,et al.  The Union between Structural and Practical Identifiability Makes Strength in Reducing Oncological Model Complexity: A Case Study , 2018, Complex..

[38]  W. O. Kermack,et al.  A contribution to the mathematical theory of epidemics , 1927 .

[39]  Bryan C. Daniels,et al.  Perspective: Sloppiness and emergent theories in physics, biology, and beyond. , 2015, The Journal of chemical physics.

[40]  R. Erban,et al.  Stochastic modelling of reaction–diffusion processes: algorithms for bimolecular reactions , 2009, Physical biology.

[41]  Alan Edelman,et al.  Julia: A Fresh Approach to Numerical Computing , 2014, SIAM Rev..

[42]  Gregory Forlenza,et al.  cgmanalysis: An R package for descriptive analysis of continuous glucose monitor data , 2019, PloS one.

[43]  Yiannis N. Kaznessis,et al.  A closure scheme for chemical master equations , 2013, Proceedings of the National Academy of Sciences.

[44]  James C. W. Locke,et al.  Using movies to analyse gene circuit dynamics in single cells , 2009, Nature Reviews Microbiology.

[45]  Qing Nie,et al.  DifferentialEquations.jl – A Performant and Feature-Rich Ecosystem for Solving Differential Equations in Julia , 2017, Journal of Open Research Software.

[46]  M. Elowitz,et al.  A synthetic oscillatory network of transcriptional regulators , 2000, Nature.

[47]  Wang Jin,et al.  Identifying density-dependent interactions in collective cell behaviour , 2020, Journal of the Royal Society Interface.

[48]  Dan Cornford,et al.  Variational Inference for Diffusion Processes , 2007, NIPS.

[49]  John K Kruschke,et al.  Bayesian data analysis. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[50]  K. Hausken,et al.  A closure approximation technique for epidemic models , 2010 .

[51]  David A. Rand,et al.  Bayesian inference for dynamic transcriptional regulation; the Hes1 system as a case study , 2007, Bioinform..

[52]  L. Isserlis ON A FORMULA FOR THE PRODUCT-MOMENT COEFFICIENT OF ANY ORDER OF A NORMAL FREQUENCY DISTRIBUTION IN ANY NUMBER OF VARIABLES , 1918 .

[53]  Anna Mummert,et al.  Parameter identification for a stochastic SEIRS epidemic model: case study influenza , 2019, Journal of mathematical biology.

[54]  A. Oudenaarden,et al.  Nature, Nurture, or Chance: Stochastic Gene Expression and Its Consequences , 2008, Cell.

[55]  Q. Sang,et al.  Human Mesenchymal Stem Cells Are Resistant to Paclitaxel by Adopting a Non-Proliferative Fibroblastic State , 2015, PloS one.

[56]  Jorge Hidalgo,et al.  Stochasticity enhances the gaining of bet-hedging strategies in contact-process-like dynamics. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  D. Rubin,et al.  Inference from Iterative Simulation Using Multiple Sequences , 1992 .

[58]  M. Khammash,et al.  Systematic Identification of Signal-Activated Stochastic Gene Regulation , 2013, Science.

[59]  C. Andrieu,et al.  The pseudo-marginal approach for efficient Monte Carlo computations , 2009, 0903.5480.

[60]  M. Beaumont Estimation of population growth or decline in genetically monitored populations. , 2003, Genetics.

[61]  Akihiro Kusumi,et al.  Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. , 2005, Biophysical journal.

[62]  R. Wilkinson Approximate Bayesian computation (ABC) gives exact results under the assumption of model error , 2008, Statistical applications in genetics and molecular biology.

[63]  M. J. Chapman,et al.  The structural identifiability of the susceptible infected recovered model with seasonal forcing. , 2005, Mathematical biosciences.

[64]  Guido Sanguinetti,et al.  The complex chemical Langevin equation. , 2014, The Journal of chemical physics.

[65]  Christopher R. Myers,et al.  Universally Sloppy Parameter Sensitivities in Systems Biology Models , 2007, PLoS Comput. Biol..

[66]  Mark A. Girolami,et al.  Information-Geometric Markov Chain Monte Carlo Methods Using Diffusions , 2014, Entropy.

