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Inferring parameters for a lattice-free model of cell migration and proliferation using experimental data. (English) Zbl 1394.92019

Summary: Collective cell spreading takes place in spatially continuous environments, yet it is often modelled using discrete lattice-based approaches. Here, we use data from a series of cell proliferation assays, with a prostate cancer cell line, to calibrate a spatially continuous individual based model (IBM) of collective cell migration and proliferation. The IBM explicitly accounts for crowding effects by modifying the rate of movement, direction of movement, and the rate of proliferation by accounting for pair-wise interactions. Taking a Bayesian approach we estimate the free parameters in the IBM using rejection sampling on three separate, independent experimental data sets. Since the posterior distributions for each experiment are similar, we perform simulations with parameters sampled from a new posterior distribution generated by combining the three data sets. To explore the predictive power of the calibrated IBM, we forecast the evolution of a fourth experimental data set. Overall, we show how to calibrate a lattice-free IBM to experimental data, and our work highlights the importance of interactions between individuals. Despite great care taken to distribute cells as uniformly as possible experimentally, we find evidence of significant spatial clustering over short distances, suggesting that standard mean-field models could be inappropriate.

MSC:

92C17 Cell movement (chemotaxis, etc.)
62P10 Applications of statistics to biology and medical sciences; meta analysis
62F15 Bayesian inference

References:

