Neural crest cell communication involves an exchange of cytoplasmic material through cellular bridges revealed by photoconversion of KikGR

Abstract

Neural crest (NC) cells invade the vertebrate embryo in ordered migratory streams, yet it is unclear whether cells communicate to maintain spacing and direction. Here, we examined NC cell communication in detail, using optical highlighting and photobleaching to monitor cell contact dynamics. We observed cytoplasmic transfer between NC cell neighbors through thin cellular bridges. The transfer of molecules between NC cells was bi-directional, not at equal rates, and independent of bridge dynamics. The cytoplasmic transfer was prevalent in recently divided NC cells. Molecular simulations, based on Brownian motion and measured cell volumes, predicted that simple diffusion could not account for observed cytoplasmic transfer rates. Cell tracking revealed that exchange of cytoplasmic material preceded the re-orientation of cells to the direction of migration. Our data suggest a mechanism by which NC cells communicate position information through the formation of cellular bridges that allow exchange of cytoplasmic material through active transport.

Tunneling nanotubes

“…The development of fluorescent protein tags and advanced confocal microscopy have facilitated TNT identification in vivo by enabling the labeling of specific proteins only present in a certain subpopulation of cells. In chick embryos, TNT-like structures were successfully identified between neural crest cells after this specific cell population had been labeled with fluorescent fusion proteins 28 , 29 . There are similar findings from gastrulation-stage embryos, 30 and in immune cells in the adult mouse cornea 31 , 32 .…”

Inter-Cellular Exchange of Cellular Components via VE-Cadherin-Dependent Trans-Endocytosis

“…Tunneling of nano-tube like structures in immune cells [53], [54] and epithelial cells [55], the cellular bridge in neural crest cells [56], and direct cell-cell contact dependent intercellular transfer of cellular components are other reported examples of similar in trans cellular communication [57]. However, none of these have identified the mechanism responsible for the observed effects.…”

Emerging physiological and pathological implications of tunneling nanotubes formation between cells

“…So far, TNTs have been observed in vivo between myeloid cells in mouse cornea (Chinnery et al, 2008;Seyed-Razavi et al, 2013), between neural crest in chicken embryo (McKinney et al, 2011;Teddy and Kulesa, 2004), and between human mesothelioma cells (Lou et al, 2012b). Moreover, there are many different types of cells (Table 1) which are able to communicate in vitro using TNTs, and their functions are impressive by these nanotubes (Austefjord et al, 2014;Wang et al, 2012b,c).…”