[67]  A. Lambert,et al.  Pathogen evolution in finite populations: slow and steady spreads the best , 2018, Journal of The Royal Society Interface.

[68]  G. Sanguinetti,et al.  Cox process representation and inference for stochastic reaction–diffusion processes , 2016, Nature Communications.

[69]  A. Doucet,et al.  Particle Markov chain Monte Carlo methods , 2010 .

[70]  E. L. Lehmann,et al.  Theory of point estimation , 1950 .

[71]  P. Moral,et al.  Sequential Monte Carlo samplers , 2002, cond-mat/0212648.

[72]  Nicolette Meshkat,et al.  On Finding and Using Identifiable Parameter Combinations in Nonlinear Dynamic Systems Biology Models and COMBOS: A Novel Web Implementation , 2014, PloS one.

[73]  Elijah Roberts,et al.  Approximation and inference methods for stochastic biochemical kinetics—a tutorial review , 2017 .

[74]  D. Wilkinson,et al.  Bayesian Inference for Stochastic Kinetic Models Using a Diffusion Approximation , 2005, Biometrics.

[75]  Leslaw Socha Linearization Methods for Stochastic Dynamic Systems , 2008 .

[76]  GERMAN ENCISO,et al.  Identifiability of stochastically modelled reaction networks , 2021, European Journal of Applied Mathematics.

[77]  Linda R. Petzold,et al.  Stochastic modelling of gene regulatory networks , 2005 .

[78]  Enrico Gratton,et al.  Probing short-range protein Brownian motion in the cytoplasm of living cells , 2014, Nature Communications.

[79]  Darren J. Wilkinson,et al.  Bayesian inference for nonlinear multivariate diffusion models observed with error , 2008, Comput. Stat. Data Anal..

[80]  Heinz Koeppl,et al.  Quasi-Steady-State Approximations Derived from the Stochastic Model of Enzyme Kinetics , 2017, Bulletin of Mathematical Biology.

[81]  T. Kurtz The Relationship between Stochastic and Deterministic Models for Chemical Reactions , 1972 .

[82]  The structural identifiability of SIR type epidemic models with incomplete immunity and birth targeted vaccination , 2008 .

[83]  Eva Balsa-Canto,et al.  GenSSI 2.0: multi-experiment structural identifiability analysis of SBML models , 2017, Bioinform..

[84]  Ruth E. Baker,et al.  Multilevel rejection sampling for approximate Bayesian computation , 2017, Comput. Stat. Data Anal..

[85]  M. Plank,et al.  Identifying density-dependent interactions in collective cell behaviour , 2019, bioRxiv.

[86]  H P Wynn,et al.  Differential algebra methods for the study of the structural identifiability of rational function state-space models in the biosciences. , 2001, Mathematical biosciences.

[87]  Heather A. Harrington,et al.  The geometry of Sloppiness , 2016, Journal of Algebraic Statistics.

[88]  Peter Guttorp,et al.  Evidence that hematopoiesis may be a stochastic process in vivo , 1996, Nature Medicine.

[89]  Ramon Grima,et al.  Single-cell variability in multicellular organisms , 2018, Nature Communications.

[90]  L. Allen An introduction to stochastic processes with applications to biology , 2003 .

[91]  Arild Thowsen,et al.  Structural identifiability , 1977, 1977 IEEE Conference on Decision and Control including the 16th Symposium on Adaptive Processes and A Special Symposium on Fuzzy Set Theory and Applications.

[92]  Gaudenz Danuser,et al.  Linking data to models: data regression , 2006, Nature Reviews Molecular Cell Biology.

[93]  J. Timmer,et al.  Identification of nucleocytoplasmic cycling as a remote sensor in cellular signaling by databased modeling , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[94]  D. Wilkinson Stochastic modelling for quantitative description of heterogeneous biological systems , 2009, Nature Reviews Genetics.

[95]  Michael B. Giles,et al.  Multilevel Monte Carlo Path Simulation , 2008, Oper. Res..

[96]  M. Feldman,et al.  Population growth of human Y chromosomes: a study of Y chromosome microsatellites. , 1999, Molecular biology and evolution.

[97]  Gerardo Chowell,et al.  Assessing parameter identifiability in compartmental dynamic models using a computational approach: application to infectious disease transmission models , 2019, Theoretical Biology and Medical Modelling.

