An interdisciplinary approach to investigate collective cell migration in neural crest

Giniūnaitė, Rasa; McLennan, Rebecca; McKinney, Mary Cathleen; Baker, Ruth E.; Kulesa, Paul M.; Maini, Philip K.

doi:10.1002/dvdy.124

Cited by 9 publications

(5 citation statements)

References 65 publications

(148 reference statements)

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“…Theoretical models can be a powerful tool to investigate and identify the cues that drive collective migration and rearrangement. For instance, modeling studies have been used to identify key cues that govern the collective behavior of neural crest cell migration (Giniūnaitė, Baker, et al, 2020; Giniūnaitė, McLennan, et al, 2020; Shellard & Mayor, 2020), cancer cell invasion (George et al, 2017; Stichel et al, 2017), bacterial swarming (Jeckel et al, 2019; Peruani et al, 2012) and collective animal behaviors (Giardina, 2008). We believe that theoretical modeling can be employed to bridge the gap between the microscopic and macroscopic scales and advance our understanding of how collective behaviors drive the emergence of macroscopic features such as vascular network morphology.…”

Section: Discussionmentioning

confidence: 99%

Computational modeling of angiogenesis: The importance of cell rearrangements during vascular growth

Stepanova,

Byrne,

Maini

et al. 2023

WIREs Mechanisms of Disease

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Angiogenesis is the process wherein endothelial cells (ECs) form sprouts that elongate from the pre‐existing vasculature to create new vascular networks. In addition to its essential role in normal development, angiogenesis plays a vital role in pathologies such as cancer, diabetes and atherosclerosis. Mathematical and computational modeling has contributed to unraveling its complexity. Many existing theoretical models of angiogenic sprouting are based on the “snail‐trail” hypothesis. This framework assumes that leading ECs positioned at sprout tips migrate toward low‐oxygen regions while other ECs in the sprout passively follow the leaders' trails and proliferate to maintain sprout integrity. However, experimental results indicate that, contrary to the snail‐trail assumption, ECs exchange positions within developing vessels, and the elongation of sprouts is primarily driven by directed migration of ECs. The functional role of cell rearrangements remains unclear. This review of the theoretical modeling of angiogenesis is the first to focus on the phenomenon of cell mixing during early sprouting. We start by describing the biological processes that occur during early angiogenesis, such as phenotype specification, cell rearrangements and cell interactions with the microenvironment. Next, we provide an overview of various theoretical approaches that have been employed to model angiogenesis, with particular emphasis on recent in silico models that account for the phenomenon of cell mixing. Finally, we discuss when cell mixing should be incorporated into theoretical models and what essential modeling components such models should include in order to investigate its functional role.This article is categorized under: Cardiovascular Diseases > Computational Models Cancer > Computational Models

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Section: Discussionmentioning

confidence: 99%

Computational modeling of angiogenesis: The importance of cell rearrangements during vascular growth

Stepanova,

Byrne,

Maini

et al. 2023

WIREs Mechanisms of Disease

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“…Neural crest migration offers a natural application within developmental biology, and more widely provides a paradigm system for studying cell invasion. One integrated experimentaltheoretical approach has focussed on chick cranial neural crest cell migration, suggesting a process in which cells follow a vascular endothelial growth factor (VEGF) attractant gradient selfgenerated through their uptake of VEGF [2]. An agent-based modelling approach suggested that distinct cell phenotypes (termed "leaders" and "followers") were required for successful migration, differing (amongst other factors) in their response to the gradient of VEGF [2].…”

Section: Discussion and Research Perspectivesmentioning

confidence: 99%

“…One integrated experimentaltheoretical approach has focussed on chick cranial neural crest cell migration, suggesting a process in which cells follow a vascular endothelial growth factor (VEGF) attractant gradient selfgenerated through their uptake of VEGF [2]. An agent-based modelling approach suggested that distinct cell phenotypes (termed "leaders" and "followers") were required for successful migration, differing (amongst other factors) in their response to the gradient of VEGF [2]. While these agent-based models have been extended to include a continuous spectrum of phenotypes [44],…”

Section: Discussion and Research Perspectivesmentioning

confidence: 99%

“…Critical to this phenomenon was the chemotactic behaviour of the bacteria, which by consuming the nutrient establishes an attractant gradient that persistently propels the population from nutrient-poor to nutrient-rich regions. In subsequent years, chemotaxis and other taxis-like motility behaviours have been implicated in a broad variety cell migration and invasion processes, including embryonic development [2,3] and cancer invasion [4,5].…”

