Codependent Activators Direct Myoblast-Specific MyoD Transcription

Developmental Cell

Volumn 15, Issue 4, 2008, Pages 534-546

  Hu, Ping ^a   Geles, Kenneth G ^a   Paik, Ji Hye ^b   DePinho, Ronald A ^b,c   Tjian, Robert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

DEVBIO

Indexed keywords

MYOD PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CELL FATE; CONTROLLED STUDY; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MYOBLASTS; MYOD PROTEIN; PAIRED BOX TRANSCRIPTION FACTORS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

MUS;

EID: 53249095869     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2008.08.018     Document Type: Article

References (75)

1. Accili D., and Arden K.C. FoxOs at the crossroads of cellular metabolism, differentiation and transformation. Cell 117 (2004) 421-426
2. Anderson M.J., Viars C.S., Czekay S., Cavenee W.K., and Arden K.C. Cloning and characterization of three human forkhead genes that comprise an FKHR-like gene subfamily. Genomics 47 (1998) 187-199
3. Arden K.C. Multiple roles of FOXO transcription factors in mammalian cells point to multiple roles in cancer. Exp. Gerontol. 41 (2006) 709-717
4. Asakura A., Lyons G.E., and Tapscott S.J. The regulation of MyoD gene expression: conserved elements mediate expression in embryonic axial muscle. Dev. Biol. 171 (1995) 386-398
5. Bajard L., Relaix F., Lagha M., Rocancourt D., Daubas P., and Buckingham M.E. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 20 (2006) 2450-2464
6. Berkes C.A., and Tapscott S.J. MyoD and the transcriptional control of myogenesis. Semin. Cell Dev. Biol. 16 (2005) 585-595
7. Biggs III W.H., Cavenee W.K., and Arden K.C. Identification and characterization of members of the FKHR (FOX O) subclass of winged-helix transcription factors in the mouse. Mamm. Genome 12 (2001) 416-425
8. Bober E., Franz T., Arnold H.H., Gruss P., and Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120 (1994) 603-612
9. Bois P.R., and Grosveld G.C. FKHR (FOXO1a) is required for myotube fusion of primary mouse myoblasts. EMBO J. 22 (2003) 1147-1157
10. Buckingham M., and Relaix F. 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 (2007) 645-673
11. Buckingham M., Bajard L., Daubas P., Esner M., Lagha M., Relaix F., and Rocancourt D. Myogenic progenitor cells in the mouse embryo are marked by the expression of Pax3/7 genes that regulate their survival and myogenic potential. Anat. Embryol. (Berl.) 211 Suppl 1 (2006) 51-56
12. Carlson M.E., and Conboy I.M. Loss of stem cell regenerative capacity within aged niches. Aging Cell 6 (2007) 371-382
13. Carter M.E., and Brunet A. FOXO transcription factors. Curr. Biol. 17 (2007) R113-R114
14. Castrillon D.H., Miao L., Kollipara R., Horner J.W., and DePinho R.A. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301 (2003) 215-218
15. Charge S.B., and Rudnicki M.A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84 (2004) 209-238
16. Chen J.C., Ramachandran R., and Goldhamer D.J. Essential and redundant functions of the MyoD distal regulatory region revealed by targeted mutagenesis. Dev. Biol. 245 (2002) 213-223
17. Choi J., Costa M.L., Mermelstein C.S., Chagas C., Holtzer S., and Holtzer H. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc. Natl. Acad. Sci. USA 87 (1990) 7988-7992
18. Collins C.A. Satellite cell self-renewal. Curr. Opin. Pharmacol. 6 (2006) 301-306
19. Conboy I.M., Conboy M.J., Wagers A.J., Girma E.R., Weissman I.L., and Rando T.A. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433 (2005) 760-764
20. Cornelison D.D., Olwin B.B., Rudnicki M.A., and Wold B.J. MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev. Biol. 224 (2000) 122-137
