The forkhead transcription factor Foxj1 controls vertebrate olfactory cilia biogenesis and sensory neuron differentiation

Dheeraj Rayamajhi, Mert Ege, Kirill Ukhanov, Christa Ringers, Yiliu Zhang, Inyoung Jung, Percival P. D'Gama, Summer Shijia Li, Mehmet Ilyas Cosacak, Caghan Kizil, Hae Chul Park, Emre Yaksi, Jeffrey R. Martens, Steven L. Brody, Nathalie Jurisch-Yaksi, Sudipto Roy

Research output: Contribution to journalArticlepeer-review

1 Citation (Scopus)

Abstract

In vertebrates, olfactory receptors localize on multiple cilia elaborated on dendritic knobs of olfactory sensory neurons (OSNs). Although olfactory cilia dysfunction can cause anosmia, how their differentiation is programmed at the transcriptional level has remained largely unexplored. We discovered in zebrafish and mice that Foxj1, a forkhead domain-containing transcription factor traditionally linked with motile cilia biogenesis, is expressed in OSNs and required for olfactory epithelium (OE) formation. In keeping with the immotile nature of olfactory cilia, we observed that ciliary motility genes are repressed in zebrafish, mouse, and human OSNs. Strikingly, we also found that besides ciliogenesis, Foxj1 controls the differentiation of the OSNs themselves by regulating their cell type-specific gene expression, such as that of olfactory marker protein (omp) involved in odor-evoked signal transduction. In line with this, response to bile acids, odors detected by OMP-positive OSNs, was significantly diminished in foxj1 mutant zebrafish. Taken together, our findings establish how the canonical Foxj1-mediated motile ciliogenic transcriptional program has been repurposed for the biogenesis of immotile olfactory cilia, as well as for the development of the OSNs.

Original languageEnglish
Article numbere3002468
JournalPLoS biology
Volume22
Issue number1
DOIs
Publication statusPublished - 2024 Jan

Bibliographical note

Publisher Copyright:
© 2024 Rayamajhi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

ASJC Scopus subject areas

  • General Neuroscience
  • General Biochemistry,Genetics and Molecular Biology
  • General Immunology and Microbiology
  • General Agricultural and Biological Sciences

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