Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells

Abstract

The enteric nervous system is formed by neural crest cells that migrate, proliferate, and differentiate into neurons and glia distributed in ganglia along the gastrointestinal tract. In the developing embryo some enteric crest cells cease their caudal movements, whereas others continue to migrate. Subsequently, the enteric neurons form a reticular network of ganglia interconnected by axonal projections. We studied the developing avian gut to characterize the pattern of migration of the crest cells, and the relationship between migration and differentiation. Crest cells at the leading edge of the migratory front appear as strands of cells; isolated individual crest cells are rarely seen. In the foregut and midgut, these strands are located immediately beneath the serosa. In contrast, crest cells entering the colon appear first in the deeper submucosal mesenchyme and later beneath the serosa. As the neural crest wavefront passes caudally, the crest cell cords become highly branched, forming a reticular lattice that presages the mature organization of the enteric nervous system. Neurons and glia first appear within the strands at the advancing wavefront. Later neurons are consistently located at the nodes where branches of the lattice intersect. In the most rostral foregut and in the colon, some neurons initially appear in close association with extrinsic nerve fibers from the vagus and Remak's nerve, respectively. We conclude that crest cells colonize the gut as chains of cells and that, within these chains, both neurons and glia appear close to the wavefront. Developmental Dynamics 226:91-98, 2003.

Normal and aberrant craniofacial myogenesis by grafted trunk somitic and segmental plate mesoderm

“…Indeed, many events classically described as involving embryonic cell migration are not accomplished by individual cell motility, but rather by continually elongating and remodeling cords of cells in which only the leading edge cells execute displacement behavior. This is equally true for neural crest cells (Conner et al, 2003;Kulesa and Fraser, 2000;Tosney et al, 1994) and some appendicular myoblasts (Jacob et al, 1979), and for some but not all angioblasts (Noden, 1990).…”

Netrin/DCC‐mediated attraction of vagal sensory axons to the fetal mouse gut

“…4K). These chains are characteristic of vagal crestderived cells migrating in the gut (Conner et al, 2003;Pomeranz et al, 1991;Young et al, 2004b). Crest-derived cells migrating in the bowel have previously been reported to be DCC immunoreactive (Jiang et al, 2003).…”

Targeted deletion of Hand2 in enteric neural precursor cells affects its functions in neurogenesis, neurotransmitter specification and gangliogenesis, causing functional aganglionosis

“…The neural adhesion molecule NCAM mediates some aspects of gangliogenesis in the ENS (Faure et al, 2007); NCAM is a direct Hand2 target (Holler et al, 2010) and its expression is significantly reduced when Hand2 is deleted in stem cell-derived neural precursor cells (M.J.H., unpublished result). It is well documented that some enteric neural crest cells migrate along leading axon-like processes (Young et al, 2002;Young, 2008;); some of these cells express pan neuronal markers (Conner et al, 2003;Barlow et al, 2008) and NOS ) and may provide a roadmap for the movement of specific subsets of cells. Since expression of NOS is essentially absent in the Hand2 mutant ENS, it is possible that the spatial and temporal pattern of migration is disrupted resulting in a disorganized scattered population of neural crest, neural precursor cells and neurons.…”