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.

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.

Mutations affecting development of the zebrafish inner ear and lateral line

Development ◽  
1996 ◽  
Vol 123 (1) ◽  
pp. 241-254 ◽  
Author(s):  
T.T. Whitfield ◽  
M. Granato ◽  
F.J. van Eeden ◽  
U. Schach ◽  
M. Brand ◽  
...  
Keyword(s):  
Inner Ear ◽  
Lateral Line ◽  
Large Scale ◽  
Sensory System ◽  
Semicircular Canals ◽  
Abnormal Development ◽  
Pigment Cells ◽  
Otic Vesicle ◽  
In The Wild ◽  
Complementation Groups

Mutations giving rise to anatomical defects in the inner ear have been isolated in a large scale screen for mutations causing visible abnormalities in the zebrafish embryo (Haffter, P., Granato, M., Brand, M. et al. (1996) Development 123, 1–36). 58 mutants have been classified as having a primary ear phenotype; these fall into several phenotypic classes, affecting presence or size of the otoliths, size and shape of the otic vesicle and formation of the semicircular canals, and define at least 20 complementation groups. Mutations in seven genes cause loss of one or both otoliths, but do not appear to affect development of other structures within the ear. Mutations in seven genes affect morphology and patterning of the inner ear epithelium, including formation of the semicircular canals and, in some, development of sensory patches (maculae and cristae). Within this class, dog-eared mutants show abnormal development of semicircular canals and lack cristae within the ear, while in van gogh, semicircular canals fail to form altogether, resulting in a tiny otic vesicle containing a single sensory patch. Both these mutants show defects in the expression of homeobox genes within the otic vesicle. In a further class of mutants, ear size is affected while patterning appears to be relatively normal; mutations in three genes cause expansion of the otic vesicle, while in little ears and microtic, the ear is abnormally small, but still contains all five sensory patches, as in the wild type. Many of the ear and otolith mutants show an expected behavioural phenotype: embryos fail to balance correctly, and may swim on their sides, upside down, or in circles. Several mutants with similar balance defects have also been isolated that have no obvious structural ear defect, but that may include mutants with vestibular dysfunction of the inner ear (Granato, M., van Eeden, F. J. M., Schach, U. et al. (1996) Development, 123, 399–413,). Mutations in 19 genes causing primary defects in other structures also show an ear defect. In particular, ear phenotypes are often found in conjunction with defects of neural crest derivatives (pigment cells and/or cartilaginous elements of the jaw). At least one mutant, dog-eared, shows defects in both the ear and another placodally derived sensory system, the lateral line, while hypersensitive mutants have additional trunk lateral line organs.

The zebrafish homologs of SET/I2PP2A oncoprotein: expression patterns and insights into their physiological roles during development

2016 ◽  
Vol 473 (24) ◽  
pp. 4609-4627 ◽  
Author(s):  
Iliana Serifi ◽  
Eleni Tzima ◽  
Katerina Soupsana ◽  
Zoe Karetsou ◽  
Dimitris Beis ◽  
...  
Keyword(s):  
Amino Acids ◽  
Lateral Line ◽  
Gene Networks ◽  
Expression Patterns ◽  
Otic Vesicle ◽  
Lateral Line System ◽  
Loss Of Function ◽  
Line System ◽  
Eye Retina

The oncoprotein SET/I2PP2A (protein phosphatase 2A inhibitor 2) participates in various cellular mechanisms such as transcription, cell cycle regulation and cell migration. SET is also an inhibitor of the serine/threonine phosphatase PP2A, which is involved in the regulation of cell homeostasis. In zebrafish, there are two paralogous set genes that encode Seta (269 amino acids) and Setb (275 amino acids) proteins which share 94% identity. We show here that seta and setb are similarly expressed in the eye, the otic vesicle, the brain and the lateral line system, as indicated by in situ hybridization labeling. Whole-mount immunofluorescence analysis revealed the expression of Seta/b proteins in the eye retina, the olfactory pit and the lateral line neuromasts. Loss-of-function studies using antisense morpholino oligonucleotides targeting both seta and setb genes (MOab) resulted in increased apoptosis, reduced cell proliferation and morphological defects. The morphant phenotypes were partially rescued when MOab was co-injected with human SET mRNA. Knockdown of setb with a transcription-blocking morpholino oligonucleotide (MOb) resulted in phenotypic defects comparable with those induced by setb gRNA (guide RNA)/Cas9 [CRISPR (clustered regularly interspaced short palindromic repeats)-associated 9] injections. In vivo labeling of hair cells showed a significantly decreased number of neuromasts in MOab-, MOb- and gRNA/Cas9-injected embryos. Microarray analysis of MOab morphant transcriptome revealed differential expression in gene networks controlling transcription in the sensory organs, including the eye retina, the ear and the lateral line. Collectively, our results suggest that seta and setb are required during embryogenesis and play roles in the zebrafish sensory system development.

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 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'.

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