Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle

Journal of Cell Science

Volumn 125, Issue 5, 2012, Pages 1309-1317

  Ono, Yusuke ^a   Masuda, Satoru ^a   Nam, Hyung Song ^b   Benezra, Robert ^c   Miyagoe Suzuki, Yuko ^a   Takeda, Shin'ichi ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Myoblasts; Satellite cells; Self renewal; Skeletal muscle; Slow dividing cells; Stemness

Indexed keywords

INHIBITOR OF DIFFERENTIATION 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL DIVISION; CELL FUNCTION; CELL PROLIFERATION; CELL RENEWAL; CELL SUBPOPULATION; COLONY FORMATION; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTER; GENE EXPRESSION PROFILING; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE SATELLITE CELL; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; FLUORESCENT DYES; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MUSCLE FIBERS, SKELETAL; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84861394115     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.096198     Document Type: Article

References (37)

1. Baroffio, A., Hamann, M., Bernheim, L., Bochaton-Piallat, M. L., Gabbiani, G. and Bader, C. R. (1996). Identification of self-renewing myoblasts in the progeny of single human muscle satellite cells. Differentiation 60, 47-57.
2. Beauchamp, J. R., Morgan, J. E., Pagel, C. N. and Partridge, T. A. (1999). Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J. Cell Biol. 144, 1113-1122.
3. Beauchamp, J. R., Heslop, L., Yu, D. S., Tajbakhsh, S., Kelly, R. G., Wernig, A., Buckingham, M. E., Partridge, T. A. and Zammit, P. S. (2000). Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151, 1221-1234.
4. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L. and Weintraub, H. (1990). The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49-59.
5. Biressi, S. and Rando, T. A. (2010). Heterogeneity in the muscle satellite cell population. Semin. Cell. Dev. Biol. 21, 845-854.
6. Cairns, J. (1975). Mutation selection and the natural history of cancer. Nature 255, 197-200.
7. Collins, C. A., Olsen, I., Zammit, P. S., Heslop, L., Petrie, A., Partridge, T. A. and Morgan, J. E. (2005). Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289-301.
8. Conboy, M. J., Karasov, A. O. and Rando, T. A. (2007). High incidence of nonrandom template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol. 5, e102.
9. Cornelison, D. D., Filla, M. S., Stanley, H. M., Rapraeger, A. C. and Olwin, B. B. (2001). Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 239, 79-94.
10. Cornelison, D. D., Wilcox-Adelman, S. A., Goetinck, P. F., Rauvala, H., Rapraeger, A. C. and Olwin, B. B. (2004). Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 18, 2231-2236.
11. Foudi, A., Hochedlinger, K., Van Buren, D., Schindler, J. W., Jaenisch, R., Carey, V. and Hock, H. (2009). Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 27, 84-90.
12. Fuchs, E. (2009). The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137, 811-819.
13. Grifone, R., Demignon, J., Giordani, J., Niro, C., Souil, E., Bertin, F., Laclef, C., Xu, P. X. and Maire, P. (2007). Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo. Dev. Biol. 302, 602-616.
14. Halevy, O., Piestun, Y., Allouh, M. Z., Rosser, B. W., Rinkevich, Y., Reshef, R., Rozenboim, I., Wleklinski-Lee, M. and Yablonka-Reuveni, Z. (2004). Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev. Dyn. 231, 489-502.
15. Hall, J. K., Banks, G. B., Chamberlain, J. S. and Olwin, B. B. (2010). Prevention of muscle aging by myofiber-associated satellite cell transplantation. Sci. Transl. Med. 2, 57ra83.
16. Heanue, T. A., Reshef, R., Davis, R. J., Mardon, G., Oliver, G., Tomarev, S., Lassar, A. B. and Tabin, C. J. (1999). Synergistic regulation of vertebrate muscle development by Dach2, Eya2, and Six1, homologs of genes required for Drosophila eye formation. Genes Dev. 13, 3231-3243.
17. Kuang, S., Kuroda, K., Le Grand, F. and Rudnicki, M. A. (2007). Asymmetric selfrenewal and commitment of satellite stem cells in muscle. Cell 129, 999-1010.
18. Miao, H., Li, D. Q., Mukherjee, A., Guo, H., Petty, A., Cutter, J., Basilion, J. P., Sedor, J., Wu, J., Danielpour, D. et al. (2009). EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 16, 9-20.
19. Montarras, D., Morgan, J., Collins, C., Relaix, F., Zaffran, S., Cumano, A., Partridge, T. and Buckingham, M. (2005). Direct isolation of satellite cells for skeletal muscle regeneration. Science 309, 2064-2067.
20. Nam, H. S. and Benezra, R. (2009). High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 5, 515-526.
21. Olguin, H. C. and Olwin, B. B. (2004). Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev. Biol. 275, 375-388.
22. Ono, Y., Gnocchi, V. F., Zammit, P. S. and Nagatomi, R. (2009). Presenilin-1 acts via Id1 to regulate the function of muscle satellite cells in a {gamma}-secretaseindependent manner. J. Cell Sci. 122, 4427-4438.
23. Ono, Y., Boldrin, L., Knopp, P., Morgan, J. E. and Zammit, P. S. (2010). Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev. Biol. 337, 29-41.
24. Ono, Y., Calhabeu, F., Morgan, J. E., Katagiri, T., Amthor, H. and Zammit, P. S. (2011). BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ. 18, 222-234.
25. Rantanen, J., Hurme, T., Lukka, R., Heino, J. and Kalimo, H. (1995). Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab. Invest. 72, 341-347.
26. Rouger, K., Brault, M., Daval, N., Leroux, I., Guigand, L., Lesoeur, J., Fernandez, B. and Cherel, Y. (2004). Muscle satellite cell heterogeneity: in vitro and in vivo evidences for populations that fuse differently. Cell Tissue Res. 317, 319-326.
27. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S. and Blau, H. M. (2008). Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506.
28. Schultz, E. (1996). Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 175, 84-94.
29. Shea, K. L., Xiang, W., LaPorta, V. S., Licht, J. D., Keller, C., Basson, M. A. and Brack, A. S. (2010). Sprouty1 regulates reversible quiescence of a self-renewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6, 117-129.
30. Shinin, V., Gayraud-Morel, B., Gomes, D. and Tajbakhsh, S. (2006). Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat. Cell Biol. 8, 677-687.
31. Tedesco, F. S., Dellavalle, A., Diaz-Manera, J., Messina, G. and Cossu, G. (2010). Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 120, 11-19.
32. Tanaka, K. K., Hall, J. K., Troy, A. A., Cornelison, D. D., Majka, S. M. and Olwin, B. B. (2009). Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4, 217-225.
33. Truitt, L., Freywald, T., DeCoteau, J., Sharfe, N. and Freywald, A. (2010). The EphB6 receptor cooperates with c-Cbl to regulate the behavior of breast cancer cells. Cancer Res. 70, 1141-1153.
34. Wilson, A., Laurenti, E., Oser, G., van der Wath, R. C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C. F., Eshkind, L., Bockamp, E. et al. (2008). Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135, 1118-1129.
35. Yoshida, N., Yoshida, S., Koishi, K., Masuda, K. and Nabeshima, Y. (1998). Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates 'reserve cells'. J. Cell Sci. 111, 769-779.
36. Zammit, P. S. (2008). All muscle satellite cells are equal, but are some more equal than others? J. Cell Sci. 121, 2975-2982.
37. Zammit, P. S., Golding, J. P., Nagata, Y., Hudon, V., Partridge, T. A. and Beauchamp, J. R. (2004). Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166, 347-357.