Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers

Development

Volumn 138, Issue 21, 2011, Pages 4609-4619

  Fukada, So Ichiro ^a   Yamaguchi, Masahiko ^a   Kokubo, Hiroki ^b   Ogawa, Ryo ^a   Uezumi, Akiyoshi ^c   Yoneda, Tomohiro ^a   Matev, Miroslav M ^a   Motohashi, Norio ^d   Ito, Takahito ^a   Zolkiewska, Anna ^e   Johnson, Randy L ^f   Saga, Yumiko ^b   Miyagoe Suzuki, Yuko ^d   Tsujikawa, Kazutake ^a   Takeda, Shin'ichi ^d   Yamamoto, Hiroshi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c FUJITA HEALTH UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^e KANSAS STATE UNIVERSITY   (United States)

^f UNIVERSITY OF TEXAS   (United States)

Author keywords

Hesr1 (Hey1); Hesr3 (Heyl); Mouse; Satellite cells; Undifferentiated quiescent state

Indexed keywords

KI 67 ANTIGEN; MYOD PROTEIN; MYOGENIN; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL COUNT; CELL DEATH; CELL DIFFERENTIATION; GENE; HESR1 GENE; HESR3 GENE; MOUSE; MUSCLE MASS; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; REGENERATIVE ABILITY; SATELLITE CELL; SKELETAL MUSCLE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL MARKERS; BODY WEIGHT; CELL COUNT; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; ORGAN SIZE; PHENOTYPE; SATELLITE CELLS, SKELETAL MUSCLE;

MUS;

EID: 80053977519     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.067165     Document Type: Article

References (40)

