TY - JOUR
T1 - miR-203 secreted in extracellular vesicles mediates the communication between neural crest and placode cells required for trigeminal ganglia formation
AU - Bernardi, Yanel E.
AU - Sanchez-Vasquez, Estefania
AU - Márquez, Rocío Belén
AU - Piacentino, Michael L.
AU - Urrutia, Hugo
AU - Rossi, Izadora
AU - Saraiva, Karina L.Alcantara
AU - Pereira-Neves, Antonio
AU - Ramirez, Marcel I.
AU - Bronner, Marianne E.
AU - de Miguel, Natalia
AU - Strobl-Mazzulla, Pablo H.
N1 - Publisher Copyright:
© 2024 Bernardi 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.
PY - 2024/7
Y1 - 2024/7
N2 - 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.
AB - 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.
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U2 - 10.1371/journal.pbio.3002074
DO - 10.1371/journal.pbio.3002074
M3 - Article
C2 - 39038054
AN - SCOPUS:85199300540
SN - 1544-9173
VL - 22
JO - PLoS biology
JF - PLoS biology
IS - 7 July
M1 - e3002074
ER -