NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration

Béryl Laplace-Builhé; Audrey Barthelaix; Said Assou; Candice Bohaud; Marine Pratlong; Dany Severac; Gautier Tejedor; Patricia Luz-Crawford; Mai Nguyen-Chi; Marc Mathieu; Christian Jorgensen; Farida Djouad

doi:10.1038/s41467-021-26422-5

NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration

Béryl Laplace-Builhé, Audrey Barthelaix, Said Assou, Candice Bohaud, Marine Pratlong, Dany Severac, Gautier Tejedor, Patricia Luz-Crawford, Mai Nguyen-Chi, Marc Mathieu, Christian Jorgensen, Farida Djouad^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

Fish species, such as zebrafish (Danio rerio), can regenerate their appendages after amputation through the formation of a heterogeneous cellular structure named blastema. Here, by combining live imaging of triple transgenic zebrafish embryos and single-cell RNA sequencing we established a detailed cell atlas of the regenerating caudal fin in zebrafish larvae. We confirmed the presence of macrophage subsets that govern zebrafish fin regeneration, and identified a foxd3-positive cell population within the regenerating fin. Genetic depletion of these foxd3-positive neural crest-derived cells (NCdC) showed that they are involved in blastema formation and caudal fin regeneration. Finally, chemical inhibition and transcriptomic analysis demonstrated that these foxd3-positive cells regulate macrophage recruitment and polarization through the NRG1/ErbB pathway. Here, we show the diversity of the cells required for blastema formation, identify a discrete foxd3-positive NCdC population, and reveal the critical function of the NRG1/ErbB pathway in controlling the dialogue between macrophages and NCdC.

Original language	English
Article number	6336
Pages (from-to)	6336
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-26422-5
State	Published - 3 Nov 2021

Bibliographical note

Funding Information:
This work was supported by Inserm and University of Montpellier. We thank the MRI facility for their assistance, T. Sauka-Spengler (University of Oxford, United Kingdom) for shipping the Tg(foxd3-mcherry)ct110 zebrafish line, M. Bagnat for shipping Tg(rcn3:gal4/UAS:mCherry) line. A. Kawakami (Tokyo Institute of Technology, Japan) for the junbl plasmid, K. Poss (Duke University Medical Center, USA) for the nrg1 plasmid, R. Kelsh (University of Bath, United Kingdom) for the Fkd6in situ hybridization plasmid. MP and DS acknowledge financial support from the France Génomique National infrastructure, funded as part of “Investissement d’avenir” programme managed by the Agence Nationale pour la Recherche (contract ANR-10-INBS-09). We also thank the Zebrafish facility of the University of Montpellier, the MRI facility for their assistance and the CARTIGEN platform.

Publisher Copyright:
© 2021, The Author(s).

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10.1038/s41467-021-26422-5

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Laplace-Builhé, B., Barthelaix, A., Assou, S., Bohaud, C., Pratlong, M., Severac, D., Tejedor, G., Luz-Crawford, P., Nguyen-Chi, M., Mathieu, M., Jorgensen, C., & Djouad, F. (2021). NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration. Nature Communications, 12(1), 6336. Article 6336. https://doi.org/10.1038/s41467-021-26422-5

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title = "NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration",

abstract = "Fish species, such as zebrafish (Danio rerio), can regenerate their appendages after amputation through the formation of a heterogeneous cellular structure named blastema. Here, by combining live imaging of triple transgenic zebrafish embryos and single-cell RNA sequencing we established a detailed cell atlas of the regenerating caudal fin in zebrafish larvae. We confirmed the presence of macrophage subsets that govern zebrafish fin regeneration, and identified a foxd3-positive cell population within the regenerating fin. Genetic depletion of these foxd3-positive neural crest-derived cells (NCdC) showed that they are involved in blastema formation and caudal fin regeneration. Finally, chemical inhibition and transcriptomic analysis demonstrated that these foxd3-positive cells regulate macrophage recruitment and polarization through the NRG1/ErbB pathway. Here, we show the diversity of the cells required for blastema formation, identify a discrete foxd3-positive NCdC population, and reveal the critical function of the NRG1/ErbB pathway in controlling the dialogue between macrophages and NCdC.",

keywords = "Animal Fins, Animals, Cell Proliferation, Forkhead Transcription Factors, Gene Expression Regulation, Neoplastic, Developmental; Genes, erbB, Larva, Macrophages, Neural Crest, Neuregulin-1, Regeneration, Signal Transduction, Stem Cells, Zebrafish, Zebrafish Proteins",

author = "B{\'e}ryl Laplace-Builh{\'e} and Audrey Barthelaix and Said Assou and Candice Bohaud and Marine Pratlong and Dany Severac and Gautier Tejedor and Patricia Luz-Crawford and Mai Nguyen-Chi and Marc Mathieu and Christian Jorgensen and Farida Djouad",

note = "Funding Information: This work was supported by Inserm and University of Montpellier. We thank the MRI facility for their assistance, T. Sauka-Spengler (University of Oxford, United Kingdom) for shipping the Tg(foxd3-mcherry)ct110 zebrafish line, M. Bagnat for shipping Tg(rcn3:gal4/UAS:mCherry) line. A. Kawakami (Tokyo Institute of Technology, Japan) for the junbl plasmid, K. Poss (Duke University Medical Center, USA) for the nrg1 plasmid, R. Kelsh (University of Bath, United Kingdom) for the Fkd6in situ hybridization plasmid. MP and DS acknowledge financial support from the France G{\'e}nomique National infrastructure, funded as part of “Investissement d{\textquoteright}avenir” programme managed by the Agence Nationale pour la Recherche (contract ANR-10-INBS-09). We also thank the Zebrafish facility of the University of Montpellier, the MRI facility for their assistance and the CARTIGEN platform. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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doi = "10.1038/s41467-021-26422-5",

