Muscle Satellite Cell Cross-Talk with a Vascular Niche Maintains Quiescence Via VEGF and Notch Signaling

Overview

Journal Cell Stem Cell

Publisher Cell Press

Specialty Cell Biology

Date 2018 Oct 6

PMID 30290177

Citations 164

Authors

Mayank Verma

Yoko Asakura

Bhavani Sai Rohit Murakonda

Thomas Pengo

Claire Latroche

Benedicte Chazaud

Linda K McLoon

Atsushi Asakura

Affiliations

Soon will be listed here.

Abstract

Skeletal muscle is a complex tissue containing tissue resident muscle stem cells (satellite cells) (MuSCs) important for postnatal muscle growth and regeneration. Quantitative analysis of the biological function of MuSCs and the molecular pathways responsible for a potential juxtavascular niche for MuSCs is currently lacking. We utilized fluorescent reporter mice and muscle tissue clearing to investigate the proximity of MuSCs to capillaries in 3 dimensions. We show that MuSCs express abundant VEGFA, which recruits endothelial cells (ECs) in vitro, whereas blocking VEGFA using both a vascular endothelial growth factor (VEGF) inhibitor and MuSC-specific VEGFA gene deletion reduces the proximity of MuSCs to capillaries. Importantly, this proximity to the blood vessels was associated with MuSC self-renewal in which the EC-derived Notch ligand Dll4 induces quiescence in MuSCs. We hypothesize that MuSCs recruit capillary ECs via VEGFA, and in return, ECs maintain MuSC quiescence though Dll4.

Citing Articles

Physical activity reverses the aging induced decline in angiogenic potential in the fast locomotory muscles of mice.

Zmudzka M, Szramel J, Karasinski J, Nieckarz Z, Zoladz J, Majerczak J Sci Rep. 2025; 15(1):8848.

PMID: 40087472 DOI: 10.1038/s41598-025-93176-1.

Mitochondrial fatty acid oxidation regulates adult muscle stem cell function through modulating metabolic flux and protein acetylation.

Yue F, Gu L, Qiu J, Oprescu S, Beckett L, Ellis J EMBO J. 2025; .

PMID: 40065099 DOI: 10.1038/s44318-025-00397-1.

The role of different physical exercises as an anti-aging factor in different stem cells.

Xu J, Song Z Biogerontology. 2025; 26(2):63.

PMID: 40009244 DOI: 10.1007/s10522-025-10205-2.

Effect of Notch1 signaling on muscle engraftment and maturation from pluripotent stem cells.

Yamashita A, Garay B, Kim H, Bosnakovski D, Abrahante J, Azzag K Stem Cell Reports. 2025; 20(2):102396.

PMID: 39889709 PMC: 11864150. DOI: 10.1016/j.stemcr.2024.102396.

FAPs orchestrate homeostasis of muscle physiology and pathophysiology.

Yin K, Zhang C, Deng Z, Wei X, Xiang T, Yang C FASEB J. 2024; 38(24):e70234.

PMID: 39676717 PMC: 11647758. DOI: 10.1096/fj.202400381R.

References

Madisen L, Zwingman T, Sunkin S, Oh S, Zariwala H, Gu H . A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci. 2009; 13(1):133-40. PMC: 2840225. DOI: 10.1038/nn.2467. View

Asakura A, Seale P, Girgis-Gabardo A, Rudnicki M . Myogenic specification of side population cells in skeletal muscle. J Cell Biol. 2002; 159(1):123-34. PMC: 2173497. DOI: 10.1083/jcb.200202092. View

Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S, Kelly R . Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell. 2009; 16(6):810-21. DOI: 10.1016/j.devcel.2009.05.008. View

Christov C, Chretien F, Abou-Khalil R, Bassez G, Vallet G, Authier F . Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell. 2007; 18(4):1397-409. PMC: 1838982. DOI: 10.1091/mbc.e06-08-0693. View

Tsai P, Kaufhold J, Blinder P, Friedman B, Drew P, Karten H . Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels. J Neurosci. 2009; 29(46):14553-70. PMC: 4972024. DOI: 10.1523/JNEUROSCI.3287-09.2009. View

Pertea M, Kim D, Pertea G, Leek J, Salzberg S . Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016; 11(9):1650-67. PMC: 5032908. DOI: 10.1038/nprot.2016.095. View

Kryvi H . The structure of the myosatellite cells in axial muscles of the shark Geleus melastomus. Anat Embryol (Berl). 1975; 147(1):35-44. DOI: 10.1007/BF00317962. View

Ramilowski J, Goldberg T, Harshbarger J, Kloppmann E, Kloppman E, Lizio M . A draft network of ligand-receptor-mediated multicellular signalling in human. Nat Commun. 2015; 6:7866. PMC: 4525178. DOI: 10.1038/ncomms8866. View

Yaron A, Sprinzak D . The cis side of juxtacrine signaling: a new role in the development of the nervous system. Trends Neurosci. 2012; 35(4):230-9. DOI: 10.1016/j.tins.2011.12.003. View

10.

Mourikis P, Sambasivan R, Castel D, Rocheteau P, Bizzarro V, Tajbakhsh S . A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells. 2011; 30(2):243-52. DOI: 10.1002/stem.775. View

11.

Gerber H, Hillan K, Ryan A, Kowalski J, Keller G, RANGELL L . VEGF is required for growth and survival in neonatal mice. Development. 1999; 126(6):1149-59. DOI: 10.1242/dev.126.6.1149. View

12.

Bjornson C, Cheung T, Liu L, Tripathi P, Steeper K, Rando T . Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells. 2011; 30(2):232-42. PMC: 3384696. DOI: 10.1002/stem.773. View

13.

Morrison S, Spradling A . Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell. 2008; 132(4):598-611. PMC: 4505728. DOI: 10.1016/j.cell.2008.01.038. View

14.

Chakkalakal J, Jones K, Basson M, Brack A . The aged niche disrupts muscle stem cell quiescence. Nature. 2012; 490(7420):355-60. PMC: 3605795. DOI: 10.1038/nature11438. View

15.

Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z . GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009; 10:48. PMC: 2644678. DOI: 10.1186/1471-2105-10-48. View

16.

Rafii S, Kloss C, Butler J, Ginsberg M, Gars E, Lis R . Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood. 2012; 121(5):770-80. DOI: 10.1182/blood-2012-07-444208. View

17.

Bentzinger C, Wang Y, von Maltzahn J, Soleimani V, Yin H, Rudnicki M . Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell. 2013; 12(1):75-87. PMC: 3539137. DOI: 10.1016/j.stem.2012.09.015. View

18.

Keefe A, Lawson J, Flygare S, Fox Z, Colasanto M, Mathew S . Muscle stem cells contribute to myofibres in sedentary adult mice. Nat Commun. 2015; 6:7087. PMC: 4435732. DOI: 10.1038/ncomms8087. View

19.

Verma M, Asakura Y, Hirai H, Watanabe S, Tastad C, Fong G . Flt-1 haploinsufficiency ameliorates muscular dystrophy phenotype by developmentally increased vasculature in mdx mice. Hum Mol Genet. 2010; 19(21):4145-59. PMC: 2951865. DOI: 10.1093/hmg/ddq334. View

20.

Krauss R, Joseph G, Goel A . Keep Your Friends Close: Cell-Cell Contact and Skeletal Myogenesis. Cold Spring Harb Perspect Biol. 2017; 9(2). PMC: 5287076. DOI: 10.1101/cshperspect.a029298. View