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9. Overlapping functions of SIX homeoproteins during embryonic myogenesis.

Author

Wurmser, Maud, Madani, Rouba, Chaverot, Nathalie, Backer, Stéphanie, Borok, Matthew, Dos Santos, Matthieu, Comai, Glenda, Tajbakhsh, Shahragim, Relaix, Frédéric, Santolini, Marc, Sambasivan, Ramkumar, Jiang, Rulang, and Maire, Pascal

Subjects
MYOGENESIS, HOMEOBOX proteins, MYOBLASTS, PROGENITOR cells, STEM cells
Abstract

Four SIX homeoproteins display a combinatorial expression throughout embryonic developmental myogenesis and they modulate the expression of the myogenic regulatory factors. Here, we provide a deep characterization of their role in distinct mouse developmental territories. We showed, at the hypaxial level, that the Six1:Six4 double knockout (dKO) somitic precursor cells adopt a smooth muscle fate and lose their myogenic identity. At the epaxial level, we demonstrated by the analysis of Six quadruple KO (qKO) embryos, that SIX are required for fetal myogenesis, and for the maintenance of PAX7+ progenitor cells, which differentiated prematurely and are lost by the end of fetal development in qKO embryos. Finally, we showed that Six1 and Six2 are required to establish craniofacial myogenesis by controlling the expression of Myf5. We have thus described an unknown role for SIX proteins in the control of myogenesis at different embryonic levels and refined their involvement in the genetic cascades operating at the head level and in the genesis of myogenic stem cells. Author summary: We demonstrate with double, triple and quadruple Six KO mouse embryos that specific Six combinations are required for proper myogenesis depending on the level of the mouse embryonic body axis. We show that the Six1 and Six2 genes are required for craniofacial myogenesis by controlling the engagement of unsegmented cranial paraxial mesodermal cells in the myogenic pathway. We also show that hypaxial somitic dermomyotomal cells from embryos mutant for the Six1 and Six4 genes are unable to engage in the skeletal muscle lineage. Last, we show that embryos mutant for the four Six genes expressed in the myogenic lineage exhibit a defect in self-renewal of PAX7+ stem cells present in their residual muscle masses, and that SIX proteins interact directly with several enhancer elements at the Pax7 locus to control its expression. We have thus characterized new functions of SIX proteins in the control of myogenesis at different embryonic levels and refined their involvement in the genetic cascades that govern the genesis of myogenic stem cells. [ABSTRACT FROM AUTHOR]

Published
2023
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30. Myf5 haploinsufficiency reveals distinct cell fate potentials for adult skeletal muscle stem cells

Author

Gayraud-Morel, Barbara, primary, Chrétien, Fabrice, additional, Jory, Aurélie, additional, Sambasivan, Ramkumar, additional, Negroni, Elisa, additional, Flamant, Patricia, additional, Soubigou, Guillaume, additional, Coppée, Jean-Yves, additional, Di Santo, James, additional, Cumano, Ana, additional, Mouly, Vincent, additional, and Tajbakhsh, Shahragim, additional

Published
2012
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36. Comparison of multiple transcriptomes exposes unified and divergent features of quiescent and activated skeletal muscle stem cells

Author

Natalia Pietrosemoli, Siham Yennek, Ramkumar Sambasivan, Daniela Di Girolamo, Shahragim Tajbakhsh, Francesca Pala, Hiroshi Sakai, Meryem B. Baghdadi, Sébastien Mella, Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Cellules Souches et Développement / Stem Cells and Development, Institute for Stem Cell Biology and Regenerative Medicine [Bengaluru, India], funded by Institut Pasteur, Centre National pour la RechercheScientific, the Agence Nationale de la Recherche (Laboratoire d’ExcellenceRevive, Investissement d’Avenir, ANR-10-LABX- 73), and the EuropeanResearch Council (advanced research grant 332893), ANR-10-LABX-0073,REVIVE,Stem Cells in Regenerative Biology and Medicine(2010), European Project: 332893,332893, Pietrosemoli, Natalia, Mella, Sébastien, Yennek, Siham, Baghdadi, Meryem B, Sakai, Hiroshi, Sambasivan, Ramkumar, Pala, Francesca, Di Girolamo, Daniela, Tajbakhsh, Shahragim, and Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, lcsh:Diseases of the musculoskeletal system, Databases, Factual, Satellite Cells, Skeletal Muscle, [SDV]Life Sciences [q-bio], Cell, Computational biology, Quiescence, Biology, Skeletal muscle satellite cells, Transcriptome, Mice, 03 medical and health sciences, 0302 clinical medicine, Gene expression, medicine, Animals, E2F, Gene, 030304 developmental biology, 0303 health sciences, Myogenesis, Gene Expression Profiling, Multi-level transcriptomic comparison, Cell Differentiation, Cell cycle, medicine.anatomical_structure, 030220 oncology & carcinogenesis, Female, lcsh:RC925-935, Stem cell, Multi-level transcriptomic comparisons, Sherpa
Abstract

BackgroundSkeletal muscle stem cells (MuSCs) are quiescent in adult mice and can undergo multiple rounds of proliferation and self-renewal following muscle injury. Several labs have profiled transcripts of myogenic cells during developmental and adult myogenesis with the aim of identifying quiescent markers. Here, we focused on the quiescent cell state and generated new transcriptome profiles that include subfractionations of adult MuSC populations, and an artificially induced prenatal quiescent state, to identify core signatures for quiescent and proliferating MuSCs.MethodsComparison of available data offered challenges related to the inherent diversity of datasets and biological conditions. We developed a standardized workflow to homogenize the normalization, filtering, quality control steps for the analysis of gene expression profiles allowing the identification up- and down-regulated genes and the subsequent gene set enrichment analysis. To share the analytical pipeline of this work, we developed Sherpa, an interactive Shiny server that allows multiscale comparisons for extraction of desired gene sets from the analysed datasets. This tool is adaptable to cell populations in other contexts and tissues.ResultsA multiscale analysis comprising eight datasets of quiescent MuSCs had 207 and 542 genes commonly up- and down-regulated, respectively. Shared up-regulated gene sets include an over-representation of the TNFa pathway via NFKb signaling, Il6-Jak-Stat3 signaling, and the apical surface processes, while shared down-regulated gene sets exhibited an over-representation of Myc and E2F targets, and genes associated to the G2M checkpoint and oxidative phosphorylation. However, virtually all datasets contained genes that are associated with activation or cell cycle entry, such as the immediate early stress response genes Fos and Jun. Empirical examination of fixed and isolated MuSCs showed that these and other genes were absent in vivo, but activated during procedural isolation of cells.ConclusionsThrough the systematic comparison and individual analysis of diverse transcriptomic profiles, we identified genes that were consistently differentially expressed among the different datasets and common underlying biological processes key to the quiescent cell state. Our findings provide impetus to define and distinguish transcripts associated with true in vivo quiescence from those that are first responding genes due to disruption of the stem cell niche.

Published
2017
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