[98]  Necibe Tuncer,et al.  Structural and practical identifiability analysis of outbreak models. , 2018, Mathematical biosciences.

[99]  Henrik Madsen,et al.  Model Identification Using Stochastic Differential Equation Grey-Box Models in Diabetes , 2013, Journal of diabetes science and technology.

[100]  Ruth E. Baker,et al.  Practical parameter identifiability for spatio-temporal models of cell invasion , 2020, Journal of the Royal Society Interface.

[101]  Matthew J Simpson,et al.  A practical guide to pseudo-marginal methods for computational inference in systems biology. , 2020, Journal of theoretical biology.

[102]  Michael P H Stumpf,et al.  Sensitivity, robustness, and identifiability in stochastic chemical kinetics models , 2011, Proceedings of the National Academy of Sciences.

[103]  Desmond J. Higham,et al.  Modeling and Simulating Chemical Reactions , 2008, SIAM Rev..

[104]  M. Turelli Random environments and stochastic calculus. , 1977, Theoretical population biology.

[105]  Chee-Keng Yap,et al.  SIAN: software for structural identifiability analysis of ODE models , 2018, Bioinform..

[106]  Darren J. Wilkinson,et al.  Bayesian Sequential Inference for Stochastic Kinetic Biochemical Network Models , 2006, J. Comput. Biol..

[107]  Kevin Burrage,et al.  Stochastic approaches for modelling in vivo reactions , 2004, Comput. Biol. Chem..

[108]  P. Donnelly,et al.  Inferring coalescence times from DNA sequence data. , 1997, Genetics.

[109]  Keegan E. Hines,et al.  Determination of parameter identifiability in nonlinear biophysical models: A Bayesian approach , 2014, The Journal of general physiology.

[110]  M. Gutmann,et al.  Approximate Bayesian Computation , 2019, Annual Review of Statistics and Its Application.

[111]  Xiaohua Xia,et al.  On Identifiability of Nonlinear ODE Models and Applications in Viral Dynamics , 2011, SIAM Rev..

[112]  Hye-Won Kang,et al.  Comparison of Deterministic and Stochastic Regime in a Model for Cdc42 Oscillations in Fission Yeast , 2019, Bulletin of mathematical biology.

[113]  Yan Zhou,et al.  Multilevel Particle Filters , 2015, SIAM J. Numer. Anal..

[114]  Jae Kyoung Kim,et al.  Beyond the Michaelis-Menten equation: Accurate and efficient estimation of enzyme kinetic parameters , 2017, Scientific Reports.

[115]  R. Seger,et al.  The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. , 2011, Biochimica et biophysica acta.

[116]  R. Hovorka,et al.  Nonlinear model predictive control of glucose concentration in subjects with type 1 diabetes. , 2004, Physiological measurement.

[117]  Rafael Meza,et al.  A Systematic Approach to Determining the Identifiability of Multistage Carcinogenesis Models , 2017, Risk analysis : an official publication of the Society for Risk Analysis.

[118]  Charles J. Geyer,et al.  Practical Markov Chain Monte Carlo , 1992 .

[119]  Gary R. Mirams,et al.  Uncertainty and variability in computational and mathematical models of cardiac physiology , 2016, The Journal of physiology.

[120]  M. Eisenberg,et al.  The underlying connections between identifiability, active subspaces, and parameter space dimension reduction , 2018, 1802.05641.

[121]  Matthew J Simpson,et al.  Optimal Quantification of Contact Inhibition in Cell Populations. , 2017, Biophysical journal.

[122]  Ursula Klingmüller,et al.  Structural and practical identifiability analysis of partially observed dynamical models by exploiting the profile likelihood , 2009, Bioinform..

[123]  P. Hövel,et al.  Control of self-organizing nonlinear systems , 2016 .

[124]  O. Reiersøl Identifiability of a Linear Relation between Variables Which Are Subject to Error , 1950 .

[125]  G. Roberts,et al.  Retrospective exact simulation of diffusion sample paths with applications , 2006 .

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

[127]  Tom Dhaene,et al.  Review of Polynomial Chaos-Based Methods for Uncertainty Quantification in Modern Integrated Circuits , 2018 .