Section: Introductionmentioning

confidence: 99%

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Trade-offs between chemotaxis and proliferation shape the phenotypic structuring of invading waves

Lorenzi,

Painter

2021

Preprint

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Chemotaxis-driven invasions have been proposed across a broad spectrum of biological processes, from cancer to ecology. The influential system of equations introduced by Keller and Segel has proven a popular choice in the modelling of such phenomena, but in its original form restricts to a homogeneous population. To account for the possibility of phenotypic heterogeneity, we extend to the case of a population continuously structured across space, time and phenotype, where the latter determines variation in chemotactic responsiveness, proliferation rate, and the level of chemical environment modulation. The extended model considered here comprises a nonlocal partial differential equation for the local phenotype distribution of cells which is coupled, through an integral term, with a differential equation for the concentration of an attractant, which is sensed and degraded by the cells. In the framework of this model, we concentrate on a chemotaxis/proliferation trade-off scenario, where the cell phenotypes span a spectrum of states from highly-chemotactic but minimally-proliferative to minimally-chemotactic but highlyproliferative. Using a combination of numerical simulation and formal asymptotic analysis, we explore the properties of travelling-wave solutions. The results of our study demonstrate how incorporating phenotypic heterogeneity may lead to a highly-structured wave profile, where cells in different phenotypic states dominate different spatial positions across the invading wave, and clarify how the phenotypic structuring of the wave can be shaped by trade-offs between chemotaxis and proliferation.

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“…We attribute the deviations of the dynamics and morphological outcomes of the multicellular masses from generic physical predictions to the contribution of agent-like behaviors, e.g., directed migration, regulated quiescence, oscillatory signal relay, of the cells themselves. Cells of clonally developing multicellular organisms can also exhibit agent-like behaviors [ 171 – 173 ]. While it is difficult to quantify the relative contributions that each class of phenomena makes to the respective developmental processes, we suggest that morphogenesis of Myxobacteria and Dictyostelia is more dependent on agent-like behaviors than that of animals or plants.…”

Section: Discussionmentioning

confidence: 99%

Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity

Angel

Nanjundiah

Benítez

et al. 2020

EvoDevo

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Myxobacteria and dictyostelids are prokaryotic and eukaryotic multicellular lineages, respectively, that after nutrient depletion aggregate and develop into structures called fruiting bodies. The developmental processes and resulting morphological outcomes resemble one another to a remarkable extent despite their independent origins, the evolutionary distance between them and the lack of traceable homology in molecular mechanisms. We hypothesize that the morphological parallelism between the two lineages arises as the consequence of the interplay within multicellular aggregates between generic processes, physical and physicochemical processes operating similarly in living and non-living matter at the mesoscale (~10–3–10–1 m) and agent-like behaviors, unique to living systems and characteristic of the constituent cells, considered as autonomous entities acting according to internal rules in a shared environment. Here, we analyze the contributions of generic and agent-like determinants in myxobacteria and dictyostelid development and their roles in the generation of their common traits. Consequent to aggregation, collective cell–cell contacts mediate the emergence of liquid-like properties, making nascent multicellular masses subject to novel patterning and morphogenetic processes. In both lineages, this leads to behaviors such as streaming, rippling, and rounding-up, as seen in non-living fluids. Later the aggregates solidify, leading them to exhibit additional generic properties and motifs. Computational models suggest that the morphological phenotypes of the multicellular masses deviate from the predictions of generic physics due to the contribution of agent-like behaviors of cells such as directed migration, quiescence, and oscillatory signal transduction mediated by responses to external cues. These employ signaling mechanisms that reflect the evolutionary histories of the respective organisms. We propose that the similar developmental trajectories of myxobacteria and dictyostelids are more due to shared generic physical processes in coordination with analogous agent-type behaviors than to convergent evolution under parallel selection regimes. Insights from the biology of these aggregative forms may enable a unified understanding of developmental evolution, including that of animals and plants.

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An interdisciplinary approach to investigate collective cell migration in neural crest

Cited by 9 publications

References 65 publications

Computational modeling of angiogenesis: The importance of cell rearrangements during vascular growth

Computational modeling of angiogenesis: The importance of cell rearrangements during vascular growth

Trade-offs between chemotaxis and proliferation shape the phenotypic structuring of invading waves

Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity

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