MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors

Giorgia Giacomazzi; Bryan Holvoet; Sander Trenson; Ellen Caluwé; Bojana Kravic; Hanne Grosemans; Álvaro Cortés-Calabuig; Christophe M. Deroose; Danny Huylebroeck; Said Hashemolhosseini; Stefan Janssens; Elizabeth McNally; Mattia Quattrocelli; Maurilio Sampaolesi

doi:10.1038/s41467-017-01359-w

MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors

Giorgia Giacomazzi, Bryan Holvoet, Sander Trenson, Ellen Caluwé, Bojana Kravic, Hanne Grosemans, Álvaro Cortés-Calabuig, Christophe M. Deroose, Danny Huylebroeck, Said Hashemolhosseini, Stefan Janssens, Elizabeth McNally, Mattia Quattrocelli, Maurilio Sampaolesi^*

^*Corresponding author for this work

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

25 Scopus citations

Abstract

Muscular dystrophies (MDs) are often characterized by impairment of both skeletal and cardiac muscle. Regenerative strategies for both compartments therefore constitute a therapeutic avenue. Mesodermal iPSC-derived progenitors (MiPs) can regenerate both striated muscle types simultaneously in mice. Importantly, MiP myogenic propensity is influenced by somatic lineage retention. However, it is still unknown whether human MiPs have in vivo potential. Furthermore, methods to enhance the intrinsic myogenic properties of MiPs are likely needed, given the scope and need to correct large amounts of muscle in the MDs. Here, we document that human MiPs can successfully engraft into the skeletal muscle and hearts of dystrophic mice. Utilizing non-invasive live imaging and selectively induced apoptosis, we report evidence of striated muscle regeneration in vivo in mice by human MiPs. Finally, combining RNA-seq and miRNA-seq data, we define miRNA cocktails that promote the myogenic potential of human MiPs.

Original language	English (US)
Article number	1249
Journal	Nature communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-01359-w
State	Published - Dec 1 2017

Funding

This work has been supported by FWO (#G060612N, #G0A8813N, #G088715N), Opening the Future Campaign EJJ-OPTFUT-02010, Excellentiefinanciering KUL Project grant and Rondoufonds voor Duchenne Onderzoek to M.S., to E.M. and AFM#18373, FWO#1263314 to M.Q. S.H. receives support by a grant from the German Research Foundation (HA 3309/1-3) and the Interdisciplinary Center for Clinical Research Erlangen (E17). M.S. and D.H. are supported by KU Leuven Research Council funding (OT-09/053) and GOA-11/012), the Belgian Agency for Science Policy (Belspo) network IUAPVII-07 DevRepair. G.G. and M.Q. are grateful to Andy Vo for critically reviewing the ms, and to Ruben Dries for valuable suggestions about RNA-seq data analysis.

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/s41467-017-01359-w

Cite this

Giacomazzi, G., Holvoet, B., Trenson, S., Caluwé, E., Kravic, B., Grosemans, H., Cortés-Calabuig, Á., Deroose, C. M., Huylebroeck, D., Hashemolhosseini, S., Janssens, S., McNally, E., Quattrocelli, M., & Sampaolesi, M. (2017). MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors. Nature communications, 8(1), Article 1249. https://doi.org/10.1038/s41467-017-01359-w

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title = "MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors",

abstract = "Muscular dystrophies (MDs) are often characterized by impairment of both skeletal and cardiac muscle. Regenerative strategies for both compartments therefore constitute a therapeutic avenue. Mesodermal iPSC-derived progenitors (MiPs) can regenerate both striated muscle types simultaneously in mice. Importantly, MiP myogenic propensity is influenced by somatic lineage retention. However, it is still unknown whether human MiPs have in vivo potential. Furthermore, methods to enhance the intrinsic myogenic properties of MiPs are likely needed, given the scope and need to correct large amounts of muscle in the MDs. Here, we document that human MiPs can successfully engraft into the skeletal muscle and hearts of dystrophic mice. Utilizing non-invasive live imaging and selectively induced apoptosis, we report evidence of striated muscle regeneration in vivo in mice by human MiPs. Finally, combining RNA-seq and miRNA-seq data, we define miRNA cocktails that promote the myogenic potential of human MiPs.",

author = "Giorgia Giacomazzi and Bryan Holvoet and Sander Trenson and Ellen Caluw{\'e} and Bojana Kravic and Hanne Grosemans and {\'A}lvaro Cort{\'e}s-Calabuig and Deroose, {Christophe M.} and Danny Huylebroeck and Said Hashemolhosseini and Stefan Janssens and Elizabeth McNally and Mattia Quattrocelli and Maurilio Sampaolesi",

