Muscle stem cells at a glance

Journal of Cell Science

Volumn 127, Issue 21, 2014, Pages 4543-4548

  Wang, Yu Xin ^a,b   Dumont, Nicolas A ^a,b   Rudnicki, Michael A ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Regeneration; Satellite cells; Skeletal muscle; Stem cells; Therapy

Indexed keywords

CELL MARKER; TRANSCRIPTION FACTOR PAX7;

ADULT STEM CELL; ARTICLE; CELL RENEWAL; CELL THERAPY; HUMAN; IN VITRO STUDY; MUSCLE DEVELOPMENT; MUSCLE STEM CELL; NONHUMAN; TISSUE REGENERATION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; PHYSIOLOGY; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; IMMUNOHISTOCHEMISTRY; MICE; MUSCLE, SKELETAL; PAX7 TRANSCRIPTION FACTOR; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELLS;

EID: 84913559641     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.151209     Document Type: Article

References (65)

1. 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.
2. Bentzinger, C. F.,Wang, Y. X. and Rudnicki, M. A. (2012). Buildingmuscle: molecular regulation of myogenesis. Cold Spring Harb. Perspect. Biol. 4, a008342.
3. Bentzinger, C. F., Wang, Y. X., von Maltzahn, J., Soleimani, V. D., Yin, H. and Rudnicki, M. A. (2013). Fibronectin regulates Wnt7a signaling and satellite cell expansion. Cell Stem Cell 12, 75-87.
4. Bentzinger, C. F., von Maltzahn, J., Dumont, N. A., Stark, D. A., Wang, Y. X., Nhan, K., Frenette, J., Cornelison, D. D. and Rudnicki, M. A. (2014). Wnt7a stimulates myogenic stem cell motility and engraftment resulting in improved muscle strength. J. Cell Biol. 205, 97-111.
5. Bjornson, C. R. R., Cheung, T. H., Liu, L., Tripathi, P. V., Steeper, K. M. and Rando, T. A. (2012). Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30, 232-242.
6. Bouchentouf, M., Benabdallah, B. F., Bigey, P., Yau, T. M., Scherman, D. and Tremblay, J. P. (2008). Vascular endothelial growth factor reduced hypoxiainduced death of human myoblasts and improved their engraftment in mouse muscles. Gene Ther. 15, 404-414.
7. Cao, Y., Zhao, Z., Gruszczynska-Biegala, J. and Zolkiewska, A. (2003). Role of metalloprotease disintegrin ADAM12 in determination of quiescent reserve cells during myogenic differentiation in vitro. Mol. Cell. Biol. 23, 6725-6738.
8. Chakkalakal, J. V., Jones, K. M., Basson, M. A. and Brack, A. S. (2012). The aged niche disrupts muscle stem cell quiescence. Nature 490, 355-360.
9. Chakkalakal, J. V., Christensen, J., Xiang, W., Tierney, M. T., Boscolo, F. S., Sacco, A. and Brack, A. S. (2014). Early forming label-retaining muscle stem cells require p27kip1 for maintenance of the primitive state. Development 141, 1649-1659.
10. Cheung, T. H. and Rando, T. A. (2013). Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14, 329-340.
11. Cheung, T. H., Quach, N. L., Charville, G. W., Liu, L., Park, L., Edalati, A., Yoo, B., Hoang, P. and Rando, T. A. (2012). Maintenance of muscle stem-cell quiescence by microRNA-489. Nature 482, 524-528.
12. 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.
13. Crist, C. G., Montarras, D. and Buckingham, M. (2012). Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of MYF5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11, 118-126.
14. Darabi, R., Santos, F. N. C., Filareto, A., Pan, W., Koene, R., Rudnicki, M. A., Kyba, M. and Perlingeiro, R. C. R. (2011). Assessment of the myogenic stem cell compartment following transplantation of Pax3/Pax7-induced embryonic stem cell-derived progenitors. Stem Cells 29, 777-790.
15. DiMario, J., Buffinger, N., Yamada, S. and Strohman, R. C. (1989). Fibroblast growth factor in the extracellular matrix of dystrophic (mdx) mouse muscle. Science 244, 688-690.
16. Faralli, H. and Dilworth, F. J. (2012). Turning on myogenin in muscle: a paradigm for understanding mechanisms of tissue-specific gene expression. Comp. Funct. Genomics 2012, 836374.
17. Fukada, S., Higuchi, S., Segawa, M., Koda, K., Yamamoto, Y., Tsujikawa, K., Kohama, Y., Uezumi, A., Imamura, M., Miyagoe-Suzuki, Y. et al. (2004). Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp. Cell Res. 296, 245-255.
18. Fukada, S., Uezumi, A., Ikemoto, M., Masuda, S., Segawa, M., Tanimura, N., Yamamoto, H., Miyagoe-Suzuki, Y. and Takeda, S. (2007). Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25, 2448-2459.
