Gene regulatory interactions underlying neural crest development and evolution

16 June 2017

Marianne Bronner
Division of Biology, Caltech

Abstract

Evolution of vertebrates is intimately linked to the advent of the neural crest, a migratory and multipotent cell population that gives rise to many defining vertebrate characteristics, including a well-defined head and peripheral ganglia. However, not all neural crest cell are alike, with different neural crest populations existing along the body axis; for example, only cranial neural crest cells give rise to cartilage and bone of the face, and only vagal neural crest cells contribute to the enteric nervous system. To identify gene regulatory networks (GRNs) that confer axial level specific identify, we have transcriptionally profiled different neural crest subpopulations in both jawed and jawless vertebrates. By characterizing the function of transcriptional and signaling components in these neural crest GRNs, we aim to understand the steps that define the neural crest from the time of induction at the neural plate border to their differentiation into diverse cell types in several vertebrate groups.

One important and early-branching group of vertebrates, the jawless fish have bona fide neural crest cells, but lack the full complement of neural crest derivatives, including jaws and sympathetic ganglia. To explore the origin of new vertebrate cell types, we have focused on cell lineage contributions to the lamprey enteric nervous system (ENS). Surprisingly, our data suggest that lampreys may be missing a discrete "vagal" neural crest population akin to those forming the ENS of jawed vertebrates. Rather, we find that late-migrating cells, originating from trunk neural tube and closely associated with nerve fibers, can differentiate into serotonergic neurons within the gut wall. These trunk neural crest cells appear to be homologous to Schwann cell precursors of mammals, recently shown to populate post-embryonic parasympathetic including enteric ganglia of the colon. Thus, we propose that ENS ganglia may represent a novel neural crest-derived cell type that arose in the vertebrate lineage with the advent of jawed vertebrates.

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