21. Deato M.D., and Tjian R. Switching of the core transcription machinery during myogenesis. Genes Dev. 21 (2007) 2137-2149
22. Furuyama T., Nakazawa T., Nakano I., and Mori N. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem. J. 349 (2000) 629-634
23. Gauthier-Rouviere C., Vandromme M., Tuil D., Lautredou N., Morris M., Soulez M., Kahn A., Fernandez A., and Lamb N. Expression and activity of serum response factor is required for expression of the muscle-determining factor MyoD in both dividing and differentiating mouse C2C12 myoblasts. Mol. Biol. Cell 7 (1996) 719-729
24. Goldhamer D.J., Brunk B.P., Faerman A., King A., Shani M., and Emerson Jr. C.P. Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development 121 (1995) 637-649
25. Gomis R.R., Alarcon C., He W., Wang Q., Seoane J., Lash A., and Massague J. A FoxO-Smad synexpression group in human keratinocytes. Proc. Natl. Acad. Sci. USA 103 (2006) 12747-12752
26. Goulding M., Lumsden A., and Paquette A.J. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120 (1994) 957-971
27. Holterman C.E., Le Grand F., Kuang S., Seale P., and Rudnicki M.A. Megf10 regulates the progression of the satellite cell myogenic program. J. Cell Biol. 179 (2007) 911-922
28. Hosaka T., Biggs III W.H., Tieu D., Boyer A.D., Varki N.M., Cavenee W.K., and Arden K.C. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl. Acad. Sci. USA 101 (2004) 2975-2980
29. Hribal M.L., Nakae J., Kitamura T., Shutter J.R., and Accili D. Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J. Cell Biol. 162 (2003) 535-541
30. Huang H., and Tindall D.J. Dynamic FoxO transcription factors. J. Cell Sci. 120 (2007) 2479-2487
31. Jacobs F.M., van der Heide L.P., Wijchers P.J., Burbach J.P., Hoekman M.F., and Smidt M.P. FoxO6, a novel member of the FoxO class of transcription factors with distinct shuttling dynamics. J. Biol. Chem. 278 (2003) 35959-35967
32. Jonsson H., Allen P., and Peng S.L. Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat. Med. 11 (2005) 666-671
33. Kadonaga J.T., and Tjian R. Affinity purification of sequence-specific DNA binding proteins. Proc. Natl. Acad. Sci. USA 83 (1986) 5889-5893
34. Kamachi Y., Uchikawa M., and Kondoh H. Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16 (2000) 182-187
35. Kassar-Duchossoy L., Giacone E., Gayraud-Morel B., Jory A., Gomes D., and Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19 (2005) 1426-1431
36. Khan J., Bittner M.L., Saal L.H., Teichmann U., Azorsa D.O., Gooden G.C., Pavan W.J., Trent J.M., and Meltzer P.S. cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. Proc. Natl. Acad. Sci. USA 96 (1999) 13264-13269
37. Kitamura T., Kitamura Y.I., Funahashi Y., Shawber C.J., Castrillon D.H., Kollipara R., DePinho R.A., Kitajewski J., and Accili D. A Foxo/Notch pathway controls myogenic differentiation and fiber type specification. J. Clin. Invest. 117 (2007) 2477-2485
38. Kondoh H., Uchikawa M., and Kamachi Y. Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int. J. Dev. Biol. 48 (2004) 819-827
39. Kucharczuk K.L., Love C.M., Dougherty N.M., and Goldhamer D.J. Fine-scale transgenic mapping of the MyoD core enhancer: MyoD is regulated by distinct but overlapping mechanisms in myotomal and non-myotomal muscle lineages. Development 126 (1999) 1957-1965
40. L'Honore A., Lamb N.J., Vandromme M., Turowski P., Carnac G., and Fernandez A. MyoD distal regulatory region contains an SRF binding CArG element required for MyoD expression in skeletal myoblasts and during muscle regeneration. Mol. Biol. Cell 14 (2003) 2151-2162
41. Lam E.W., Francis R.E., and Petkovic M. FOXO transcription factors: key regulators of cell fate. Biochem. Soc. Trans. 34 (2006) 722-726
