Evolutionary Transition in the Regulation of Vertebrate Pronephros Development: A New Role for Retinoic Acid

Pascal Schmidt, Eva Leman, Ronan Lagadec, Michael Schubert, Sylvie Mazan, Ram Reshef

Research output: Contribution to journalArticlepeer-review

Abstract

The anterior-posterior (AP) axis in chordates is regulated by a conserved set of genes and signaling pathways, including Hox genes and retinoic acid (RA), which play well-characterized roles in the organization of the chordate body plan. The intermediate mesoderm (IM), which gives rise to all vertebrate kidneys, is an example of a tissue that differentiates sequentially along this axis. Yet, the conservation of the spatiotemporal regulation of the IM across vertebrates remains poorly understood. In this study, we used a comparative developmental approach focusing on non-conventional model organisms, a chondrichthyan (catshark), a cyclostome (lamprey), and a cephalochordate (amphioxus), to assess the involvement of RA in the regulation of chordate and vertebrate pronephros formation. We report that the anterior expression boundary of early pronephric markers (Pax2 and Lim1), positioned at the level of somite 6 in amniotes, is conserved in the catshark and the lamprey. Furthermore, RA, driving the expression of Hox4 genes like in amniotes, regulates the anterior pronephros boundary in the catshark. We find no evidence for the involvement of this regulatory hierarchy in the AP positioning of the lamprey pronephros and the amphioxus pronephros homolog, Hatschek’s nephridium. This suggests that despite the conservation of Pax2 and Lim1 expressions in chordate pronephros homologs, the responsiveness of the IM, and hence of pronephric genes, to RA-and Hox-dependent regulation is a gnathostome novelty.

Original languageEnglish
Article number1304
JournalCells
Volume11
Issue number8
DOIs
StatePublished - 1 Apr 2022

Bibliographical note

Funding Information:
This research received partial funding from the European Union?s Horizon 2020 research and innovation program ASSEMBLE Plus, grant number 9764 BA0320 (R.R.), EMBRC-France, a FP7 Construction of New Research Infrastructure Project, host contract 990-BA/2017-08 (R.R), and the Agence Nationale de la Recherche contract ANR-16-CE13-0013-02 (S.M.). This study was further supported by the CNRS (M.S. and S.M.). The above-mentioned services of the Institut de la Mer de Villefranche (France) and the Observatoire Oc?anologique de Banyuls-sur-Mer (France) received financial support from EMBRC-France (ANR-10-INBS-02). This study was generously supported by internal funding to R.R from the Research Authority of the University of Haifa, Israel.

Funding Information:
Funding: This research received partial funding from the European Union’s Horizon 2020 research and innovation program ASSEMBLE Plus, grant number 9764 BA0320 (R.R.), EMBRC-France, a FP7 Construction of New Research Infrastructure Project, host contract 990-BA/2017-08 (R.R), and the Agence Nationale de la Recherche contract ANR-16-CE13-0013-02 (S.M.). This study was further supported by the CNRS (M.S. and S.M.). The above-mentioned services of the Institut de la Mer de Villefranche (France) and the Observatoire Océanologique de Banyuls-sur-Mer (France) received financial support from EMBRC-France (ANR-10-INBS-02). This study was generously supported by internal funding to R.R from the Research Authority of the University of Haifa, Israel.

Publisher Copyright:
© 2022 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

  • amphioxus
  • catshark
  • evolution of development
  • Hox genes
  • kidney
  • lamprey
  • pronephros
  • retinoic acid

ASJC Scopus subject areas

  • Medicine (all)

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