Six family genes control the proliferation and differentiation of muscle satellite cells

Experimental Cell Research

Volumn 316, Issue 17, 2010, Pages 2932-2944

  Yajima, Hiroshi ^a   Motohashi, Norio ^b   Ono, Yusuke ^b   Sato, Shigeru ^a   Ikeda, Keiko ^a   Masuda, Satoru ^b   Yada, Erica ^b   Kanesaki, Hironori ^b   Miyagoe Suzuki, Yuko ^b   Takeda, Shin'ichi ^b   Kawakami, Kiyoshi ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

Cell proliferation; Gene knockdown; Muscle differentiation; Muscle satellite cell; Retrovirus mediated overexpression; Six gene

Indexed keywords

MYOGENIN; NUCLEIC ACID; NUCLEIC ACID BINDING PROTEIN; SIX4 PROTEIN; TRANSCRIPTION FACTOR SIX1; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; SIX4 PROTEIN, MOUSE; SIX5 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL; TIBIALIS ANTERIOR MUSCLE; ADULT; ANIMAL; BIOSYNTHESIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; MUSCLE CELL; PHYSIOLOGY;

MUS;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; MUSCLE CELLS; MYOGENIN; SATELLITE CELLS, SKELETAL MUSCLE; TRANS-ACTIVATORS;

EID: 77956880144     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.08.001     Document Type: Article

References (57)

