Co-option of the PRDM14-CBFA2T complex from motor neurons to pluripotent cells during vertebrate evolution

Development. 2019 Jan 28;146(2):dev168633. doi: 10.1242/dev.168633.

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.This article has an associated 'The people behind the papers' interview.

Keywords: CBFA2T; Co-option; Motor neuron; PRDM14; Pluripotent cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biological Evolution*
  • Biomarkers / metabolism
  • DNA Demethylation
  • DNA Methylation
  • DNA-Binding Proteins
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Developmental
  • Lancelets / embryology
  • Lancelets / metabolism
  • Mice
  • Mice, Knockout
  • Motor Neurons / metabolism*
  • Mouse Embryonic Stem Cells / metabolism*
  • Phylogeny
  • Pluripotent Stem Cells / metabolism*
  • Protein Binding
  • Protein Domains
  • RNA-Binding Proteins
  • Repressor Proteins / chemistry
  • Repressor Proteins / metabolism*
  • Sea Urchins / embryology
  • Sea Urchins / metabolism
  • Sequence Homology, Nucleic Acid
  • Synteny / genetics
  • Transcription Factors / metabolism*
  • Vertebrates / embryology
  • Vertebrates / metabolism*
  • Zebrafish / embryology
  • Zebrafish / metabolism

Substances

  • Biomarkers
  • CBFA2T2 myeloid-transforming gene-related protein
  • DNA-Binding Proteins
  • Prdm14 protein, mouse
  • RNA-Binding Proteins
  • Repressor Proteins
  • Transcription Factors