scholarly journals Relationship between surrounding tissue morphology and directional collective migration of the posterior lateral line primordium in zebrafish

2020 ◽  
Vol 25 (8) ◽  
pp. 582-592
Author(s):  
Akari Karaiwa ◽  
Sohei Yamada ◽  
Hodaka Yamamoto ◽  
Mizuho Wakasa ◽  
Hannosuke Ishijima ◽  
...  
Keyword(s):  
Lateral Line ◽  
Surrounding Tissue ◽  
Collective Migration ◽  
Tissue Morphology ◽  
Posterior Lateral Line

scholarly journals Zebrafish Posterior Lateral Line primordium migration requires interactions between a superficial sheath of motile cells and the skin

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Damian E Dalle Nogare ◽  
Naveen Natesh ◽  
Harshad D Vishwasrao ◽  
Hari Shroff ◽  
Ajay B Chitnis
Keyword(s):  
Lateral Line ◽  
Fgf Signaling ◽  
Collective Migration ◽  
Directed Migration ◽  
Posterior Lateral Line ◽  
Motile Cells ◽  
And Migration

The Zebrafish Posterior Lateral Line primordium migrates in a channel between the skin and somites. Its migration depends on the coordinated movement of its mesenchymal-like leading cells and trailing cells, which form epithelial rosettes, or protoneuromasts. We describe a superficial population of flat primordium cells that wrap around deeper epithelialized cells and extend polarized lamellipodia to migrate apposed to the overlying skin. Polarization of lamellipodia extended by both superficial and deeper protoneuromast-forming cells depends on Fgf signaling. Removal of the overlying skin has similar effects on superficial and deep cells: lamellipodia are lost, blebs appear instead, and collective migration fails. When skinned embryos are embedded in Matrigel, basal and superficial lamellipodia are recovered; however, only the directionality of basal protrusions is recovered, and migration is not rescued. These observations support a key role played by superficial primordium cells and the skin in directed migration of the Posterior Lateral Line primordium.

scholarly journals Collective migration and patterning during early development of zebrafish posterior lateral line

2020 ◽  
Vol 375 (1807) ◽  
pp. 20190385 ◽  
Author(s):  
Annachiara Colombi ◽  
Marco Scianna ◽  
Luigi Preziosi
Keyword(s):  
Lateral Line ◽  
Mathematical Community ◽  
Cellular Level ◽  
Collective Migration ◽  
Chemical Sensitivity ◽  
Multi Scale ◽  
Posterior Lateral Line ◽  
Discrete Approach ◽  
Continuous Description ◽  
Parameter Values

The morphogenesis of zebrafish posterior lateral line (PLL) is a good predictive model largely used in biology to study cell coordinated reorganization and collective migration regulating pathologies and human embryonic processes. PLL development involves the formation of a placode formed by epithelial cells with mesenchymal characteristics which migrates within the animal myoseptum while cyclically assembling and depositing rosette-like clusters (progenitors of neuromast structures). The overall process mainly relies on the activity of specific diffusive chemicals, which trigger collective directional migration and patterning. Cell proliferation and cascade of phenotypic transitions play a fundamental role as well. The investigation on the mechanisms regulating such a complex morphogenesis has become a research topic, in the last decades, also for the mathematical community. In this respect, we present a multiscale hybrid model integrating a discrete approach for the cellular level and a continuous description for the molecular scale. The resulting numerical simulations are then able to reproduce both the evolution of wild-type (i.e. normal) embryos and the pathological behaviour resulting form experimental manipulations involving laser ablation. A qualitative analysis of the dependence of these model outcomes from cell-cell mutual interactions, cell chemical sensitivity and internalization rates is included. The aim is first to validate the model, as well as the estimated parameter values, and then to predict what happens in situations not tested yet experimentally. This article is part of the theme issue ‘Multi-scale analysis and modelling of collective migration in biological systems'.

scholarly journals Leading and trailing cells cooperate in collective migration of the zebrafish posterior lateral line primordium