19. Fukada, S., Yamaguchi, M., Kokubo, H., Ogawa, R., Uezumi, A., Yoneda, T., Matev, M. M., Motohashi, N., Ito, T., Zolkiewska, A. et al. (2011). Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development 138, 4609-4619.
20. Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E. G., Sacco, A., Leonardi, N. A., Kraft, P., Nguyen, N. K., Thrun, S., Lutolf, M. P. and Blau, H. M. (2010). Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081.
21. Gnocchi, V. F., White, R. B., Ono, Y., Ellis, J. A. and Zammit, P. S. (2009). Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS ONE 4, e5205.
22. Gopinath, S. D., Webb, A. E., Brunet, A. and Rando, T. A. (2014). FOXO3 Promotes Quiescence in Adult Muscle Stem Cells during the Process of Self-Renewal. Stem Cell Reports 2, 414-426.
23. Günther, S., Kim, J., Kostin, S., Lepper, C., Fan, C.-M. and Braun, T. (2013). MYF5-positive satellite cells contribute to Pax7-dependent long-term maintenance of adult muscle stem cells. Cell Stem Cell 13, 590-601.
24. Hannon, K., Kudla, A. J., McAvoy, M. J., Clase, K. L. and Olwin, B. B. (1996). Differentially expressed fibroblast growth factors regulate skeletal muscle development through autocrine and paracrine mechanisms. J. Cell Biol. 132, 1151-1159.
25. Huard, J., Bouchard, J. P., Roy, R., Malouin, F., Dansereau, G., Labrecque, C., Albert, N., Richards, C. L., Lemieux, B. and Tremblay, J. P. (1992). Human myoblast transplantation: preliminary results of 4 cases. Muscle Nerve 15, 550-560.
26. Jones, N. C., Tyner, K. J., Nibarger, L., Stanley, H. M., Cornelison, D. D. W., Fedorov, Y. V. and Olwin, B. B. (2005). The p38alpha/beta MAPK functions as a molecular switch to activate the quiescent satellite cell. J. Cell Biol. 169, 105-116.
27. Kästner, S., Elias, M. C., Rivera, A. J. and Yablonka-Reuveni, Z. (2000). Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J. Histochem. Cytochem. 48, 1079-1096.
28. Kawabe, Y., Wang, Y. X., McKinnell, I. W., Bedford, M. T. and Rudnicki, M. A. (2012). Carm1 regulates Pax7 transcriptional activity through MLL1/2 recruitment during asymmetric satellite stem cell divisions. Cell Stem Cell 11, 333-345.
29. Kuang, S., Kuroda, K., Le Grand, F. and Rudnicki, M. A. (2007). Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129, 999-1010.
30. Kuang, S., Gillespie, M. A. and Rudnicki, M. A. (2008). Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2, 22-31.
31. Lafreniere, J.-F., Caron, M.-C., Skuk, D., Goulet, M., Cheikh, A. R. and Tremblay, J. P. (2009). Growth factor coinjection improves the migration potential of monkey myogenic precursors without affecting cell transplantation success. Cell Transplant. 18, 719-730.
32. Latil, M., Rocheteau, P., Châtre, L., Sanulli, S., Mémet, S., Ricchetti, M., Tajbakhsh, S. and Chrétien, F. (2012). Skeletal muscle stem cells adopt a dormant cell state post mortem and retain regenerative capacity. Nat. Commun. 3, 903.
33. Le Grand, F., Jones, A. E., Seale, V., Scimè, A. and Rudnicki, M. A. (2009). Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4, 535-547.
34. Lepper, C., Partridge, T. A. and Fan, C.-M. (2011). An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138, 3639-3646.
35. Lipton, B. H. and Schultz, E. (1979). Developmental fate of skeletal muscle satellite cells. Science 205, 1292-1294.
36. Mann, C. J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A. L. and Muñoz-Cánoves, P. (2011). Aberrant repair and fibrosis development in skeletal muscle. Skelet. Muscle 1, 21.
37. Manzur, A. Y., Kuntzer, T., Pike, M. and Swan, A. V. (1996). Glucocorticoid corticosteroids for Duchenne muscular dystrophy. In Cochrane Database of Systematic Reviews. New York, NY: John Wiley & Sons, Ltd.
38. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493-495.
39. McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., Srikuea, R., Lawson, B. A., Grimes, B., Keller, C. et al. (2011). Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138, 3657-3666.
40. McKinnell, I. W., Ishibashi, J., Le Grand, F., Punch, V. G. J., Addicks, G. C., Greenblatt, J. F., Dilworth, F. J. and Rudnicki, M. A. (2008). Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat. Cell Biol. 10, 77-84.
