Collective gradient sensing and chemotaxis: modeling and recent developments

Camley, Brian A.

doi:10.1088/1361-648x/aabd9f

Cited by 55 publications

(56 citation statements)

References 144 publications

(348 reference statements)

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“…We adopted the Cellular Potts Model to model cells because it allowed for a straightforward implementation of the evolvable receptor-ligand system. Several other models of cell clusters and collective chemotaxis have been proposed ([30, 32]), in some cases displaying chemotaxis in qualitatively different ways (for instance without sensing the chemokine gradient, only its concentration [47]). We hypothesise that the evolutionary mechanism described here are independent of the particular cell model choice, and thus would also work with other models discussed in [30], provided that cells were able to polarise or move also in the absence of other cells.…”

Section: Discussionmentioning

confidence: 99%

“…With this model setup, we consider collective cell movement as an emergent driver of multicellularity. Collective movement is important in simpler multicellular organisms [21–23] as well as in many processes within complex multicellular organisms, such as embryogenesis, tissue repair and cancer [24, 25], and has been modelled extensively [26–32]. In our model, cells perform chemotaxis towards the source of a noisy, shallow chemokine gradient.…”

Section: Introductionmentioning

confidence: 99%

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Evolution of multicellularity by collective integration of spatial information

Colizzi

Vroomans

Merks

2020

Preprint

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10At the origin of multicellularity, cells may have evolved aggregation in 11 response to predation, for functional specialisation or to allow large-scale 12 integration of environmental cues. These group-level properties emerged 13 from the interactions between cells in a group, and determined the selection 14 pressures experienced by these cells. 15 We investigate the evolution of multicellularity with an evolutionary 16 model where cells search for resources by chemotaxis in a shallow, noisy 17 gradient. Cells can evolve their adhesion to others in a periodically chang-18 ing environment, where a cell's fitness solely depends on its distance from 19 the gradient source. 20 We show that multicellular aggregates evolve because they perform chemo-21 taxis more efficiently than single cells. Only when the environment changes 22 too frequently, a unicellular state evolves which relies on cell dispersal. Both 23 strategies prevent the invasion of the other through interference competition, 24 creating evolutionary bi-stability. Therefore, collective behaviour can be an 25 emergent selective driver for undifferentiated multicellularity. 26 1 1 Introduction 27The evolution of multicellularity is a major transition in individuality, from au-28 tonomously replicating cells to groups of interdependent cells forming a higher-29 level of organisation [1, 2]. It has evolved independently several times across the 30 tree of life [3, 4]. Comparative genomics suggests [5], and experimental evolution 31 confirms [6, 7] that the increase of cell-cell adhesion drives the early evolution 32 of (undifferentiated) multicellularity. Increased cell adhesion may be temporally 33 limited and/or may be triggered by environmental changes (e.g. in Dictyostelids 34 and Myxobacteria [8, 9]). Moreover, multicellular organisation may come about 35 either by aggregation of genetically distinct cells or by incomplete separation after 36 cell division [8, 10]. 37The genetic toolkit and the cellular components that allow for multicellularity 38 -including adhesion proteins -pre-date multicellular species and are found in 39 their unicellular relatives [8,[11][12][13]. Aggregates of cells can organise themselves 40 by exploiting these old components in the new multicellular context, allowing 41 them to perform novel functions (or to perform old functions in novel ways) that 42 may confer some competitive advantage over single cells. Greater complexity can 43 later evolve by coordinating the division of tasks between different cell lineages 44 of the same organism (e.g. in the soma-germline division of labour), giving rise 45 to embryonic development. Nevertheless, the properties of early multicellular 46 organisms are defined by self-organised aggregate cell dynamics, and the space of 47 possible multicellular outcomes and emergent functions resulting from such self-48 organisation seems large -even with limited differential adhesion and signalling 49 between cells. However, the evolution of emergent functions as a consequence of 50 ad...

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Evolution of multicellularity by collective integration of spatial information

Colizzi

Vroomans

Merks

2020

Preprint

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“…Some studies reported faster migration of greater-size groups [9], others -that the group's speed is largely independent of its size [46], yet others -that single cells move faster than groups [26]. Theoretical models can explain, as the experimental measurements indicate, that both increase and decrease of group's velocity with its size are possible [45,47]. In this study, we found that single cells moved faster than the groups, and the groups' speed decreased with their size (Fig.…”

Section: Ef Guides Both Individual Cells and Groups Of Cells To The Cmentioning

confidence: 99%

“…Integration of individual cells into cohesive groups can lead to the groups higher sensitivity to directional signals than single cells [47]. For example, it was reported in [17] that isolated cells did not detect a weak EF, but cell groups did.…”

Section: Ef Guides Both Individual Cells and Groups Of Cells To The Cmentioning

confidence: 99%

“…Indeed, in this case, all cells of a PI3K-inhibited group would be polarized to the anode, and so the whole group would move to the anode, contrary to the data. To explain these results, it is informative to consider two simple conceptual models of collective directional cell motility [47]. Two more models are considered and argued against in the Discussion; the list of models we consider is by no means complete.…”

Section: Possible Explanations Of Collective Galvanotactic Directionamentioning

confidence: 99%

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PI3K inhibition reverses migratory direction of single cells but not cell groups in electric field

Sun

Yue

Copos³

et al. 2020

Preprint

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Motile cells migrate directionally in the electric field in a process known as galvanotaxis. Galvanotaxis is important in wound healing, development, cell division, and nerve growth. Different cell types migrate in opposite directions in electric fields, to either cathode, or anode, and the same cell can switch the directionality depending on chemical conditions. We previously reported that individual fish keratocyte cells sense electric fields and migrate to the cathode, while inhibition of PI3K reverses single cells to the anode. Many physiological processes rely on collective, not individual, cell migration, so here we report on directional migration of cohesive cell groups in electric fields. Uninhibited cell groups of any size move to the cathode, with speed decreasing and directionality increasing with the group size. Surprisingly, large groups of PI3K-inhibited cells move to the cathode, in the direction opposite to that of individual cells, which move to the anode, while such small groups are not persistently directional. In the large groups, cells’ velocities are distributed unevenly: the fastest cells are at the front of the uninhibited groups, but at the middle and rear of the PI3K-inhibited groups. Our results are most consistent with the hypothesis, supported by the computational model, that cells inside and at the edge of the groups interpret directional signals differently. Namely, cells in the group interior are directed to the cathode independently of their chemical state. Meanwhile, edge cells behave like the individual cells: they are directed to the cathode/anode in uninhibited/PI3K-inhibited groups, respectively. As a result, all cells drive uninhibited groups to the cathode, but a mechanical tug-of-war between the inner and edge cells directs large PI3K-inhibited groups with cell majority in the interior to the cathode, while rendering small groups non-directional.Significance statementMotile cells migrate directionally in electric fields. This behavior – galvanotaxis – is important in many physiological phenomena. Individual fish keratocytes migrate to the cathode, while inhibition of PI3K reverses single cells to the anode. Uninhibited cell groups move to the cathode. Surprisingly, large groups of PI3K-inhibited cells also move to the cathode, in the direction opposite to that of individual cells. The fastest cells are at the front of the uninhibited groups, but at the middle and rear of the PI3K-inhibited groups. We posit that inner and edge cells interpret directional signals differently, and that a tug-of-war between the edge and inner cells directs the cell groups. These results shed light on general principles of collective cell migration.

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