Development ◽  
2014 ◽  
Vol 141 (16) ◽  
pp. 3188-3196 ◽  
Author(s):  
D. Dalle Nogare ◽  
K. Somers ◽  
S. Rao ◽  
M. Matsuda ◽  
M. Reichman-Fried ◽  
...  
Keyword(s):  
Lateral Line ◽  
Collective Migration ◽  
Posterior Lateral Line

scholarly journals Eya1-dependent homeostasis of morphogenetic territories during collective cell migration

2021 ◽  
Author(s):  
Jerónimo R. Miranda-Rodríguez ◽  
Augusto Borges ◽  
Filipe Pinto-Teixeira ◽  
Indra Wibowo ◽  
Hans-Martin Pogoda ◽  
...  
Keyword(s):  
Cell Migration ◽  
Lateral Line ◽  
Chemokine Receptor ◽  
Collective Cell Migration ◽  
Intercellular Signaling ◽  
Collective Migration ◽  
Posterior Lateral Line ◽  
The Stability ◽  
Signaling Domains ◽  
Fgfr1 Expression

SUMMARYTissue remodeling presents an enormous challenge to the stability of intercellular signaling domains. Here we investigate this issue during the development of the posterior lateral line in zebrafish. We find that the transcriptional co-activator and phosphatase Eya1, mutated in the branchio-oto-renal syndrome in humans, is essential for the homeostasis of the Wnt/β-catenin and FGF morphogenetic domains during the collective migration of lateral-line primordial cells. Loss of Eya1 strongly diminishes the expression of Dkk1, expanding Wnt/β-catenin activity in the primordium, which in turn abrogates FGFR1 expression. Deficits in Eya1 also abolishes the expression of the chemokine receptor CXCR7b, disrupting primordium migration. These results reinforce the concept that morphogenetic domains in dynamically remodeling tissues are formed by cellular states maintained by continuous signaling.

scholarly journals A sheath of motile cells supports collective migration in of the Zebrafish posterior lateral line primordium under the skin

2019 ◽  
Author(s):  
Damian Dalle Nogare ◽  
Naveen Natesh ◽  
Ajay Chitnis
Keyword(s):  
Epithelial Cells ◽  
Lateral Line ◽  
Sensory System ◽  
Otic Vesicle ◽  
Confined Space ◽  
Collective Migration ◽  
Posterior Lateral Line ◽  
Motile Cells ◽  
Sheath Cells

AbstractDuring embryonic development, cells must navigate through diverse three-dimensional environments robustly and reproducibly. The zebrafish posterior lateral line primordium (PLLp), a group of approximately 120 cells which migrates from the otic vesicle to the tip of the tail, spearheading the development of the lateral line sensory system, is an excellent model to study such collective migration in an in vivo context. This system migrates in a channel formed by the underlying horizontal myoseptum and somites, and the overlying skin. While cells in the leading part of the PLLp are flat and have a more mesenchymal morphology, cells in the trailing part progressively reorganize to form epithelial rosettes, called protoneuromasts. These epithelial cells extend basal cryptic lamellipodia in the direction of migration in response to both chemokine and FGF signals. In this study, we show that, in addition to these cryptic lamellipodia, the core epithelial cells are in fact surrounded by a population of motile cells which extend actin-rich migratory processes apposed to the overlying skin. These thin cells wrap around the protoneuromasts, forming a continuous sheath of cells around the apical and lateral surface of the PLLp. The processes extended by these cells are highly polarized in the direction of migration and this directionality, like that of the basal lamellipodia, is dependent on FGF signaling. Consistent with interactions of sheath cells with the overlying skin contributing to migration, removal of the skin stalls migration. However, this is accompanied by some surprising changes. There is a profound change in the morphology of the sheath cells, with directional superficial lamellipodia being replaced with the appearance of undirected blebs or ruffles. Furthermore, removal of the skin not only affects underlying lamellipodia, it simultaneously alters the morphology and behavior of the deeper basal cryptic lamellipodia, even though these cells do not directly contact the skin. Directional actin-rich protrusions on both the apical and basal surface and migration are completely and simultaneously restored upon regrowth of the skin over the PLLp. We suggest that this system utilizes a circumferential sheath of motile cells to allow the internal epithelial cells to migrate collectively in the confined space of the horizontal myopseptum and that elastic confinement provided by the overlying skin is essential for effective collective migratory behavior of primordium cells.

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