Abstract
Neurons and pancreatic endocrine cells have a common physiology and express a similar toolkit of transcription factors during development. To explain these common features, it has been hypothesized that pancreatic cells most likely co-opted a pre-existing gene regulatory program from ancestral neurons. To test this idea, we looked for neurons with a “pre-pancreatic” program in an early-branched deuterostome, the sea urchin. Only vertebrates have a proper pancreas, however, our lab previously found that cells with a pancreatic-like signature are localized within the sea urchin embryonic gut. We also found that the pancreatic transcription factors Xlox/Pdx1 and Brn1/2/4 co-localize in a sub-population of ectodermal cells. Here, we find that the ectodermal SpLox+ SpBrn1/2/4 cells are specified as SpSoxC and SpPtf1a neuronal precursors that become the lateral ganglion and the apical organ neurons. Two of the SpLox+ SpBrn1/2/4 cells also express another pancreatic transcription factor, the LIM-homeodomain gene islet-1. Moreover, we find that SpLox neurons produce the neuropeptide SpANP2, and that SpLox regulates SpANP2 expression. Taken together, our data reveal that there is a subset of sea urchin larval neurons with a gene program that predated pancreatic cells. These findings suggest that pancreatic endocrine cells co-opted a regulatory signature from an ancestral neuron that was already present in an early-branched deuterostome.
Highlights
Complex organisms have more cell types than structurally simple ones
Pancreatic endocrine β-cells and neurons are an example of different cell types that share a similar gene program but exert different functions
In order to identify terminal differentiation genes of the SpLox neurons, we looked at the expression of the sea urchin neuropeptides described by Woods et al and Rowe et al [54]
Summary
Functionally distinct cell types show remarkably similar gene programs. This shared program can be the result of a common evolutionary ancestor cell or of convergent evolution. Pancreatic endocrine β-cells and neurons are an example of different cell types that share a similar gene program but exert different functions. These two cell types share many remarkable features [1,2,3,4,5,6,7]. Many genes expressed in neuronal development are expressed in the development of pancreatic β-cells [7], like the homeodomain protein Isl1 [9], the bHLH transcription factors neurogenins [10,11,12], and the homeobox transcription factor PDX1 [13, 14]
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