[1] Baker, R. E.; Simpson, M. J., Correcting mean-field approximations for birth-death-movement processes, Phys Rev E, 82, 041905 (2010)
[2] Binder, B. J.; Simpson, M. J., Quantifying spatial structure in experimental observations and agent-based simulations using pair-correlation functions, Phys Rev E, 88, 022705 (2013)
[3] Binny, R. N.; Haridas, P.; James, A.; Law, R.; Simpson, M. J.; Plank, M. J., Spatial structure arising from neighbour-dependent bias in collective cell movement, PeerJ, 4, e1689 (2016)
[4] Binny, R. N.; James, A.; Plank, M. J., Collective cell behaviour with neighbour-dependent proliferation, death and directional bias, Bull Math Biol, 78, 2277-2301 (2016) · Zbl 1357.92007
[5] Bosco, D. B.; Kenworthy, R.; Zorio, D. A.R.; Sang, Q. X.A., Human mesenchymal stem cells are resistant to paclitaxel by adopting a non-proliferative fibroblastic state, PLoS One, 10, e0128511 (2015)
[6] Bourseguin, J.; Bonet, C.; Renaud, E.; Pandiani, C.; Boncompagni, M.; Giuliano, S.; Pawlikowska, P.; Karmous-Benailly, H.; Ballotti, R.; Rosselli, F.; Bertolotto, C., FANCD2 functions as a critical factor downstream of miTF to maintain the proliferation and survival of melanoma cells, Sci Rep, 6, 36539 (2016)
[7] Browning, A. P.; McCue, S. W.; Simpson, M. J., A bayesian computational approach to explore the optimal duration of a cell proliferation assay, Bull Math Biol, 10, 1888-1906 (2017) · Zbl 1373.92004
[8] Cai, A. Q.; Landman, K. A.; Hughes, B. D., Multi-scale modeling of a wound-healing cell migration assay, J Theor Biol, 245, 576-594 (2007) · Zbl 1451.92063
[9] Codling, E. A.; Plank, M. J.; Benhamou, S., Random walk models in biology, J R Soc Interface, 5, 813-834 (2008)
[10] Collis, J.; Connor, A. J.; Paczkowski, M.; Kannan, P.; Pitt-Francis, J.; Byrne, H. M.; Hubbard, M. E., Bayesian calibration, validation and uncertainty quantification for predictive modelling of tumour growth: a tutorial, Bull Math Biol, 79, 939-974 (2017) · Zbl 1372.92042
[11] Fletcher, A. G.; Breward, C. J.W.; Chapman, S. J., Mathematical modelling of monoclonal conversion in the colonic crypt, J Theor Biol, 300, 118-133 (2012) · Zbl 1397.92161
[12] Forbes, C.; Evans, M.; Hastings, N.; Peacock, B., Statistical distributions (2011), 4th ed. John Wiley & Sons: 4th ed. John Wiley & Sons New Jersey · Zbl 1258.62012
[13] Frascoli, F.; Hughes, B. D.; Zaman, M. H.; Landman, K. A., A computational model for collective cellular cotion in three dimensions: general framework and case study for cell pair dynamics, PLoS ONE, 8, e59249 (2013)
[14] Fröhlich, F.; Thomas, P.; Kazeroonian, A.; Theis, F. J.; Grima, R.; Hasenauer, J., Inference for stochastic chemical kinetics using moment equations and system size expansion, PLoS Comput Biol, 12, e1005030 (2016)
[15] Gillespie, D. T., Exact stochastic simulation of coupled chemical reactions, J Phys Chem, 81, 2340-2361 (1977)
[16] Jin, W.; Shah, E. T.; Penington, C. J.; McCue, S. W.; Maini, P. K.; Simpson, M. J., Logistic proliferation of cells in scratch assays is delayed, Bull Math Biol, 79, 1028-1050 (2017) · Zbl 1368.92112
[17] Johnston, S. T.; Ross, J. V.; Binder, B. J.; McElwain, D. L.S.; Haridas, P.; Simpson, M. J., Quantifying the effect of experimental design choices for in vitro scratch assays, J Theor Biol, 400, 19-31 (2016)
[18] Johnston, S. T.; Shah, E. T.; Chopin, L. K.; McElwain, D. L.S.; Simpson, M. J., Estimating cell diffusivity and cell proliferation rate by interpreting incucyte ZOOM TM assay data using the Fisher-Kolmogorov model, BMC Syst Biol, 9, 38 (2015)
[19] Johnston, S. T.; Simpson, M. J.; McElwain, D. L.S.; Binder, B. J.; Ross, J. V., Interpreting scratch assays using pair density dynamics and approximate Bayesian computation, Open Biol, 4, 140097 (2014)
[20] Kabla, A. J., Collective cell migration: leadership, invasion and segregation, J R Soc Interface, 9, 20120448 (2012)
[21] Kaighn, M. E.; Narayan, K. S.; Ohnuki, Y.; Lechner, J. F.; Jones, L. W., Establishment and characterization of a human prostatic carcinoma cell line (PC-3), Invest Urol, 17, 16-23 (1979)
[22] Law, R.; Murrell, D. J.; Dieckmann, U., Population growth in space and time: Spatial logistic equations, Ecology, 84, 252-262 (2003)
[23] Liepe, J.; Kirk, P.; Filippi, S.; Toni, T.; Barnes, C. P.; Stumpf, M. P.H., A framework for parameter estimation and model selection from experimental data in systems biology using approximate bayesian computation, Nat Protoc, 9, 439-456 (2014)
