ABSTRACT
Gene regulatory networks underlying cellular pluripotency are controlled by a core circuitry of transcription factors in mammals, including POU5F1. However, the evolutionary origin and transformation of pluripotency-related transcriptional networks have not been elucidated in deuterostomes. PR domain-containing protein 14 (PRDM14) is specifically expressed in pluripotent cells and germ cells, and is required for establishing embryonic stem cells (ESCs) and primordial germ cells in mice. Here, we compared the functions and expression patterns of PRDM14 orthologues within deuterostomes. Amphioxus PRDM14 and zebrafish PRDM14, but not sea urchin PRDM14, compensated for mouse PRDM14 function in maintaining mouse ESC pluripotency. Interestingly, sea urchin PRDM14 together with sea urchin CBFA2T, an essential partner of PRDM14 in mouse ESCs, complemented the self-renewal defect in mouse Prdm14 KO ESCs. Contrary to the Prdm14 expression pattern in mouse embryos, Prdm14 was expressed in motor neurons of amphioxus embryos, as observed in zebrafish embryos. Thus, Prdm14 expression in motor neurons was conserved in non-tetrapod deuterostomes and the co-option of the PRDM14-CBFA2T complex from motor neurons into pluripotent cells may have maintained the transcriptional network for pluripotency during vertebrate evolution.
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Footnotes
Author contributions
Conceptualization: Y. Seki; Methodology: Y. Seki; Validation: Y. Seki; Investigation: Y. Seki, M.K., K.S., C.-Y.L., S.K., Y. Suwa, S. Hashimoto, L.W.Y., K.T., S. Higashida, D.K.; Writing - original draft: Y. Seki; Writing - review & editing: Y. Seki, S.K., K.M., J.-K.Y.; Supervision: Y. Seki; Project administration: Y. Seki; Funding acquisition: Y. Seki, J.-K.Y.
Funding
This study was supported by a Grant-in-Aid for Young Scientists (A) (Japan Society for the Promotion of Science KAKENHI grant number 24681040), by a Grant-in-Aid for Scientific Research (B) (Japan Society for the Promotion of Science KAKENHI grant number 18H02422), by the Promotion of Joint International Research (Japan Society for the Promotion of Science KAKENHI grant number 15KK0262), by Scientific Research on Innovative Areas, ‘Epigenome dynamics and regulation in germ cells’ (Ministry of Education, Culture, Sports, Science, and Technology KAKENHI grant numbers 26112514 and 16H01223), by Scientific Research on Innovative Areas, ‘Mechanisms regulating gamete formation in animals’ (Ministry of Education, Culture, Sports, Science, and Technology KAKENHI grant number 16H01258), by support from Academia Sinica, Taiwan (to J.-K.Y.) and by support from the Ministry of Science and Technology, Taiwan (grant number MOST 102-2311-B-001-011-MY3 to J.-K.Y.).
Data availability
Microarray data have been deposited in GEO under accession number GSE112904.