[128]  Matthew J Simpson,et al.  Quantifying the effect of experimental design choices for in vitro scratch assays. , 2016, Journal of theoretical biology.

[129]  Michael P H Stumpf,et al.  Multivariate moment closure techniques for stochastic kinetic models. , 2015, The Journal of chemical physics.

[130]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.

[131]  Michael I. Jordan,et al.  Learning with Mixtures of Trees , 2001, J. Mach. Learn. Res..

[132]  Alejandro Fernández Villaverde,et al.  Observability and Structural Identifiability of Nonlinear Biological Systems , 2018, Complex..

[133]  Marisa C Eisenberg,et al.  Determining identifiable parameter combinations using subset profiling. , 2014, Mathematical biosciences.

[134]  H. Pohjanpalo System identifiability based on the power series expansion of the solution , 1978 .

[135]  W. K. Hastings,et al.  Monte Carlo Sampling Methods Using Markov Chains and Their Applications , 1970 .

[136]  C. Cobelli,et al.  Parameter and structural identifiability concepts and ambiguities: a critical review and analysis. , 1980, The American journal of physiology.

[137]  P. Nestel,et al.  Distribution and turnover of cholesterol in humans. , 1969, The Journal of clinical investigation.

[138]  Edmund J Crampin,et al.  MCMC can detect nonidentifiable models. , 2012, Biophysical journal.

[139]  Matthew J Simpson,et al.  Inferring parameters for a lattice-free model of cell migration and proliferation using experimental data , 2017, bioRxiv.

[140]  .. W. V. Der,et al.  On Profile Likelihood , 2000 .

[141]  Maria Pia Saccomani,et al.  DAISY: A new software tool to test global identifiability of biological and physiological systems , 2007, Comput. Methods Programs Biomed..

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

[143]  Paul C. Bressloff,et al.  Stochastic switching in biology: from genotype to phenotype , 2017 .

[144]  Gareth O. Roberts,et al.  Examples of Adaptive MCMC , 2009 .

[145]  John Lygeros,et al.  Moment-Based Methods for Parameter Inference and Experiment Design for Stochastic Biochemical Reaction Networks , 2015, ACM Trans. Model. Comput. Simul..

[146]  Duarte Antunes,et al.  Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes , 2016, PLoS Comput. Biol..

[147]  Jens Timmer,et al.  Data-based identifiability analysis of non-linear dynamical models , 2007, Bioinform..

[148]  Zhi-Yong Ran,et al.  Parameter Identifiability in Statistical Machine Learning: A Review , 2017, Neural Computation.

[149]  Julio R. Banga,et al.  Reverse engineering and identification in systems biology: strategies, perspectives and challenges , 2014, Journal of The Royal Society Interface.

[150]  J. Rosenthal,et al.  Optimal scaling for various Metropolis-Hastings algorithms , 2001 .

[151]  Michael P. H. Stumpf,et al.  Maximizing the Information Content of Experiments in Systems Biology , 2013, PLoS Comput. Biol..

[152]  Evelyn Buckwar,et al.  Spectral density-based and measure-preserving ABC for partially observed diffusion processes. An illustration on Hamiltonian SDEs , 2019, Statistics and Computing.

[153]  Kevin Burrage,et al.  Comparison of continuous and discrete stochastic ion channel models , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[154]  G. Marion,et al.  Using model-based proposals for fast parameter inference on discrete state space, continuous-time Markov processes , 2015, Journal of The Royal Society Interface.

[155]  K. S. Brown,et al.  Statistical mechanical approaches to models with many poorly known parameters. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[156]  Dan Cornford,et al.  Gaussian Process Approximations of Stochastic Differential Equations , 2007, Gaussian Processes in Practice.

[157]  Brian Munsky,et al.  Listening to the noise: random fluctuations reveal gene network parameters , 2009, Molecular systems biology.

[158]  Christos-Savvas Bouganis,et al.  Particle MCMC algorithms and architectures for accelerating inference in state-space models☆ , 2017, Int. J. Approx. Reason..

[159]  Julio R. Banga,et al.  A Comparison of Methods for Quantifying Prediction Uncertainty in Systems Biology , 2019, IFAC-PapersOnLine.

[160]  David J. Warne,et al.  Hindsight is 2020 vision: a characterisation of the global response to the COVID-19 pandemic , 2020, BMC Public Health.