[24] Maclaren, O. J.; Byrne, H. M.; Fletcher, A. G.; Maini, P. K., Models, measurement and inference in epithelial tissue dynamics, Math Biosci Eng, 12, 1321 (2015) · Zbl 1326.92016
[25] Maini, P. K.; McElwain, D. L.S.; Leavesley, D. I., Traveling wave model to interpret a wound-healing cell migration assay for human peritoneal mesothelial cells, Tissue Eng, 10, 475-482 (2004)
[26] Mathworks, 2017. Kernel smoothing function estimate for univariate and bivariate data. http://www.mathworks.com/help/stats/ksdensity.html; Mathworks, 2017. Kernel smoothing function estimate for univariate and bivariate data. http://www.mathworks.com/help/stats/ksdensity.html
[27] Murray, J. D., Mathematical Biology (2002), Springer: Springer Berlin · Zbl 1006.92001
[28] Peirce, S. M.; Van Gieson, E. J.; Skalak, T. C., Multicellular simulation predicts microvascular patterning and in silico tissue assembly, FASEB J, 18, 731-733 (2004)
[29] Plank, M. J.; Simpson, M. J., Models of collective cell behaviour with crowding effects: comparing lattice-based and lattice-free approaches, J R Soc Interface, 9, 2983-2996 (2012)
[30] QUT High Performance Computing, 2017. https://www.student.qut.edu.au/technology/research-computing/high-performance-computing; QUT High Performance Computing, 2017. https://www.student.qut.edu.au/technology/research-computing/high-performance-computing
[31] Read, M.; Andrews, P. S.; Timmis, J.; Kumar, V., Techniques for grounding agent-based simulations in the real domain: a case study in experimental autoimmune encephalomyelitis, Math Comp Model Dyn, 18, 67-86 (2012) · Zbl 1251.93014
[32] Sarapata, E. A.; de Pillis, L. G., A comparison and catalog of intrinsic tumor growth models, Bull Math Biol, 76, 2010-2024 (2014) · Zbl 1300.92042
[33] Schnoerr, D.; Grima, R.; Sanguinetti, G., Cox process representation and inference for stochastic reaction-diffusion processes, Nat Commun, 7, 11729 (2016)
[34] Schnoerr, D.; Sanguinetti, G.; Grima, R., Approximation and inference methods for stochastic biochemical kineticsa tutorial review, J Phys A, 50, 093001 (2017) · Zbl 1360.92051
[35] Sengers, B. G.; Please, C. P.; Oreffo, R. O.C., Experimental characterization and computational modelling of two-dimensional cell spreading for skeletal regeneration, J R Soc Interface, 4, 1107 (2007)
[36] Sharkey, K. J., Deterministic epidemiological models at the individual level, J Math Biol, 57, 311-331 (2008) · Zbl 1141.92039
[37] Sharkey, K. J.; Fernandez, C.; Morgan, K. L.; Peeler, E.; Thrush, M.; Turnbull, J. F.; Bowers, R. G., Pair-level approximations to the spatio-temporal dynamics of epidemics on asymmetric contact networks, J Math Biol, 53, 61-85 (2006) · Zbl 1100.92056
[38] Sherratt, J. A.; Murray, J. D., Models of epidermal wound healing, P Roy Soc Lond B, 241, 29 (1990) · Zbl 0721.92010
[39] Simpson, M. J.; Landman, K. A.; Hughes, B. D.; Newgreen, D. F., Looking inside an invasion wave of cells using continuum models: Proliferation is the key, J Theor Biol, 243, 343-360 (2006) · Zbl 1447.92062
[40] Stichel, D.; Middleton, A. M.; Müller, B. F.; Depner, S.; Klingmüller, U.; Breuhahn, K.; Matthäus, F., An individual-based model for collective cancer cell migration explains speed dynamics and phenotype variability in response to growth factors, NPJ Syst Biol Appl, 3, 5 (2017)
[41] Tanaka, M. M.; Francis, A. R.; Luciani, F.; Sisson, S. A., Using approximate bayesian computation to estimate tuberculosis transmission parameters from genotype data, Genetics, 173, 1511-1520 (2006)
[42] Tang, L.; de; Guo, D.; Andasari, V.; Cristini, V.; Li, K. C.; Zhou, X., Computational modeling of 3d tumor growth and angiogenesis for chemotherapy evaluation, PLoS One, 9, e83962 (2014)
[43] Treloar, K. K.; Simpson, M. J.; Haridas, P.; Manton, K. J.; Leavesley, D. I.; McElwain, D. L.S.; Baker, R. E., Multiple types of data are required to identify the mechanisms influencing the spatial expansion of melanoma cell colonies, BMC Syst Biol, 7, 137 (2013)
[44] Tremel, A.; Cai, A.; Tirtaatmadja, N.; Hughes, B. D.; Stevens, G. W.; Landman, K. A.; O’Connor, A. J., Cell migration and proliferation during monolayer formation and wound healing, Chem Eng Sci, 64, 247-253 (2009)
[45] Warne, D. J.; Baker, R. E.; Simpson, M. J., Optimal quantification of contact inhibition in cell populations (2017), In press Biophysical Journal
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