41. Moncaut, N., Rigby, P. W. J. and Carvajal, J. J. (2013). Dial M(RF) for myogenesis. FEBS J. 280, 3980-3990.
42. Morgan, J., Rouche, A., Bausero, P., Houssaïni, A., Gross, J., Fiszman, M. Y. and Alameddine, H. S. (2010). MMP-9 overexpression improves myogenic cell migration and engraftment. Muscle Nerve 42, 584-595.
43. Murphy, M. M., Lawson, J. A., Mathew, S. J., Hutcheson, D. A. and Kardon, G. (2011). Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 138, 3625-3637.
44. Ono, Y., Masuda, S., Nam, H.-S., Benezra, R., Miyagoe-Suzuki, Y. and Takeda, S. (2012). Slow-dividing satellite cells retain long-term self-renewal ability in adult muscle. J. Cell Sci. 125, 1309-1317.
45. Partridge, T. A. and Sloper, J. C. (1977). A host contribution to the regeneration of muscle grafts. J. Neurol. Sci. 33, 425-435.
46. Partridge, T. A., Grounds, M. and Sloper, J. C. (1978). Evidence of fusion between host and donor myoblasts in skeletal muscle grafts. Nature 273, 306-308.
47. Partridge, T. A., Morgan, J. E., Coulton, G. R., Hoffman, E. P. and Kunkel, L. M. (1989). Conversion of mdx myofibres from dystrophin-negative to-positive by injection of normal myoblasts. Nature 337, 176-179.
48. Pasut, A., Oleynik, P. and Rudnicki, M. A. (2012). Isolation of muscle stem cells by fluorescence activated cell sorting cytometry. Methods Mol. Biol. 798, 53-64.
49. Punch, V. G., Jones, A. E. and Rudnicki, M. A. (2009). Transcriptional networks that regulate muscle stem cell function. Wiley Interdiscip. Rev. Syst. Biol. Med. 1, 128-140.
50. Rocheteau, P., Gayraud-Morel, B., Siegl-Cachedenier, I., Blasco, M. A. and Tajbakhsh, S. (2012). A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell 148, 112-125.
51. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S. and Blau, H. M. (2008). Selfrenewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506.
52. Sambasivan, R., Yao, R., Kissenpfennig, A., Van Wittenberghe, L., Paldi, A., Gayraud-Morel, B., Guenou, H., Malissen, B., Tajbakhsh, S. and Galy, A. (2011). Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138, 3647-3656.
53. Schultz, E. (1996). Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 175, 84-94.
54. Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P. and Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777-786.
55. 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 selfrenewing adult muscle stem cell pool during regeneration. Cell Stem Cell 6, 117-129.
56. Shinin, V., Gayraud-Morel, B., Gomés, D. and Tajbakhsh, S. (2006). Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat. Cell Biol. 8, 677-682.
57. Snow, M. H. (1978). An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscles in young rats. Cell Tissue Res. 186, 535-540.
58. Soleimani, V. D., Yin, H., Jahani-Asl, A., Ming, H., Kockx, C. E. M., van Ijcken, W. F. J., Grosveld, F. and Rudnicki, M. A. (2012). Snail regulates MyoD binding-site occupancy to direct enhancer switching and differentiation-specific transcription in myogenesis. Mol. Cell 47, 457-468.
59. Troy, A., Cadwallader, A. B., Fedorov, Y., Tyner, K., Tanaka, K. K. and Olwin, B. B. (2012). Coordination of satellite cell activation and self-renewal by Parcomplex-dependent asymmetric activation of p38a/b MAPK. Cell Stem Cell 11, 541-553.
60. Urciuolo, A., Quarta, M., Morbidoni, V., Gattazzo, F., Molon, S., Grumati, P., Montemurro, F., Tedesco, F. S., Blaauw, B., Cossu, G. et al. (2013). Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat. Commun. 4, 1964.
61. von Maltzahn, J., Jones, A. E., Parks, R. J. and Rudnicki, M. A. (2013). Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc. Natl. Acad. Sci. USA 110, 16474-16479.
62. Wang, Y. X. and Rudnicki, M. A. (2012). Satellite cells, the engines of muscle repair. Nat. Rev. Mol. Cell Biol. 13, 127-133.
63. Wang, Y. X., Bentzinger, C. F. and Rudnicki, M. A. (2013). Treating muscular dystrophy by stimulating intrinsic repair. Regen. Med. 8, 237-240.
64. Wen, Y., Bi, P., Liu, W., Asakura, A., Keller, C. and Kuang, S. (2012). Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol. Cell. Biol. 32, 2300-2311.
65. Yablonka-Reuveni, Z., Seger, R. and Rivera, A. J. (1999). Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J. Histochem. Cytochem. 47, 23-42.