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Biology subjects

Prince, V. E.

Publications and source records attributed to Prince, V. E..

2 recordsLinked to original sources

Development of the zebrafish anterior lateral line system is influenced by underlying cranial neural crest

The mechanosensory lateral line system of aquatic vertebrates comprises a superficial network of distributed sensory organs, the neuromasts, which are arranged over the head and trunk and innervated by lateral line nerves to allow detection of changes in water flow and pressure. While the well-studied zebrafish posterior lateral line has emerged as a powerful model to study collective cell migration, far less is known about development of the anterior lateral line, which produces the supraorbital and infraorbital lines around the eye, as well as mandibular and opercular lines over the jaw and cheek. Here we show that normal development of the zebrafish anterior lateral line system from cranial placodes is dependent on another vertebrate-specific cell type, the cranial neural crest. We find that cranial neural crest and anterior lateral lines develop in close proximity, with absence of neural crest cells leading to major disruptions in the overlying anterior lateral line system. Specifically, in the absence of neural crest neither supraorbital nor infraorbital lateral lines fully extend, such that the most anterior cranial regions remain devoid of neuromasts, while supernumerary ectopic neuromasts form in the posterior supraorbital region. Both neural crest and cranial placodes contribute neurons to the lateral line ganglia that innervate the neuromasts and in the absence of neural crest these ganglia, as well as the lateral line afferent nerves, are disrupted. Finally, we establish that as ontogeny proceeds, the most anterior supraorbital neuromasts come to lie within neural crest-derived frontal and nasal bones in the developing cranium. These are the same anterior supraorbital neuromasts that are absent or mislocated in specimens lacking neural crest cells. Together, our results establish that cranial neural crest and cranial placode derivatives function in concert over the course of ontogeny to build the complex cranial lateral line system. HighlightsO_LIThe anterior lateral line and cranial neural crest develop in close proximity C_LIO_LIAbsence of neural crest disrupts anterior lateral line development C_LIO_LIAbsence of neural crest disrupts lateral line ganglion morphology and innervation C_LIO_LIEarly interactions of neural crest and placodes prefigure later anatomical interactions C_LI O_FIG O_LINKSMALLFIG WIDTH=196 HEIGHT=200 SRC="FIGDIR/small/637483v1_ufig1.gif" ALT="Figure 1"> View larger version (42K): org.highwire.dtl.DTLVardef@ce9c43org.highwire.dtl.DTLVardef@7511e5org.highwire.dtl.DTLVardef@1e9e208org.highwire.dtl.DTLVardef@1f6af7d_HPS_FORMAT_FIGEXP M_FIG C_FIG

developmental biology↗

Notch controls the cell cycle to define leader versus follower identities during collective cell migration.

Coordination of cell proliferation and migration is fundamental for life, and its dysregulation has catastrophic consequences, as cancer. How cell cycle progression affects migration, and vice-versa, remains largely unknown. We address these questions by combining in silico modelling and in vivo experimentation in the zebrafish Trunk Neural Crest (TNC). TNC migrate collectively, forming chains with a leader cell directing the movement of trailing followers. We show that the acquisition of migratory identity is autonomously controlled by Notch signalling in TNC. High Notch activity defines leaders, while low Notch determines followers. Moreover, cell cycle progression is required for TNC migration and is regulated by Notch. Cells with low Notch activity stay longer in G1 and become followers, while leaders with high Notch activity quickly undergo G1/S transition and remain in S-phase longer. We propose that migratory behaviours are defined through the interaction of Notch signalling and cell cycle progression.

developmental biology↗