Direct development of neurons within foregut endoderm of sea urchin embryos

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 108; no. 22; pp. 9143 - 9147
• Main Authors: Wei, Zheng, Angerer, Robert C., Angerer, Lynne M.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 31.05.2011; National Acad Sciences
• Subjects: Animals; Bilateria; Biological Sciences; Cell Lineage; Cells; Echinoidea; Ectoderm; Embryogenesis; Embryonic stem cells; Embryos; Endoderm; Endoderm - cytology; Eye Proteins - metabolism; Foregut; Gene expression; Gene Expression Regulation, Developmental; Homeobox Protein SIX3; Homeodomain Proteins - metabolism; In Situ Hybridization; Intestines - cytology; Invertebrates; Marine; Models, Biological; Nerve Tissue Proteins - metabolism; Neural stem cells; Neurons; Neurons - metabolism; Oligonucleotides, Antisense - genetics; Pluripotent stem cells; Proteins; RNA, Messenger - metabolism; Sea Urchins; SOXB1 Transcription Factors - metabolism; Time Factors
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1018513108

Although it is well established that neural cells are ectodermal derivatives in bilaterian animals, here we report the surprising discovery that some of the pharyngeal neurons of sea urchin embryos develop de novo from the endoderm. The appearance of these neurons is independent of mouth formation, in which the stomodeal ectoderm joins the foregut. The neurons do not derive from migration of ectoderm cells to the foregut, as shown by lineage tracing with the photoactivatable protein KikGR. Their specification and development depend on expression of Nkx3-2, which in turn depends on Six3, both of which are expressed in the foregut lineage. SoxB1, which is closely related to the vertebrate Sox factors that support a neural precursor state, is also expressed in the foregut throughout gastrulation, suggesting that this region of the fully formed archenteron retains an unexpected pluripotency. Together, these results lead to the unexpected conclusion that, within a cell lineage already specified to be endoderm by a well-established gene regulatory network [Peter IS, Davidson EH (2010) Dev Biol 340:188–199], there also operates a Six3/Nkx3-2—dependent pathway required for the de novo specification of some of the neurons in the pharynx. As a result, neuroendoderm precursors form in the foregut aided by retention of a SoxB1-dependent pluripotent state.