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Laplace-Builhé, B, Barthelaix, A, Assou, S, Bohaud, C, Pratlong, M, Severac, D, Tejedor, G, Luz-Crawford, P, Nguyen-Chi, M, Mathieu, M, Jorgensen, C & Djouad, F 2021, 'NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration', Nature Communications, vol. 12, no. 1, 6336, pp. 6336. https://doi.org/10.1038/s41467-021-26422-5

TY - JOUR

T1 - NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration

AU - Laplace-Builhé, Béryl

AU - Barthelaix, Audrey

AU - Assou, Said

AU - Bohaud, Candice

AU - Pratlong, Marine

AU - Severac, Dany

AU - Tejedor, Gautier

AU - Luz-Crawford, Patricia

AU - Nguyen-Chi, Mai

AU - Mathieu, Marc

AU - Jorgensen, Christian

AU - Djouad, Farida

N1 - Funding Information: This work was supported by Inserm and University of Montpellier. We thank the MRI facility for their assistance, T. Sauka-Spengler (University of Oxford, United Kingdom) for shipping the Tg(foxd3-mcherry)ct110 zebrafish line, M. Bagnat for shipping Tg(rcn3:gal4/UAS:mCherry) line. A. Kawakami (Tokyo Institute of Technology, Japan) for the junbl plasmid, K. Poss (Duke University Medical Center, USA) for the nrg1 plasmid, R. Kelsh (University of Bath, United Kingdom) for the Fkd6in situ hybridization plasmid. MP and DS acknowledge financial support from the France Génomique National infrastructure, funded as part of “Investissement d’avenir” programme managed by the Agence Nationale pour la Recherche (contract ANR-10-INBS-09). We also thank the Zebrafish facility of the University of Montpellier, the MRI facility for their assistance and the CARTIGEN platform. Publisher Copyright: © 2021, The Author(s).

PY - 2021/11/3

Y1 - 2021/11/3

N2 - Fish species, such as zebrafish (Danio rerio), can regenerate their appendages after amputation through the formation of a heterogeneous cellular structure named blastema. Here, by combining live imaging of triple transgenic zebrafish embryos and single-cell RNA sequencing we established a detailed cell atlas of the regenerating caudal fin in zebrafish larvae. We confirmed the presence of macrophage subsets that govern zebrafish fin regeneration, and identified a foxd3-positive cell population within the regenerating fin. Genetic depletion of these foxd3-positive neural crest-derived cells (NCdC) showed that they are involved in blastema formation and caudal fin regeneration. Finally, chemical inhibition and transcriptomic analysis demonstrated that these foxd3-positive cells regulate macrophage recruitment and polarization through the NRG1/ErbB pathway. Here, we show the diversity of the cells required for blastema formation, identify a discrete foxd3-positive NCdC population, and reveal the critical function of the NRG1/ErbB pathway in controlling the dialogue between macrophages and NCdC.

AB - Fish species, such as zebrafish (Danio rerio), can regenerate their appendages after amputation through the formation of a heterogeneous cellular structure named blastema. Here, by combining live imaging of triple transgenic zebrafish embryos and single-cell RNA sequencing we established a detailed cell atlas of the regenerating caudal fin in zebrafish larvae. We confirmed the presence of macrophage subsets that govern zebrafish fin regeneration, and identified a foxd3-positive cell population within the regenerating fin. Genetic depletion of these foxd3-positive neural crest-derived cells (NCdC) showed that they are involved in blastema formation and caudal fin regeneration. Finally, chemical inhibition and transcriptomic analysis demonstrated that these foxd3-positive cells regulate macrophage recruitment and polarization through the NRG1/ErbB pathway. Here, we show the diversity of the cells required for blastema formation, identify a discrete foxd3-positive NCdC population, and reveal the critical function of the NRG1/ErbB pathway in controlling the dialogue between macrophages and NCdC.

KW - Animal Fins

KW - Animals

KW - Cell Proliferation

KW - Forkhead Transcription Factors

KW - Gene Expression Regulation, Neoplastic

KW - Developmental; Genes

KW - erbB

KW - Larva

KW - Macrophages

KW - Neural Crest

KW - Neuregulin-1

KW - Regeneration

KW - Signal Transduction

KW - Stem Cells

KW - Zebrafish

KW - Zebrafish Proteins

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U2 - 10.1038/s41467-021-26422-5

DO - 10.1038/s41467-021-26422-5

M3 - Article

C2 - 34732706

AN - SCOPUS:85118570447

SN - 2041-1723

VL - 12

SP - 6336

JO - Nature Communications

JF - Nature Communications

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M1 - 6336

ER -

NRG1/ErbB signalling controls the dialogue between macrophages and neural crest-derived cells during zebrafish fin regeneration

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