miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation

Yanel E. Bernardi, Estefania Sanchez-Vasquez, Rocío Belén Márquez, Michael L. Piacentino, Hugo Urrutia, Izadora Rossi, Karina L.Alcantara Saraiva, Antonio Pereira-Neves, Marcel I. Ramirez, Marianne E. Bronner, Natalia de Miguel, Pablo H. Strobl-Mazzulla

Research output: Contribution to journalArticlepeer-review

Abstract

AWUhi:lePilnetaesreaccotniofinrms tbheattwalelheenandeinugrlaelvcelrseasrtearenpdrepsleanctoeddceocrerellcstlayr:e critical for the proper formation of the trigeminal ganglion, the mechanisms underlying this process remain largely uncharacterized. Here, by using chick embryos, we show that the microRNA (miR)-203, whose epigenetic repression is required for neural crest migration, is reactivated in coalescing and condensing trigeminal ganglion cells. Overexpression of miR-203 induces ectopic coalescence of neural crest cells and increases ganglion size. By employing cell-specific electroporations for either miR-203 sponging or genomic editing using CRISPR/Cas9, we elucidated that neural crest cells serve as the source, while placode cells serve as the site of action for miR-203 in trigeminal ganglion condensation. Demonstrating intercellular communication, overexpression of miR-203 in the neural crest in vitro or in vivo represses an miRresponsive sensor in placode cells. Moreover, neural crest-secreted extracellular vesicles (EVs), visualized using pHluorin-CD63 vector, become incorporated into the cytoplasm of placode cells. Finally, RT-PCR analysis shows that small EVs isolated from condensing trigeminal ganglia are selectively loaded with miR-203. Together, our findings reveal a critical role in vivo for neural crest-placode communication mediated by sEVs and their selective microRNA cargo for proper trigeminal ganglion formation.

Original languageEnglish (US)
Article numbere3002074
JournalPLoS biology
Volume22
Issue number7 July
DOIs
StatePublished - Jul 2024
Externally publishedYes

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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