Doublecortin marks a new population of transiently amplifying muscle progenitor cells and is required for myofiber maturation during skeletal muscle regeneration

Development (Cambridge)

Volumn 142, Issue 1, 2015, Pages 51-61

  Ogawa, Ryo ^a   Ma, Yuran ^a   Yamaguchi, Masahiko ^a   Ito, Takahito ^a   Watanabe, Yoko ^a   Ohtani, Takuji ^a   Murakami, Satoshi ^a   Uchida, Shizuka ^b   De Gaspari, Piera ^c   Uezumi, Akiyoshi ^d   Nakamura, Miki ^a   Miyagoe Suzuki, Yuko ^e   Tsujikawa, Kazutake ^a   Hashimoto, Naohiro ^f   Braun, Thomas ^c   Tanaka, Teruyuki ^g   Takeda, Shin’Ichi ^e   Yamamoto, Hiroshi ^a   Fukada, So Ichiro ^a  

^a OSAKA UNIVERSITY   (Japan)

^b GOETHE UNIVERSITY   (Germany)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^d FUJITA HEALTH UNIVERSITY   (Japan)

^e NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^f NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

Author keywords

Doublecortin; Myofiber maturation; Regeneration; Satellite cells

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; COMPLEMENTARY DNA; DOUBLECORTIN; RETROVIRUS VECTOR; RNA; CARDIOTOXIN; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MYOD PROTEIN; NEUROPEPTIDE; PAX7 PROTEIN, MOUSE; TRANSCRIPTION FACTOR PAX7;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL MOTILITY; CELL PROLIFERATION ASSAY; HISTOLOGY; IMMUNOCYTOCHEMISTRY; MICROENVIRONMENT; MUSCLE CELL; MUSCLE MASS; MUSCLE REGENERATION; MUSCLE STEM CELL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SATELLITE CELL CULTURE; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; TISSUE REGENERATION; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; DEFICIENCY; KNOCKOUT MOUSE; METABOLISM; MYOBLAST; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE SATELLITE CELL; STEM CELL; TUMOR MICROENVIRONMENT;

MUS;

ANIMALS; CARDIOTOXINS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLULAR MICROENVIRONMENT; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MUSCLE FIBERS, SKELETAL; MYOBLASTS; MYOD PROTEIN; NEUROPEPTIDES; PAX7 TRANSCRIPTION FACTOR; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELLS;

EID: 84918514151     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.112557     Document Type: Article

References (38)

1. Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K. and Chazaud, B. (2007). Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204, 1057-1069.
2. 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.
3. Brack, A. S., Conboy, I. M., Conboy, M. J., Shen, J. and Rando, T. A. (2008). A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2, 50-59.
4. Bröhl, D., Vasyutina, E., Czajkowski, M. T., Griger, J., Rassek, C., Rahn, H.-P., Purfürst, B., Wende, H. and Birchmeier, C. (2012). Colonization of the satellite cell niche by skeletal muscle progenitor cells depends on Notch signals. Dev. Cell 23, 469-481.
5. Buckingham, M. (2007). Skeletal muscle progenitor cells and the role of Pax genes. C. R. Biol. 330, 530-533.
6. 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.
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. Corbo, J. C., Deuel, T. A., Long, J. M., LaPorte, P., Tsai, E., Wynshaw-Boris, A. and Walsh, C. A. (2002). Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 22, 7548-7557.
9. des Portes, V., Pinard, J. M., Billuart, P., Vinet, M. C., Koulakoff, A., Carrié, A., Gelot, A., Dupuis, E., Motte, J., Berwald-Netter, Y. et al. (1998). A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92, 51-61.
10. Fukada, S., Higuchi, S., Segawa, M., Koda, K.-i., 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. 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.
13. Gayraud-Morel, B, Chrétien, F., Flamant, P., Gomes, D., Zammit, P. S. and Tajbakhsh, S. (2007). A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev. Biol. 312, 13-28.
14. Gleeson, J. G., Allen, K. M., Fox, J.W., Lamperti, E. D., Berkovic, S., Scheffer, I., Cooper, E. C., Dobyns, W. B., Minnerath, S. R., Ross, M. E. et al. (1998). Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92, 63-72.
15. Horsley, V., Jansen, K. M., Mills, S. T. and Pavlath, G. K. (2003). IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113, 483-494.
16. Jockusch, H. and Voigt, S. (2003). Migration of adult myogenic precursor cells as revealed by GFP/nLacZ labelling of mouse transplantation chimeras. J. Cell Sci. 116, 1611-1616.
17. Kitamura, T., Koshino, Y., Shibata, F., Oki, T., Nakajima, H., Nosaka, T. and Kumagai, H. (2003). Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol. 31, 1007-1014.
18. 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.
19. Le Grand, F., Jones, A. E., Seale, V., Scime, 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.
20. 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.
21. 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.
22. Montarras, D., Lindon, C., Pinset, C. and Domeyne, P. (2000). Cultured myf5 null and myoD null muscle precursor cells display distinct growth defects. Biol. Cell 92, 565-572.
23. Morita, S., Kojima, T. and Kitamura, T. (2000). Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Therapy 7, 1063-1066.
24. Nosaka, T., Kawashima, T., Misawa, K., Ikuta, K., Mui, A. L.-F. and Kitamura, T. (1999). STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 18, 4754-4765.
25. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. and Nishimune, Y. (1997). ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett. 407, 313-319.
26. Pallafacchina, G., François, 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.
27. Piens, M., Muller, M., Bodson, M., Baudouin, G. and Plumier, J.-C. (2010). A short upstream promoter region mediates transcriptional regulation of the mouse doublecortin gene in differentiating neurons. BMC Neurosci. 11, 64.
28. 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, 91-102.
29. Rudnicki, M. A., Le Grand, F., McKinnell, I. and Kuang, S. (2008). The molecular regulation of muscle stem cell function. Cold Spring Harb. Symp. Quant. Biol. 73, 323-331.
30. Sabourin, L. A. and Rudnicki, M. A. (2000). The molecular regulation of myogenesis. Clin. Genet. 57, 16-25.
31. Sabourin, L. A., Girgis-Gabardo, A., Seale, P., Asakura, A. and Rudnicki, M. A. (1999). Reduced differentiation potential of primary MyoD-/-myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144, 631-643.
32. 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.
33. Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
34. Tallquist, M. D., Weismann, K. E., Hellstrom, M. and Soriano, P. (2000). Early myotome specification regulates PDGFA expression and axial skeleton development. Development 127, 5059-5070.
35. Tanaka, T., Serneo, F. F., Higgins, C., Gambello, M. J., Wynshaw-Boris, A. and Gleeson, J. G. (2004). Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165, 709-721.
36. Uezumi, A., Ojima, K., Fukada, S.-i., 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.
37. Zammit, P. S. (2008). All muscle satellite cells are equal, but are some more equal than others? J. Cell Sci. 121, 2975-2982.
38. 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.