1. Asakura, A., Hirai, H., Kablar, B., Morita, S., Ishibashi, J., Piras, B. A., Christ, A. J., Verma, M., Vineretsky, K. A. and Rudnicki, M. A. (2007). Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle. Proc. Natl. Acad. Sci. USA 104, 16552-16557.
2. 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.
3. Buas, M. F., Kabak, S. and Kadesch, T. (2009). Inhibition of myogenesis by Notch: evidence for multiple pathways. J. Cell. Physiol. 218, 84-93.
4. Charge, S. B. and Rudnicki, M. A. (2004). Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238.
5. Conboy, I. M., Conboy, M. J., Smythe, G. M. and Rando, T. A. (2003). Notchmediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577.
6. Dyczynska, E., Sun, D., Yi, H., Sehara-Fujisawa, A., Blobel, C. P. and Zolkiewska, A. (2007). Proteolytic processing of delta-like 1 by ADAM proteases. J. Biol. Chem. 282, 436-444.
7. Fischer, A. and Gessler, M. (2007). Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res. 35, 4583-4596.
8. Fischer, A., Schumacher, N., Maier, M., Sendtner, M. and Gessler, M. (2004). The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911.
9. Fischer, A., Steidl, C., Wagner, T. U., Lang, E., Jakob, P. M., Friedl, P., Knobeloch, K. P. and Gessler, M. (2007). Combined loss of Hey1 and HeyL causes congenital heart defects because of impaired epithelial to mesenchymal transition. Circ. Res. 100, 856-863.
10. 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.
11. 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.
12. Hirsinger, E., Malapert, P., Dubrulle, J., Delfini, M. C., Duprez, D., Henrique, D., Ish-Horowicz, D. and Pourquie, O. (2001). Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation. Development 128, 107-116.
13. Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K. and Kageyama, R. (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 30, 3489-3498.
14. Joe, A. W., Yi, L., Natarajan, A., Le Grand, F., So, L., Wang, J., Rudnicki, M. A. and Rossi, F. M. (2010). Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12, 153-163.
15. Kadi, F., Charifi, N., Denis, C., Lexell, J., Andersen, J. L., Schjerling, P., Olsen, S. and Kjaer, M. (2005). The behaviour of satellite cells in response to exercise: what have we learned from human studies? Pflugers Arch. 451, 319-327.
16. Kageyama, R., Ohtsuka, T. and Tomita, K. (2000). The bHLH gene Hes1 regulates differentiation of multiple cell types. Mol. Cells 10, 1-7.
17. Kokubo, H., Miyagawa-Tomita, S. and Johnson, R. L. (2005a). Hesr, a mediator of the Notch signaling, functions in heart and vessel development. Trends Cardiovasc. Med. 15, 190-194.
18. Kokubo, H., Miyagawa-Tomita, S., Nakazawa, M., Saga, Y. and Johnson, R. L. (2005b). Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev. Biol. 278, 301-309.
19. Kuang, S., Charge, S. B., Seale, P., Huh, M. and Rudnicki, M. A. (2006). Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J. Cell Biol. 172, 103-113.
20. 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.
21. Kuroda, K., Tani, S., Tamura, K., Minoguchi, S., Kurooka, H. and Honjo, T. (1999). Delta-induced Notch signaling mediated by RBP-J inhibits MyoD expression and myogenesis. J. Biol. Chem. 274, 7238-7244.
22. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973.
23. Leimeister, C., Externbrink, A., Klamt, B. and Gessler, M. (1999). Hey genes: a novel subfamily of hairy- and Enhancer of split related genes specifically expressed during mouse embryogenesis. Mech. Dev. 85, 173-177.
24. 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.
25. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493-495.
26. Megeney, L. A., Kablar, B., Garrett, K., Anderson, J. E. and Rudnicki, M. A. (1996). MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10, 1173-1183.
27. Moss, F. P. and Leblond, C. P. (1971). Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 170, 421-435.
28. Nakagawa, O., Nakagawa, M., Richardson, J. A., Olson, E. N. and Srivastava, D. (1999). HRT1, HRT2, and HRT3: a new subclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev. Biol. 216, 72-84.
29. Pallafacchina, G., Francois, S., Regnault, B., Czarny, B., Dive, V., Cumano, A., Montarras, D. and Buckingham, M. (2010). An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res. 4, 77-91.
30. Sabourin, L. A. and Rudnicki, M. A. (2000). The molecular regulation of myogenesis. Clin. Genet. 57, 16-25.
31. Schultz, E., Gibson, M. C. and Champion, T. (1978). Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J. Exp. Zool. 206, 451-456.
32. Schuster-Gossler, K., Cordes, R. and Gossler, A. (2007). Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc. Natl. Acad. Sci. USA 104, 537-542.
33. 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.
34. Segawa, M., Fukada, S., Yamamoto, Y., Yahagi, H., Kanematsu, M., Sato, M., Ito, T., Uezumi, A., Hayashi, S., Miyagoe-Suzuki, Y. et al. (2008). Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp. Cell Res. 314, 3232-3244.
35. Uezumi, A., Ojima, K., Fukada, S., Ikemoto, M., Masuda, S., Miyagoe-Suzuki, Y. and Takeda, S. (2006). Functional heterogeneity of side population cells in skeletal muscle. Biochem. Biophys. Res. Commun. 341, 864-873.
36. Uezumi, A., Fukada, S., Yamamoto, N., Takeda, S. and Tsuchida, K. (2010). Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12, 143-152.
37. Vasyutina, E., Lenhard, D. C., Wende, H., Erdmann, B., Epstein, J. A. and Birchmeier, C. (2007). RBP-J (Rbpsuh) is essential to maintain muscle progenitor cells and to generate satellite cells. Proc. Natl. Acad. Sci. USA 104, 4443-4448.
38. White, R. B., Bierinx, A. S., Gnocchi, V. F. and Zammit, P. S. (2010). Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev. Biol. 10, 21.
39. 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.
40. Zhang, K., Sha, J. and Harter, M. L. (2010). Activation of Cdc6 by MyoD is associated with the expansion of quiescent myogenic satellite cells. J. Cell Biol. 188, 39-48.