Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors

Journal of Cell Science

Volumn 123, Issue 15, 2010, Pages 2632-2639

  Young, Arthur P ^a,b,c   Wagers, Amy J ^a,b  

^a JOSLIN DIABETES CENTER   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

C2C12; Muscle stem cells; Myogenic differentiation; Myogenic regulatory factors; Pax3; Pax7; Satellite cells

Indexed keywords

MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIC FACTOR 4; MYOGENIC FACTOR 5; MYOGENIN; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; POSTNATAL GROWTH; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; STEM CELL; TRANSCRIPTION REGULATION; UPREGULATION;

CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MUSCLE, SKELETAL; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; MYOGENIC REGULATORY FACTORS; MYOGENIN; PAIRED BOX TRANSCRIPTION FACTORS; POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 77955384142     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.061606     Document Type: Article

References (47)

1. Bajard, L., Relaix, F., Lagha, M., Rocancourt, D., Daubas, P. and Buckingham, M. E. (2006). A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 20, 2450-2464. (Pubitemid 44320392)
2. Berkes, C. A. and Tapscott, S. J. (2005). MyoD and the transcriptional control of myogenesis. Semin. Cell Dev. Biol. 16, 585-595.
3. Borycki, A. G., Li, J., Jin, F., Emerson, C. P. and Epstein, J. A. (1999). Pax3 functions in cell survival and in pax7 regulation. Development 126, 1665-1674. (Pubitemid 29204331)
4. Boutet, S. C., Disatnik, M. H., Chan, L. S., Iori, K. and Rando. T. A. (2007). Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130, 349-362. (Pubitemid 47081135)
5. Braun, T., Rudnicki, M. A., Arnold, H. H. and Jaenisch, R. (1992). Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369-382.
6. Brzóska, E., Przewozniak, M., Grabowska, I., Janczyk-Ilach, K. and Maraczewski, J. (2009). Pax3 and Pax7 expression during myoblast differentiation in vitro and fast and slow muscle regeneration in vivo. Cell Biol. Int. 33, 483-492.
7. Buckingham, M. and Relaix, F. (2007). The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu. Rev. Cell Dev. Biol. 23, 645-673.
8. Buckingham, M., Bajard, L., Chang, T., Daubas, P., Hadchouel, J., Meilhac, S., Montarras, D., Rocancourt, D. and Relaix, F. (2002). The formation of skeletal muscle: from somite to limb. J. Anat. 202, 59-68.
9. Cerletti, M., Jurga, S., Witczak, C. A., Hirshman, M. F., Shadrach, J. L., Goodyear, L. J. and Wagers, A. J. (2008). Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134, 37-47.
10. Conboy, I. M. and Rando, T. A. (2002). The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3, 397-409.
11. Darabi, R., Gehlbach, K., Bachoo, R. M., Kamath, S., Osawa, M., Kamm, K. E., Kyba, M. and Perlingeiro, R. C. (2008). Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat. Med. 14, 134-143. (Pubitemid 351214552)
12. Epstein, J. A., Lam, P., Jepeal, L., Maas, R. L. and Shapiro, D. N. (1995). Pax3 inhibits myogenic differentiation of cultured myoblast cells. J. Biol. Chem. 270, 11719-11722.
13. Epstein, J. A., Shapiro, D. N., Cheng, J., Lam, P. Y. and Maas, R. L. (1996). Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc. Natl. Acad. Sci. USA 93, 4213-4218.
14. Franz, T., Kothary, R., Surani, M. A., Halata, Z. and Grim, M. (1993). The Splotch mutation interferes with muscle development in the limbs. Anat. Embryol. 187, 153-160. (Pubitemid 23063315)
15. Fux, C., Langer, D. and Fussenegger, M. (1994). Dual-regulated myoD- and msx1-based interventions in C2C12-derived cells enable precise myogenic/osteogenic/adipogenic lineage control. J. Gene Med. 6, 1159-1169.
16. Gruss, P. and Walther, C. (1992). Pax in development. Cell 69, 719-722.
17. Hasty, P., Bradley, A., Morris, J. H., Edmondson, D. G., Venuti, J. M., Olson, E. N. and Klein, W. H. (1993). Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506.
18. Hu, P., Geles, K. G., Paik, J. H., DePinho, R. A. and Tjian, R. (2008). Codependent activators direct myoblast-specific MyoD transcription. Dev. Cell 15, 534-546.
19. Jostes, B., Walter, C. and Gruss, P. (1990). The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system. Mech. Dev. 33, 27-37.
20. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., Rocancourt, D., Buckingham, M., Shinin, V. and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431, 466-471. (Pubitemid 39329587)