[161]  David Gavaghan,et al.  Inference-based assessment of parameter identifiability in nonlinear biological models , 2018, Journal of The Royal Society Interface.

[162]  Eric Mjolsness,et al.  Measuring single-cell gene expression dynamics in bacteria using fluorescence time-lapse microscopy , 2011, Nature Protocols.

[163]  German Enciso,et al.  Embracing Noise in Chemical Reaction Networks , 2019, Bulletin of Mathematical Biology.

[164]  David B Brückner,et al.  Inferring the Dynamics of Underdamped Stochastic Systems. , 2020, Physical review letters.

[165]  João Pedro Hespanha,et al.  A Derivative Matching Approach to Moment Closure for the Stochastic Logistic Model , 2007, Bulletin of mathematical biology.

[166]  Eva Balsa-Canto,et al.  Bioinformatics Applications Note Systems Biology Genssi: a Software Toolbox for Structural Identifiability Analysis of Biological Models , 2022 .

[167]  M. Jirstrand,et al.  Stochastic differential equations as a tool to regularize the parameter estimation problem for continuous time dynamical systems given discrete time measurements. , 2014, Mathematical biosciences.

[168]  Eric Walter,et al.  Identifiability of parametric models , 1987 .

[169]  Jens Timmer,et al.  Likelihood based observability analysis and confidence intervals for predictions of dynamic models , 2011, BMC Systems Biology.

[170]  Johan Karlsson,et al.  Comparison of approaches for parameter identifiability analysis of biological systems , 2014, Bioinform..

[171]  Darren J Wilkinson,et al.  Bayesian parameter inference for stochastic biochemical network models using particle Markov chain Monte Carlo , 2011, Interface Focus.

[172]  Yves Lecourtier,et al.  Unidentifiable compartmental models: what to do? , 1981 .

[173]  A. Oudenaarden,et al.  Cellular Decision Making and Biological Noise: From Microbes to Mammals , 2011, Cell.

[174]  Sarah Filippi,et al.  A framework for parameter estimation and model selection from experimental data in systems biology using approximate Bayesian computation , 2014, Nature Protocols.

[175]  Suresh Kumar Poovathingal,et al.  Global parameter estimation methods for stochastic biochemical systems , 2010, BMC Bioinformatics.

[176]  Ursula Klingmüller,et al.  Simulation Methods for Optimal Experimental Design in Systems Biology , 2003, Simul..

[177]  D. Balding,et al.  Approximate Bayesian computation in population genetics. , 2002, Genetics.

[178]  Radek Erban,et al.  Tensor methods for parameter estimation and bifurcation analysis of stochastic reaction networks , 2015, Journal of The Royal Society Interface.

[179]  J. Lygeros,et al.  Moment-based inference predicts bimodality in transient gene expression , 2012, Proceedings of the National Academy of Sciences.

[180]  Gunnar Cedersund,et al.  Prediction Uncertainty Estimation Despite Unidentifiability: An Overview of Recent Developments , 2016 .

[181]  Christian Kuehn,et al.  Moment Closure—A Brief Review , 2015, 1505.02190.

[182]  John Lygeros,et al.  Designing experiments to understand the variability in biochemical reaction networks , 2013, Journal of The Royal Society Interface.

[183]  Oliver J. Maclaren,et al.  What can be estimated? Identifiability, estimability, causal inference and ill-posed inverse problems , 2019, ArXiv.

[184]  J. Jacquez,et al.  Numerical parameter identifiability and estimability: Integrating identifiability, estimability, and optimal sampling design , 1985 .

[185]  Ruth E. Baker,et al.  Mechanistic and experimental models of cell migration reveal the importance of cell-to-cell pushing in cell invasion , 2019, Biomedical Physics & Engineering Express.

[186]  Thomas House,et al.  Influencing public health policy with data-informed mathematical models of infectious diseases: Recent developments and new challenges. , 2020, Epidemics.

[187]  Dongbin Xiu,et al.  The Wiener-Askey Polynomial Chaos for Stochastic Differential Equations , 2002, SIAM J. Sci. Comput..

[188]  Neil D. Evans,et al.  Parameter Identifiability of Fundamental Pharmacodynamic Models , 2016, Front. Physiol..

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