1. Mauro A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 1961, 9:493-495.
2. Otto A., Collins-Hooper H., Patel K. The origin, molecular regulation and therapeutic potential of myogenic stem cell populations. J. Anat. 2009, 215:477-497.
3. Zammit P.S., Golding J.P., Nagata Y., Hudon V., Partridge T.A., Beauchamp J.R. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal?. J. Cell Biol. 2004, 166:347-357.
4. Fukada S., Higuchi S., Segawa M., Koda K., Yamamoto Y., Tsujikawa K., Kohama Y., Uezumi A., Imamura M., Miyagoe-Suzuki Y., Takeda S., Yamamoto H. Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody. Exp. Cell Res. 2004, 296:245-255.
5. Fukada S., Uezumi A., Ikemoto M., Masuda S., Segawa M., Tanimura N., Yamamoto H., Miyagoe-Suzuki Y., Takeda S. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 2007, 25:2448-2459.
6. Serikaku M.A., O'Tousa J.E. sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 1994, 138:1137-1150.
7. Cheyette B.N., Green P.J., Martin K., Garren H., Hartenstein V., Zipursky S.L. The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 1994, 12:977-996.
8. Kawakami K., Sato S., Ozaki H., Ikeda K. Six family genes-structure and function as transcription factors and their roles in development. Bioessays 2000, 22:616-626.
9. Kobayashi H., Kawakami K., Asashima M., Nishinakamura R. Six1 and Six4 are essential for Gdnf expression in the metanephric mesenchyme and ureteric bud formation, while Six1 deficiency alone causes mesonephric-tubule defects. Mech. Dev. 2007, 124:290-303.
10. Konishi Y., Ikeda K., Iwakura Y., Kawakami K. Six1 and Six4 promote survival of sensory neurons during early trigeminal gangliogenesis. Brain Res. 2006, 1116:93-102.
11. Ozaki H., Nakamura K., Funahashi J., Ikeda K., Yamada G., Tokano H., Okamura H.O., Kitamura K., Muto S., Kotaki H., Sudo K., Horai R., Iwakura Y., Kawakami K. Six1 controls patterning of the mouse otic vesicle. Development 2004, 131:551-562.
12. Zheng W., Huang L., Wei Z.B., Silvius D., Tang B., Xu P.X. The role of Six1 in mammalian auditory system development. Development 2003, 130:3989-4000.
13. Xu P.X., Zheng W., Huang L., Maire P., Laclef C., Silvius D. Six1 is required for the early organogenesis of mammalian kidney. Development 2003, 130:3085-3094.
14. Laclef C., Souil E., Demignon J., Maire P. Thymus, kidney and craniofacial abnormalities in Six 1 deficient mice. Mech. Dev. 2003, 120:669-679.
15. Laclef C., Hamard G., Demignon J., Souil E., Houbron C., Maire P. Altered myogenesis in Six1-deficient mice. Development 2003, 130:2239-2252.
16. Ozaki H., Watanabe Y., Takahashi K., Kitamura K., Tanaka A., Urase K., Momoi T., Sudo K., Sakagami J., Asano M., Iwakura Y., Kawakami K. Six4, a putative myogenin gene regulator, is not essential for mouse embryonal development. Mol. Cell. Biol. 2001, 21:3343-3350.
17. Oliver G., Wehr R., Jenkins N.A., Copeland N.G., Cheyette B.N., Hartenstein V., Zipursky S.L., Gruss P. Homeobox genes and connective tissue patterning. Development 1995, 121:693-705.
18. Ikeda K., Ookawara S., Sato S., Ando Z., Kageyama R., Kawakami K. Six1 is essential for early neurogenesis in the development of olfactory epithelium. Dev. Biol. 2007, 311:53-68.
19. Suzuki Y., Ikeda K., Kawakami K. Regulatory role of Six1 in the development of taste papillae. Cell Tissue Res. 2010, 339:513-525.
20. K. Ikeda, R. Kageyama, Y. Suzuki, K. Kawakami, Six1 is indispensable for production of functional apical and basal progenitors during olfactory epithelial development, Int. J. Dev. Biol. (in press), http://doi:10.1387/ijdb.093041ki.
21. Grifone R., Demignon J., Houbron C., Souil E., Niro C., Seller M.J., Hamard G., Maire P. Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 2005, 132:2235-2249.
22. Grifone R., Laclef C., Spitz F., Lopez S., Demignon J., Guidotti J.E., Kawakami K., Xu P.X., Kelly R., Petrof B.J., Daegelen D., Concordet J.P., Maire P. Six1 and Eya1 expression can reprogram adult muscle from the slow-twitch phenotype into the fast-twitch phenotype. Mol. Cell. Biol. 2004, 24:6253-6267.
23. Niro C., Demignon J., Vincent S., Liu Y., Giordani J., Sgarioto N., Favier M., Guillet-Deniau I., Blais A., Maire P. Six1 and Six4 gene expression is necessary to activate the fast-type muscle gene program in the mouse primary myotome. Dev. Biol. 2010, 338:168-182.
24. Klesert T.R., Cho D.H., Clark J.I., Maylie J., Adelman J., Snider L., Yuen E.C., Soriano P., Tapscott S.J. Mice deficient in Six5 develop cataracts: implications for myotonic dystrophy. Nat. Genet. 2000, 25:105-109.
25. Heath S.K., Carne S., Hoyle C., Johnson K.J., Wells D.J. Characterisation of expression of mDMAHP, a homeodomain-encoding gene at the murine DM locus. Hum. Mol. Genet. 1997, 6:651-657.
26. Spitz F., Demignon J., Porteu A., Kahn A., Concordet J.P., Daegelen D., Maire P. Expression of myogenin during embryogenesis is controlled by Six/sine oculis homeoproteins through a conserved MEF3 binding site. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14220-14225.
27. Ohto H., Kamada S., Tago K., Tominaga S.I., Ozaki H., Sato S., Kawakami K. Cooperation of six and eya in activation of their target genes through nuclear translocation of Eya. Mol. Cell. Biol. 1999, 19:6815-6824.
