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Learning dynamical models of single and collective cell migration: a review

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Abstract

Single and collective cell migration are fundamental processes critical for physiological phenomena ranging from embryonic development and immune response to wound healing and cancer metastasis. To understand cell migration from a physical perspective, a broad variety of models for the underlying physical mechanisms that govern cell motility have been developed. A key challenge in the development of such models is how to connect them to experimental observations, which often exhibit complex stochastic behaviours. In this review, we discuss recent advances in data-driven theoretical approaches that directly connect with experimental data to infer dynamical models of stochastic cell migration. Leveraging advances in nanofabrication, image analysis, and tracking technology, experimental studies now provide unprecedented large datasets on cellular dynamics. In parallel, theoretical efforts have been directed towards integrating such datasets into physical models from the single cell to the tissue scale with the aim of conceptualising the emergent behaviour of cells. We first review how this inference problem has been addressed in both freely migrating and confined cells. Next, we discuss why these dynamics typically take the form of underdamped stochastic equations of motion, and how such equations can be inferred from data. We then review applications of data-driven inference and machine learning approaches to heterogeneity in cell behaviour, subcellular degrees of freedom, and to the collective dynamics of multicellular systems. Across these applications, we emphasise how data-driven methods can be integrated with physical active matter models of migrating cells, and help reveal how underlying molecular mechanisms control cell behaviour. Together, these data-driven approaches are a promising avenue for building physical models of cell migration directly from experimental data, and for providing conceptual links between different length-scales of description.

Original languageEnglish
Article number056601
Pages (from-to)1-39
Number of pages39
JournalReports on Progress in Physics
Volume87
Issue number5
Early online date4 Apr 2024
DOIs
Publication statusPublished - May 2024

Bibliographical note

Publisher Copyright:
© 2024 The Author(s). Published by IOP Publishing Ltd.

Funding

This work was supported by the Deutsche Forschungsgemeinschaft (German Research Foundation)\u2014Project-ID 201269156\u2014SFB 1032 (Project B12). D B B was supported by an NOMIS Fellowship and an EMBO Fellowship (ALTF 343-2022). We thank Joachim R\u00E4dler, Alexandra Fink, Erwin Frey, Pierre Ronceray, Ricard Alert, Edouard Hannezo, Henrik Flyvbjerg, Ulrich Schwarz, Joshua Shaevitz, Greg Stephens, Andrea Cavagna, Grzegorz Gradziuk, Fridtjof Brauns, Nikolas Claussen, Tom Brandst\u00E4tter, Johannes Flommersfeld, Christoph Schreiber, Nicolas Arlt, Matthew Schmitt, Joris Messelink, Federico Gnesotto, Federica Mura, Bram Hoogland, Manon Wigbers, Isabella Graf, Jessica Lober, and many others for inspiring discussions. We also thank Claudia Flandoli for the artwork in figures , , and .

FundersFunder number
Deutsche Forschungsgemeinschaft201269156—SFB 1032
European Molecular Biology OrganizationALTF 343-2022

    Keywords

    • active matter
    • cell migration
    • collective phenomena
    • data-driven models
    • inference
    • machine learning
    • stochastic dynamics

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