note = "Funding Information: This work has been supported by FWO (#G060612N, #G0A8813N, #G088715N), Opening the Future Campaign EJJ-OPTFUT-02010, Excellentiefinanciering KUL Project grant and Rondoufonds voor Duchenne Onderzoek to M.S., to E.M. and AFM#18373, FWO#1263314 to M.Q. S.H. receives support by a grant from the German Research Foundation (HA 3309/1-3) and the Interdisciplinary Center for Clinical Research Erlangen (E17). M.S. and D.H. are supported by KU Leuven Research Council funding (OT-09/053) and GOA-11/012), the Belgian Agency for Science Policy (Belspo) network IUAPVII-07 DevRepair. G.G. and M.Q. are grateful to Andy Vo for critically reviewing the ms, and to Ruben Dries for valuable suggestions about RNA-seq data analysis. Publisher Copyright: {\textcopyright} 2017 The Author(s).",

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Giacomazzi, G, Holvoet, B, Trenson, S, Caluwé, E, Kravic, B, Grosemans, H, Cortés-Calabuig, Á, Deroose, CM, Huylebroeck, D, Hashemolhosseini, S, Janssens, S, McNally, E, Quattrocelli, M & Sampaolesi, M 2017, 'MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors', Nature communications, vol. 8, no. 1, 1249. https://doi.org/10.1038/s41467-017-01359-w

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T1 - MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors

AU - Giacomazzi, Giorgia

AU - Holvoet, Bryan

AU - Trenson, Sander

AU - Caluwé, Ellen

AU - Kravic, Bojana

AU - Grosemans, Hanne

AU - Cortés-Calabuig, Álvaro

AU - Deroose, Christophe M.

AU - Huylebroeck, Danny

AU - Hashemolhosseini, Said

AU - Janssens, Stefan

AU - McNally, Elizabeth

AU - Quattrocelli, Mattia

AU - Sampaolesi, Maurilio

N1 - Funding Information: This work has been supported by FWO (#G060612N, #G0A8813N, #G088715N), Opening the Future Campaign EJJ-OPTFUT-02010, Excellentiefinanciering KUL Project grant and Rondoufonds voor Duchenne Onderzoek to M.S., to E.M. and AFM#18373, FWO#1263314 to M.Q. S.H. receives support by a grant from the German Research Foundation (HA 3309/1-3) and the Interdisciplinary Center for Clinical Research Erlangen (E17). M.S. and D.H. are supported by KU Leuven Research Council funding (OT-09/053) and GOA-11/012), the Belgian Agency for Science Policy (Belspo) network IUAPVII-07 DevRepair. G.G. and M.Q. are grateful to Andy Vo for critically reviewing the ms, and to Ruben Dries for valuable suggestions about RNA-seq data analysis. Publisher Copyright: © 2017 The Author(s).

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N2 - Muscular dystrophies (MDs) are often characterized by impairment of both skeletal and cardiac muscle. Regenerative strategies for both compartments therefore constitute a therapeutic avenue. Mesodermal iPSC-derived progenitors (MiPs) can regenerate both striated muscle types simultaneously in mice. Importantly, MiP myogenic propensity is influenced by somatic lineage retention. However, it is still unknown whether human MiPs have in vivo potential. Furthermore, methods to enhance the intrinsic myogenic properties of MiPs are likely needed, given the scope and need to correct large amounts of muscle in the MDs. Here, we document that human MiPs can successfully engraft into the skeletal muscle and hearts of dystrophic mice. Utilizing non-invasive live imaging and selectively induced apoptosis, we report evidence of striated muscle regeneration in vivo in mice by human MiPs. Finally, combining RNA-seq and miRNA-seq data, we define miRNA cocktails that promote the myogenic potential of human MiPs.

AB - Muscular dystrophies (MDs) are often characterized by impairment of both skeletal and cardiac muscle. Regenerative strategies for both compartments therefore constitute a therapeutic avenue. Mesodermal iPSC-derived progenitors (MiPs) can regenerate both striated muscle types simultaneously in mice. Importantly, MiP myogenic propensity is influenced by somatic lineage retention. However, it is still unknown whether human MiPs have in vivo potential. Furthermore, methods to enhance the intrinsic myogenic properties of MiPs are likely needed, given the scope and need to correct large amounts of muscle in the MDs. Here, we document that human MiPs can successfully engraft into the skeletal muscle and hearts of dystrophic mice. Utilizing non-invasive live imaging and selectively induced apoptosis, we report evidence of striated muscle regeneration in vivo in mice by human MiPs. Finally, combining RNA-seq and miRNA-seq data, we define miRNA cocktails that promote the myogenic potential of human MiPs.

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MicroRNAs promote skeletal muscle differentiation of mesodermal iPSC-derived progenitors

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