21. Koblar, S. A., Murphy, M., Barrett, G. L., Underhill, A., Gros, P. and Bartlett, P. F. (1999). Pax-3 regulates neurogenesis in neural crest-derived precursor cells. J. Neurosci. Res. 56, 518-530.
22. Kuang, S., Chargé, S. B., Seale, P., Huh, M. and Rudnicki, M. A. (2006). Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 176, 103-113.
23. Kumar, D., Shadrach, J. L., Wagers, A. J. and Lassar, A. B. (2009). Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells. Mol. Biol. Cell 20, 3170-3177.
24. Lagha, M., Sato, T., Bajard, L., Daubas, P., Esner, M., Montarras, D., Relaix, F. and Buckingham, M. (2008). Regulation of skeletal muscle stem cell behavior by Pax3 and Pax7. Cold Spring Harbor Symp. Quant. Biol. 73, 1-9.
25. Lepper, C., Conway, S. J. and Fan, C. M. (2009). Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627-631.
26. Mancini, A., El Bounkari, O., Norrenbrock, A. F., Scherr, M., Schaefer, D., Eder, M., Banham, A. H., Pulford, K., Lyne, L., Whetton, A. D. et al. (2007). FMIP controls the adipocyte lineage commitment of C2C12 cells by downmodulation of C/EBP alpha. Oncogene 26, 1020-1027.
27. Maroto, M., Reshef, R., Münsterberg, A. E., Koester, S., Goulding, M. and Lassar, A. B. (1997). Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139-148. (Pubitemid 27180593)
28. McKinnell, I. W., Ishibashi, J., Le Grand, F., Punch, V. G., Addicks, G. C., Greenblatt, J. F., Dilworth, F. J. and Rudnicki, M. A. (2007). Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat. Cell Biol. 10, 77-84.
29. Nabeshima, Y., Hanaoka, K., Hayasaka, M., Esumi, E., Li, S., Nonaka, I. and Nabeshima, Y. (1993). Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532-535.
30. 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.
31. Olguin, H. C., Yang, Z., Tapscott, S. J. and Olwin, B. B. (2007). Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J. Cell Biol. 177, 169-179.
32. Ott, M.-O., Bober, E., Lyons, G., Arnold, H. and Buckingham, M. (1991). Early expression of the myogenic regulatory gene, Myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097-1107. (Pubitemid 21900264)
33. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2004). Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev. 18, 1088-1105.
34. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2005). A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953. (Pubitemid 40896320)
35. Relaix, F., Montarras, D., Zaffran, S., Gayraud-Morel, B., Rocancourt, D., Tajbakhsh, S., Mansouri, A., Cumano, A. and Buckingham, M. (2006). Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172, 92-101.
36. Ridgeway, A. G. and Skerjanc, I. S. (2001). Pax3 is essential for skeletal myogenesis and the expression of Six1 and Eya2. J. Biol. Chem. 276, 19033-19039.
37. Rudnicki, M. A., Braun, T., Hinuma, S. and Jaenisch, R. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390.
38. Rudnicki, M. A., Schnegelsberg, P. N. J., Stead, R. H., Braun, T., Arnold, H. H., Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359. (Pubitemid 24021909)
39. 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.
40. 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.
41. Sherwood, R. I., Christensen, J. L., Conboy, I. M., Conboy, M. J., Rando, T. A., Weissman, I. L. and Wagers, A. J. (2004). Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 119, 543-554.
42. Springer, M. L., Ozawa, C. R. and Blau, H. M. (2002). Transient production of alpha-smooth muscle actin by skeletal myoblasts during differentiation in culture and following intramuscular implantation. Cell Motil. Cytoskeleton 51, 177-186.
43. Tajbakhsh, S., Rocancourt, D., Cossu, G. and Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127-138. (Pubitemid 27180592)
44. Tremblay, P. and Gruss, P. (1994). Pax: genes for mice and men. Pharmacol. Ther. 61, 205-226.
45. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T. K., Turner, D., Rupp, R., Hollenberg, S. et al. (1991). The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766.
46. Williams, B. A. and Ordahl, C. P. (1994). Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 120, 785-796.
47. Zammit, P. S., Relaix, F., Nagata, Y., Ruiz, A. P., Collins, C. A., Partridge, T. A. and Beauchamp, J. R. (2006). Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119, 1824-1832.