28. Olson E.N., Klein W.H. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 1994, 8:1-8.
29. Yun K., Wold B. Skeletal muscle determination and differentiation: story of a core regulatory network and its context. Curr. Opin. Cell Biol. 1996, 8:877-889.
30. Cornelison D.D., Wold B.J. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 1997, 191:270-283.
31. Seale P., Sabourin L.A., Girgis-Gabardo A., Mansouri A., Gruss P., Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells. Cell 2000, 102:777-786.
32. Irintchev A., Zeschnigk M., Starzinski-Powitz A., Wernig A. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 1994, 199:326-337.
33. Kitamura T., Koshino Y., Shibata F., Oki T., Nakajima H., Nosaka T., Kumagai H. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol. 2003, 31:1007-1014.
34. Nabeshima Y., Hanaoka K., Hayasaka M., Esumi E., Li S., Nonaka I. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 1993, 364:532-535.
35. Hasty P., Bradley A., Morris J.H., Edmondson D.G., Venuti J.M., Olson E.N., Klein W.H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 1993, 364:501-506.
36. Sarkar P.S., Appukuttan B., Han J., Ito Y., Ai C., Tsai W., Chai Y., Stout J.T., Reddy S. Heterozygous loss of Six5 in mice is sufficient to cause ocular cataracts. Nat. Genet. 2000, 25:110-114.
37. Rudnicki M.A., Le Grand F., McKinnell I., Kuang S. The molecular regulation of muscle stem cell function. Cold Spring Harb. Symp. Quant. Biol. 2008, 73:323-331.
38. Serrano M., Lee H., Chin L., Cordon-Cardo C., Beach D., DePinho R.A. Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996, 85:27-37.
39. Dean J.L., McClendon A.K., Stengel K.R., Knudsen E.S. Modeling the effect of the RB tumor suppressor on disease progression: dependence on oncogene network and cellular context. Oncogene 2010, 29:68-80.
40. Zuber M.E., Perron M., Philpott A., Bang A., Harris W.A. Giant eyes in Xenopus laevis by overexpression of XOptx2. Cell 1999, 98:341-352.
41. Coletta R.D., Christensen K., Reichenberger K.J., Lamb J., Micomonaco D., Huang L., Wolf D.M., Muller-Tidow C., Golub T.R., Kawakami K., Ford H.L. The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6478-6483.
42. Yu Y., Davicioni E., Triche T.J., Merlino G. The homeoprotein six1 transcriptionally activates multiple protumorigenic genes but requires ezrin to promote metastasis. Cancer Res. 2006, 66:1982-1989.
43. Li X., Oghi K.A., Zhang J., Krones A., Bush K.T., Glass C.K., Nigam S.K., Aggarwal A.K., Maas R., Rose D.W., Rosenfeld M.G. Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature 2003, 426:247-254.
44. Zhang H., Stavnezer E. Ski regulates muscle terminal differentiation by transcriptional activation of Myog in a complex with Six1 and Eya3. J. Biol. Chem. 2009, 284:2867-2879.
45. Y. Liu, A. Chu, I. Chakroun, U. Islam, A. Blais, Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation, Nucleic Acids Res. (in press), http://doi:10.1093/nar/gkq585.
46. Ando Z., Sato S., Ikeda K., Kawakami K. Slc12a2 is a direct target of two closely related homeobox proteins, Six1 and Six4. FEBS J. 2005, 272:3026-3041.
47. Sato S., Nakamura M., Cho D.H., Tapscott S.J., Ozaki H., Kawakami K. Identification of transcriptional targets for Six5: implication for the pathogenesis of myotonic dystrophy type 1. Hum. Mol. Genet. 2002, 11:1045-1058.
48. Kawakami K., Ohto H., Ikeda K., Roeder R.G. Structure, function and expression of a murine homeobox protein AREC3, a homologue of Drosophila sine oculis gene product, and implication in development. Nucleic Acids Res. 1996, 24:303-310.
49. Ohto H., Takizawa T., Saito T., Kobayashi M., Ikeda K., Kawakami K. Tissue and developmental distribution of Six family gene products. Int. J. Dev. Biol. 1998, 42:141-148.
50. Ojima K., Uezumi A., Miyoshi H., Masuda S., Morita Y., Fukase A., Hattori A., Nakauchi H., Miyagoe-Suzuki Y., Takeda S. Mac-1(low) early myeloid cells in the bone marrow-derived SP fraction migrate into injured skeletal muscle and participate in muscle regeneration. Biochem. Biophys. Res. Commun. 2004, 321:1050-1061.
51. Ono Y., Gnocchi V.F., Zammit P.S., Nagatomi R. Presenilin-1 acts via Id1 to regulate the function of muscle satellite cells in a gamma-secretase-independent manner. J. Cell Sci. 2009, 122:4427-4438.
52. Ozaki H., Watanabe Y., Ikeda K., Kawakami K. Impaired interactions between mouse Eyal harboring mutations found in patients with branchio-oto-renal syndrome and Six, Dach, and G proteins. J. Hum. Genet. 2002, 47:107-116.
53. Morita S., Kojima T., Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 2000, 7:1063-1066.
54. Kawakami K., Yanagisawa K., Watanabe Y., Tominaga S., Nagano K. Different factors bind to the regulatory region of the Na+, K(+)-ATPase alpha 1-subunit gene during the cell cycle. FEBS Lett. 1993, 335:251-254.
55. Jacquemin V., Furling D., Bigot A., Butler-Browne G.S., Mouly V. IGF-1 induces human myotube hypertrophy by increasing cell recruitment. Exp. Cell Res. 2004, 299:148-158.
56. Horsley V., Jansen K.M., Mills S.T., Pavlath G.K. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 2003, 113:483-494.
57. Horsley V., Friday B.B., Matteson S., Kegley K.M., Gephart J., Pavlath G.K. Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J. Cell Biol. 2001, 153:329-338.