Organizing moving groups during morphogenesis

Lecaudey, Virginie; Gilmour, Darren

doi:10.1016/j.ceb.2005.12.001

Cited by 113 publications

(114 citation statements)

References 44 publications

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“…The movement of large number of cells stretching considerable distance, typical of migratory chains, calls for strong driving forces being at work. In addition, the presence of highly mobile cells at the leading edge suggests that a specialized population of cells guides the rest of the chain (for review, see Lecaudey and Gilmour, 2006). The difficulty of manipulating individual glial cells and nervous tissue complexity, however, make it hard to test this hypothesis at the single cell level.…”

Section: Introductionmentioning

confidence: 99%

Glial Chain Migration Requires Pioneer Cells

Aigouy¹,

Lepelletier²,

Giangrande³

2008

J. Neurosci.

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The migration of glial chains along the nerve entails directional and coordinated movement. Despite its importance in the formation of the nervous system, this process remains poorly understood, because of the difficulty of manipulating identified cells. Using confocal time-lapse and cell ablation in the whole animal, we provide direct evidence for a discrete number of Drosophila peripheral glial cells acting as pioneers and guiding the rest of the migratory chain. These cells are in direct contact with several follower cells through a very long and stable cytoplasmic extension. The presence of pioneer cells and homotypic interactions at the tip of the chain allows coordinated movement and the formation of a continuous sheath around the nerve. These in vivo data open novel perspectives for understanding the cellular bases of vertebrate glial migration in physiological and pathological conditions.

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Section: Introductionmentioning

confidence: 99%

Glial Chain Migration Requires Pioneer Cells

Aigouy¹,

Lepelletier²,

Giangrande³

2008

J. Neurosci.

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“…active matter | cell mechanics | jamming | collective cell dynamics | nonequilibrium T he collective motion of cells within a tissue is a fundamental biological process, both in health and in disease; for example it is essential to embryonic morphogenesis, organ regeneration, and wound repair (1)(2)(3)(4). However, while the motion of individual cells is well understood, collective motion of a large number of cells such as in tissues is only understood in specific instances.…”

mentioning

confidence: 99%

Glass-like dynamics of collective cell migration

Angelini

Hannezo

Trepat

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

685

715

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Collective cell migration in tissues occurs throughout embryonic development, during wound healing, and in cancerous tumor invasion, yet most detailed knowledge of cell migration comes from single-cell studies. As single cells migrate, the shape of the cell body fluctuates dramatically through cyclic processes of extension, adhesion, and retraction, accompanied by erratic changes in migration direction. Within confluent cell layers, such subcellular motions must be coupled between neighbors, yet the influence of these subcellular motions on collective migration is not known. Here we study motion within a confluent epithelial cell sheet, simultaneously measuring collective migration and subcellular motions, covering a broad range of length scales, time scales, and cell densities. At large length scales and time scales collective migration slows as cell density rises, yet the fastest cells move in large, multicell groups whose scale grows with increasing cell density. This behavior has an intriguing analogy to dynamic heterogeneities found in particulate systems as they become more crowded and approach a glass transition. In addition we find a diminishing self-diffusivity of short-wavelength motions within the cell layer, and growing peaks in the vibrational density of states associated with cooperative cell-shape fluctuations. Both of these observations are also intriguingly reminiscent of a glass transition. Thus, these results provide a broad and suggestive analogy between cell motion within a confluent layer and the dynamics of supercooled colloidal and molecular fluids approaching a glass transition.active matter | cell mechanics | jamming | collective cell dynamics | nonequilibrium T he collective motion of cells within a tissue is a fundamental biological process, both in health and in disease; for example it is essential to embryonic morphogenesis, organ regeneration, and wound repair (1-4). However, while the motion of individual cells is well understood, collective motion of a large number of cells such as in tissues is only understood in specific instances. Moreover, the transition of the motion of single cells to the collective motion of many cells has not been as extensively studied. This transition is well represented by single monolayers of cells; as they become confluent, the motion of the cells becomes increasingly collective, depending on the presence of their neighbors (5). During collective migration within confluent cell layers, cell sheets flow like a fluid yet remain fixed and solidlike at short time scales, with the motion of each cell constrained by the crowding due to its neighbors (5-7). This solid-like character over short times and collective flow over longer times is reminiscent of many crowded particulate systems, which undergo a transition from a supercooled fluid-like state to a glass-like state. By analogy, the collective motion of cells might be described by a similar transition: as cell density rises, neighboring cells restrict the motion of each cell, forcing cells to move in g...

