Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells

Molecular Biology of the Cell

Volumn 20, Issue 14, 2009, Pages 3170-3177

  Kumar, Deepak ^a   Shadrach, Jennifer L ^b,c   Wagers, Amy J ^b,c   Lassar, Andrew B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOSLIN DIABETES CENTER   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA; LUCIFERASE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CULTURE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; DNA BINDING; GENE; GENE EXPRESSION; ID3 GENE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SATELLITE CELL; SKELETAL MUSCLE; STEM CELL;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INHIBITOR OF DIFFERENTIATION PROTEINS; LUCIFERASES; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PAIRED BOX TRANSCRIPTION FACTORS; PAX7 TRANSCRIPTION FACTOR; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA, SMALL INTERFERING; SATELLITE CELLS, SKELETAL MUSCLE; TRANSCRIPTION, GENETIC;

EID: 67749132526     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-12-1185     Document Type: Article

References (35)

1. Attema, J. L., Papathanasiou, P., Forsberg, E. C., Xu, J., Smale, S. T., and Weissman, I. L. (2007). Epigenetic characterization of hematopoietic stem cell differentiation using miniChIP and bisulfite sequencing analysis. Proc. Natl. Acad. Sci. USA 104, 12371-12376.
2. Bai, G., Sheng, N., Xie, Z., Bian, W., Yokota, Y., Benezra, R., Kageyama, R., Guillemot, F., and Jing, N. (2007). Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev. Cell 13, 283-297.
3. 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.
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. 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.
6. Chalepakis, G., Goulding, M., Read, A., Strachan, T., and Gruss, P. (1994). Molecular basis of splotch and Waardenburg Pax-3 mutations. Proc. Natl. Acad. Sci. USA 91, 3685-3689.
7. Chalepakis, G., and Gruss, P. (1995). Identification of DNA recognition sequences for the Pax3 paired domain. Gene 162, 267-270.
8. 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.
9. 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.
10. Gros, J., Manceau, M., Thome, V., and Marcelle, C. (2005). A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435, 954-958.
11. 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.
12. Jankovic, V., Ciarrocchi, A., Boccuni, P., DeBlasio, T., Benezra, R., and Nimer, S. D. (2007). Id1 restrains myeloid commitment, maintaining the self-renewal capacity of hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 104, 1260-1265.
13. Kassar-Duchossoy, L., Giacone, E., Gayraud-Morel, B., Jory, A., Gomes, D., and Tajbakhsh, S. (2005). Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19, 1426-1431.
14. 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.
15. Lagha, M., Kormish, J. D., Rocancourt, D., Manceau, M., Epstein, J. A., Zaret, K. S., Relaix, F., and Buckingham, M. E. (2008). Pax3 regulation of FGF signaling affects the progression of embryonic progenitor cells into the myogenic program. Genes Dev. 22, 1828-1837.
16. Maroto, M., Reshef, R., Munsterberg, 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.
17. McKinnell, I. W., Ishibashi, J., Le Grand, F., Punch, V. G., 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.
18. 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.
19. Munsterberg, A. E., Kitajewski, J., Bumcrot, D. A., McMahon, A. P., and Lassar, A. B. (1995). Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911-2922.
20. Nakatani, Y., and Ogryzko, V. (2003). Immunoaffinity purification of mammalian protein complexes. Methods Enzymol. 370, 430-444.
21. 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, 769-779.
22. Pan, L., Sato, S., Frederick, J. P., Sun, X. H., and Zhuang, Y. (1999). Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Mol. Cell Biol. 19, 5969-5980.
23. Perk, J., Iavarone, A., and Benezra, R. (2005). Id family of helix-loop-helix proteins in cancer. Nat. Rev. Cancer 5, 603-614.
24. Relaix, F., Polimeni, M., Rocancourt, D., Ponzetto, C., Schafer, B. W., and Buckingham, M. (2003). The transcriptional activator PAX3-FKHR rescues the defects of Pax3 mutant mice but induces a myogenic gain-of-function phenotype with ligand-independent activation of Met signaling in vivo. Genes Dev. 17, 2950-2965.
25. 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.
26. Relaix, F., Rocancourt, D., Mansouri, A., and Buckingham, M. (2005). A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953.
27. Ruzinova, M. B., and Benezra, R. (2003). Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13, 410-418.
28. Schienda, J., Engleka, K. A., Jun, S., Hansen, M. S., Epstein, J. A., Tabin, C. J., Kunkel, L. M., and Kardon, G. (2006). Somitic origin of limb muscle satellite and side population cells. Proc. Natl. Acad. Sci. USA 103, 945-950.
29. Seale, P., Ishibashi, J., Scime, A., and Rudnicki, M. A. (2004). Pax7 is necessary and sufficient for the myogenic specification of CD45+:Sca1+ stem cells from injured muscle. PLoS Biol. 2, E130.
30. Smith, H. K., Maxwell, L., Rodgers, C. D., McKee, N. H., and Plyley, M. J. (2001). Exercise-enhanced satellite cell proliferation and new myonuclear accretion in rat skeletal muscle. J. Appl. Physiol. 90, 1407-1414.
31. Tajbakhsh, S., Rocancourt, D., Cossu, G., and Buckingham, M. (1997). Rede-fining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127-138.
32. Vasyutina, E., Stebler, J., Brand-Saberi, B., Schulz, S., Raz, E., and Birchmeier, C. (2005). CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev. 19, 2187-2198.
33. Yan, Z., Choi, S., Liu, X., Zhang, M., Schageman, J. J., Lee, S. Y., Hart, R., Lin, L., Thurmond, F. A., and Williams, R. S. (2003). Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278, 8826-8836.
34. Yeh, K., and Lim, R. W. (2000). Genomic organization and promoter analysis of the murine Id3 gene. Gene 254, 163-171.
35. Zammit, P. S., Partridge, T. A., and Yablonka-Reuveni, Z. (2006). The skeletal muscle satellite cell: the stem cell that came in from the cold. J. Histochem. Cytochem. 54, 1177-1191.