A Tead1-Apelin axis directs paracrine communication from myogenic to endothelial cells in skeletal muscle

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Summary

Apelin (Apln) is a myokine that regulates skeletal muscle plasticity and metabolism and declines during aging. Through a yeast one-hybrid transcription factor binding screen, we identified the TEA domain transcription factor 1 (Tead1) as a novel regulator of the Apln promoter. Single-cell analysis of regenerating muscle revealed that the apelin receptor ( Aplnr) is enriched in endothelial cells, whereas Tead1 is enriched in myogenic cells. Knock-down of Tead1 stimulates Apln secretion from muscle cells in vitro and myofiber-specific overexpression of Tead1 suppresses Apln secretion in vivo. Apln secretion via Tead1 knock-down in muscle cells stimulates endothelial cell expansion via endothelial Aplnr. In vivo, Apln peptide supplementation enhances endothelial cell expansion while Tead1 muscle overexpression delays endothelial remodeling following muscle injury. Our work describes a novel paracrine crosstalk in which Apln secretion is controlled by Tead1 in myogenic cells and influences endothelial remodeling during muscle repair.

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Highlights

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A transcription factor binding screen identified that Tead1 binds the Apln promoter
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Tead1 represses the secretion of the Apln peptide from myogenic cells
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Apln stimulates endothelial cell remodeling during muscle regeneration
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Tead1-mediated regulation of Apln in myogenic cells controls endothelial cell remodeling

Abstract

Molecular biology; Molecular mechanism of gene regulation; Cell biology

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Most cited references 66

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Integrating single-cell transcriptomic data across different conditions, technologies, and species

Rahul Satija, Efthymia Papalexi, Peter Smibert … (2018)

Computational single-cell RNA-seq (scRNA-seq) methods have been successfully applied to experiments representing a single condition, technology, or species to discover and define cellular phenotypes. However, identifying subpopulations of cells that are present across multiple data sets remains challenging. Here, we introduce an analytical strategy for integrating scRNA-seq data sets based on common sources of variation, enabling the identification of shared populations across data sets and downstream comparative analysis. We apply this approach, implemented in our R toolkit Seurat (http://satijalab.org/seurat/), to align scRNA-seq data sets of peripheral blood mononuclear cells under resting and stimulated conditions, hematopoietic progenitors sequenced using two profiling technologies, and pancreatic cell 'atlases' generated from human and mouse islets. In each case, we learn distinct or transitional cell states jointly across data sets, while boosting statistical power through integrated analysis. Our approach facilitates general comparisons of scRNA-seq data sets, potentially deepening our understanding of how distinct cell states respond to perturbation, disease, and evolution.

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Fast, sensitive, and accurate integration of single cell data with Harmony

Ilya Korsunsky, Nghia Millard, Jean Fan … (2019)

The emerging diversity of single cell RNAseq datasets allows for the full transcriptional characterization of cell types across a wide variety of biological and clinical conditions. However, it is challenging to analyze them together, particularly when datasets are assayed with different technologies. Here, real biological differences are interspersed with technical differences. We present Harmony, an algorithm that projects cells into a shared embedding in which cells group by cell type rather than dataset-specific conditions. Harmony simultaneously accounts for multiple experimental and biological factors. In six analyses, we demonstrate the superior performance of Harmony to previously published algorithms. We show that Harmony requires dramatically fewer computational resources. It is the only currently available algorithm that makes the integration of ~106 cells feasible on a personal computer. We apply Harmony to PBMCs from datasets with large experimental differences, 5 studies of pancreatic islet cells, mouse embryogenesis datasets, and cross-modality spatial integration.

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Satellite cells and the muscle stem cell niche.

Hang Yin, Feodor Price, Michael A Rudnicki (2013)

Adult skeletal muscle in mammals is a stable tissue under normal circumstances but has remarkable ability to repair after injury. Skeletal muscle regeneration is a highly orchestrated process involving the activation of various cellular and molecular responses. As skeletal muscle stem cells, satellite cells play an indispensible role in this process. The self-renewing proliferation of satellite cells not only maintains the stem cell population but also provides numerous myogenic cells, which proliferate, differentiate, fuse, and lead to new myofiber formation and reconstitution of a functional contractile apparatus. The complex behavior of satellite cells during skeletal muscle regeneration is tightly regulated through the dynamic interplay between intrinsic factors within satellite cells and extrinsic factors constituting the muscle stem cell niche/microenvironment. For the last half century, the advance of molecular biology, cell biology, and genetics has greatly improved our understanding of skeletal muscle biology. Here, we review some recent advances, with focuses on functions of satellite cells and their niche during the process of skeletal muscle regeneration.

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Author and article information

Contributors

Jerome N. Feige

Journal

Journal ID (nlm-ta): iScience

Journal ID (iso-abbrev): iScience

Title: iScience

Publisher: Elsevier

ISSN (Electronic): 2589-0042

Publication date PMC-release: 14 June 2022

Publication date Collection: 15 July 2022

Publication date (Electronic): 14 June 2022

Volume: 25

Issue: 7

Electronic Location Identifier: 104589

Affiliations

[1 ]Nestlé Institute of Health Sciences, Nestlé Research, Lausanne, Switzerland

[2 ]Meinig School of Biomedical Engineering, Cornell University, Ithaca, NY, USA

[3 ]School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

[4 ]Department of Physiology and Cell Biology, The Ohio State University College of Medicine, Columbus, OH, USA

Author notes

[∗ ]Corresponding author jerome.feige@ 123456rd.nestle.com

[5]

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Publisher Item ID: S2589-0042(22)00861-6 Publisher ID: 104589

DOI: 10.1016/j.isci.2022.104589

PMC ID: 9250016

PubMed ID: 35789856

SO-VID: ea1494ab-8345-4a3d-95bb-71f5975c4409

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

A Tead1-Apelin axis directs paracrine communication from myogenic to endothelial cells in skeletal muscle

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Evolutionary Cell Biology

Most cited references 66

Integrating single-cell transcriptomic data across different conditions, technologies, and species

Fast, sensitive, and accurate integration of single cell data with Harmony

Satellite cells and the muscle stem cell niche.

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