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“…In addition to its aesthetic qualities, social cell migration is involved in embryonic development (7), wound healing (8), and immune response (9), and unregulated migration leads to disease, including cancer metastasis (10). Previous work on single-cell migration has focused on isolated (11)(12)(13)(14)(15)(16)(17)(18)(19)(20) or strongly polarized and aligning (21,22) cell types, mostly using population-averaged bulk assays (23) or simple observations in a social context (2,3).…”

mentioning

confidence: 99%

Migration of cells in a social context

Vedel

Tay

Johnston

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

103

104

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In multicellular organisms and complex ecosystems, cells migrate in a social context. Whereas this is essential for the basic processes of life, the influence of neighboring cells on the individual remains poorly understood. Previous work on isolated cells has observed a stereotypical migratory behavior characterized by short-time directional persistence with long-time random movement. We discovered a much richer dynamic in the social context, with significant variations in directionality, displacement, and speed, which are all modulated by local cell density. We developed a mathematical model based on the experimentally identified "cellular traffic rules" and basic physics that revealed that these emergent behaviors are caused by the interplay of single-cell properties and intercellular interactions, the latter being dominated by a pseudopod formation bias mediated by secreted chemicals and pseudopod collapse following collisions. The model demonstrates how aspects of complex biology can be explained by simple rules of physics and constitutes a rapid test bed for future studies of collective migration of individual cells.cell migration | single-cell analysis | physical modeling | microfluidics C ollective migration, from migrating cells in tissue (1-3) to swarming insects (4) to flocks of birds (5) and pedestrians in heavy traffic (6), constitutes one of the most fascinating spectacles in nature. In addition to its aesthetic qualities, social cell migration is involved in embryonic development (7), wound healing (8), and immune response (9), and unregulated migration leads to disease, including cancer metastasis (10). Previous work on single-cell migration has focused on isolated (11)(12)(13)(14)(15)(16)(17)(18)(19)(20) or strongly polarized and aligning (21, 22) cell types, mostly using population-averaged bulk assays (23) or simple observations in a social context (2, 3). However, strongly cross-correlated cell motion and collective substrate deformation has been found to arise in mechanically interlinked cells transmitting forces through both cell-cell linkages and the substrate (24-29). These studies revealed useful information on cell migration, but because in general the relevant interactions in a social context and their relative importance are not established, migratory behavior of cells in a social context remains as one of the major unresolved problems in biology (30). Furthermore, striking social effects such as highly sensitive collective responses in a number of sensing systems [e.g., quorum sensing (31, 32) and onset of collective behavior in Dictyostelium discoideum (33)] mediated by increased levels of cell-secreted signals in higher cell density indicate that mechanical links are not necessary for collective behavior. At the subcellular level, many types of nonswimming motile cells involved in multicellular biology [e.g., fibroblasts, Dictyostelium, and neutrophils (13,14,(16)(17)(18)] have been found to transmit traction force to the substrate by intracellularly polymerizing their cytoskeleton...

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Organizing moving groups during morphogenesis

Cited by 113 publications

References 44 publications

Glial Chain Migration Requires Pioneer Cells

Glial Chain Migration Requires Pioneer Cells

Glass-like dynamics of collective cell migration

Migration of cells in a social context

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