Asymmetric Self-renewal and Commitment of Satellite Stem Cells in Muscle

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2007 Jun 2

PMID 17540178

Citations 683

Authors

Shihuan Kuang

Kazuki Kuroda

Fabien Le Grand

Michael A Rudnicki

Affiliations

Soon will be listed here.

Abstract

Satellite cells play a central role in mediating the growth and regeneration of skeletal muscle. However, whether satellite cells are stem cells, committed progenitors, or dedifferentiated myoblasts has remained unclear. Using Myf5-Cre and ROSA26-YFP Cre-reporter alleles, we observed that in vivo 10% of sublaminar Pax7-expressing satellite cells have never expressed Myf5. Moreover, we found that Pax7(+)/Myf5(-) satellite cells gave rise to Pax7(+)/Myf5(+) satellite cells through apical-basal oriented divisions that asymmetrically generated a basal Pax7(+)/Myf5(-) and an apical Pax7(+)/Myf5(+) cells. Prospective isolation and transplantation into muscle revealed that whereas Pax7(+)/Myf5(+) cells exhibited precocious differentiation, Pax7(+)/Myf5(-) cells extensively contributed to the satellite cell reservoir throughout the injected muscle. Therefore, we conclude that satellite cells are a heterogeneous population composed of stem cells and committed progenitors. These results provide critical insights into satellite cell biology and open new avenues for therapeutic treatment of neuromuscular diseases.

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References

Megeney L, Kablar B, Garrett K, Anderson J, Rudnicki M . MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 1996; 10(10):1173-83. DOI: 10.1101/gad.10.10.1173. View

Schultz E . Satellite cell proliferative compartments in growing skeletal muscles. Dev Biol. 1996; 175(1):84-94. DOI: 10.1006/dbio.1996.0097. View

Tajbakhsh S, Rocancourt D, Buckingham M . Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature. 1996; 384(6606):266-70. DOI: 10.1038/384266a0. View

Minoguchi S, Taniguchi Y, Kato H, Okazaki T, Strobl L, Zimber-Strobl U . RBP-L, a transcription factor related to RBP-Jkappa. Mol Cell Biol. 1997; 17(5):2679-87. PMC: 232118. DOI: 10.1128/MCB.17.5.2679. View

CARMENA A, Menon D, Jimenez F, Chia W . Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev. 1998; 12(3):304-15. PMC: 316482. DOI: 10.1101/gad.12.3.304. View

Qu Z, Balkir L, van Deutekom J, Robbins P, Pruchnic R, Huard J . Development of approaches to improve cell survival in myoblast transfer therapy. J Cell Biol. 1998; 142(5):1257-67. PMC: 2149359. DOI: 10.1083/jcb.142.5.1257. View

Kuroda K, Tani S, Tamura K, Minoguchi S, Kurooka H, Honjo T . Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J Biol Chem. 1999; 274(11):7238-44. DOI: 10.1074/jbc.274.11.7238. View

Beauchamp J, Morgan J, Pagel C, Partridge T . Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J Cell Biol. 1999; 144(6):1113-22. PMC: 2150577. DOI: 10.1083/jcb.144.6.1113. View

Burkin D, Kaufman S . The alpha7beta1 integrin in muscle development and disease. Cell Tissue Res. 1999; 296(1):183-90. DOI: 10.1007/s004410051279. View

10.

Ben-Yair R, Kalcheim C . Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development. 2005; 132(4):689-701. DOI: 10.1242/dev.01617. View

11.

Conboy I, Conboy M, Wagers A, Girma E, Weissman I, Rando T . Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 2005; 433(7027):760-4. DOI: 10.1038/nature03260. View

12.

Relaix F, Rocancourt D, Mansouri A, Buckingham M . A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature. 2005; 435(7044):948-53. DOI: 10.1038/nature03594. View

13.

Gros J, Manceau M, Thome V, Marcelle C . A common somitic origin for embryonic muscle progenitors and satellite cells. Nature. 2005; 435(7044):954-8. DOI: 10.1038/nature03572. View

14.

Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S . Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 2005; 19(12):1426-31. PMC: 1151658. DOI: 10.1101/gad.345505. View

15.

Venters S, Ordahl C . Asymmetric cell divisions are concentrated in the dermomyotome dorsomedial lip during epaxial primary myotome morphogenesis. Anat Embryol (Berl). 2005; 209(6):449-60. DOI: 10.1007/s00429-005-0461-2. View

16.

Collins C, Olsen I, Zammit P, Heslop L, Petrie A, Partridge T . Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005; 122(2):289-301. DOI: 10.1016/j.cell.2005.05.010. View

17.

Lechler T, Fuchs E . Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature. 2005; 437(7056):275-80. PMC: 1399371. DOI: 10.1038/nature03922. View

18.

Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A . Direct isolation of satellite cells for skeletal muscle regeneration. Science. 2005; 309(5743):2064-7. DOI: 10.1126/science.1114758. View

19.

McKinnell I, Parise G, Rudnicki M . Muscle stem cells and regenerative myogenesis. Curr Top Dev Biol. 2005; 71:113-30. DOI: 10.1016/S0070-2153(05)71004-8. View

20.

Yablonka-Reuveni Z, Anderson J . Satellite cells from dystrophic (mdx) mice display accelerated differentiation in primary cultures and in isolated myofibers. Dev Dyn. 2005; 235(1):203-12. DOI: 10.1002/dvdy.20602. View