Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells

Abstract

SUMMARYAt the protochordate-vertebrate transition, a new predatory lifestyle and increased body size coincided with the appearance of a true head. Characteristic innovations of this head are a skull protecting and accommodating a centralized nervous system, a jaw for prey capture and gills as respiratory organs. The neural crest (NC) is a major ontogenetic source for the 'new head' of vertebrates and its contribution to the cranial skeleton has been intensively studied in different model organisms. However, the role of NC in the expansion of the respiratory surface of the gills has been neglected. Here, we use genetic lineage labeling to address the contribution of NC to specific head structures, in particular to the gills of adult zebrafish. We generated a sox10:ER T2 -Cre line and labeled NC cells by inducing Cre/loxP recombination with tamoxifen at embryonic stages. In juvenile and adult fish, we identified numerous established NC derivatives and, in the cranium, we precisely defined the crest/mesoderm interface of the skull roof. We show the NC origin of the opercular bones and of multiple cell types contributing to the barbels, chemosensory organs located in the mouth region. In the gills, we observed labeled primary and secondary lamellae. Clonal analysis reveals that pillar cells, a craniate innovation that mechanically supports the filaments and forms gill-specific capillaries, have a NC origin. Our data point to a crucial role for the NC in enabling more efficient gas exchange, thus uncovering a novel, direct involvement of this embryonic tissue in the evolution of respiratory systems at the protochordate-vertebrate transition.

Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish

“…6A). Indeed, pdgfrb reporter larvae crossed with Tg(sox10:Cre) line exhibited mVenus fluorescence in the pdgfrb promoter-active neural crest-derived tissues, including iris, jaw and pharyngeal arch (Mongera et al, 2013;Rodrigues et al, 2012), suggesting that this lineage-tracing system works (Fig. 6B).…”

New Model Systems to Illuminate Thyroid Organogenesis. Part I: An Update on the Zebrafish Toolbox

“…Once integrated, Cre and Flp recombinases were shown to faithfully carry out excision, inversion or exchange of such DNA sequences [58,59,60]. To date, the Cre/ loxP system has been used in zebrafish predominantly for lineage-tracing experiments [61,62,63] and to control transgene expression in a tissue- and time-dependent manner [64]. One exciting recent development is the application of site-specific recombinase systems in conjunction with gene-trapping approaches.…”

Endogenous Natural Complement Inhibitor Regulates Cardiac Development

“…Neural crest cells are involved in the genesis of craniofacial cartilage structures, a subset of pigment cells, and cardiac development (35). Whole-mount ISH revealed notable expression of MAp44 in the midbrain and hindbrain, and we observed craniofacial abnormalities following MAp44 knockdown, as visualized by Alcian blue staining (Supplemental Fig.…”