42. Lang D., Powell S.K., Plummer R.S., Young K.P., and Ruggeri B.A. PAX genes: roles in development, pathophysiology, and cancer. Biochem. Pharmacol. 73 (2007) 1-14
43. Lefebvre V., Dumitriu B., Penzo-Mendez A., Han Y., and Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int. J. Biochem. Cell Biol. 39 (2007) 2195-2214
44. Li H., Liang J., Castrillon D.H., DePinho R.A., Olson E.N., and Liu Z.P. FoxO4 regulates tumor necrosis factor alpha-directed smooth muscle cell migration by activating matrix metalloproteinase 9 gene transcription. Mol. Cell. Biol. 27 (2007) 2676-2686
45. Lin L., Hron J.D., and Peng S.L. Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21 (2004) 203-213
46. Liu Z.P., Wang Z., Yanagisawa H., and Olson E.N. Phenotypic modulation of smooth muscle cells through interaction of Foxo4 and myocardin. Dev. Cell 9 (2005) 261-270
47. Machida S., Spangenburg E.E., and Booth F.W. Forkhead transcription factor FoxO1 transduces insulin-like growth factor's signal to p27Kip1 in primary skeletal muscle satellite cells. J. Cell. Physiol. 196 (2003) 523-531
48. Mammucari C., Milan G., Romanello V., Masiero E., Rudolf R., Del Piccolo P., Burden S.J., Di Lisi R., Sandri C., Zhao J., et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6 (2007) 458-471
49. Maroto M., Reshef R., Munsterberg A.E., Koester S., Goulding M., and Lassar A.B. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89 (1997) 139-148
50. Marr II M.T., D'Alessio J.A., Puig O., and Tjian R. IRES-mediated functional coupling of transcription and translation amplifies insulin receptor feedback. Genes Dev. 21 (2007) 175-183
51. McKinnell I.W., Ishibashi J., Le Grand F., Punch V.G., Addicks G.C., Greenblatt J.F., Dilworth F.J., and Rudnicki M.A. Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat. Cell Biol. 10 (2008) 77-84 10.1038/ncb1671 Published online December 9, 2007
52. Mercado G.E., and Barr F.G. Fusions involving PAX and FOX genes in the molecular pathogenesis of alveolar rhabdomyosarcoma: recent advances. Curr. Mol. Med. 7 (2007) 47-61
53. Morosetti R., Mirabella M., Gliubizzi C., Broccolini A., De Angelis L., Tagliafico E., Sampaolesi M., Gidaro T., Papacci M., Roncaglia E., et al. MyoD expression restores defective myogenic differentiation of human mesoangioblasts from inclusion-body myositis muscle. Proc. Natl. Acad. Sci. USA 103 (2006) 16995-17000
54. Paddison P.J., Cleary M., Silva J.M., Chang K., Sheth N., Sachidanandam R., and Hannon G.J. Cloning of short hairpin RNAs for gene knockdown in mammalian cells. Nat. Methods 1 (2004) 163-167
55. Paik J.H., Kollipara R., Chu G., Ji H., Xiao Y., Ding Z., Miao L., Tothova Z., Horner J.W., Carrasco D.R., et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128 (2007) 309-323
56. Parthun M.R., and Jaehning J.A. Purification and characterization of the yeast transcriptional activator GAL4. J. Biol. Chem. 265 (1990) 209-213
57. Puig O., and Tjian R. Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev. 19 (2005) 2435-2446
58. Puig O., Marr M.T., Ruhf M.L., and Tjian R. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17 (2003) 2006-2020
59. Relaix F., Rocancourt D., Mansouri A., and Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435 (2005) 948-953
60. Roth J.F., Shikama N., Henzen C., Desbaillets I., Lutz W., Marino S., Wittwer J., Schorle H., Gassmann M., and Eckner R. Differential role of p300 and CBP acetyltransferase during myogenesis: p300 acts upstream of MyoD and Myf5. EMBO J. 22 (2003) 5186-5196
61. Rudnicki M.A., Schnegelsberg P.N., Stead R.H., Braun T., Arnold H.H., and Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75 (1993) 1351-1359
62. -/- myogenic cells derived from adult skeletal muscle. J. Cell Biol. 144 (1999) 631-643
63. Sandri M., Sandri C., Gilbert A., Skurk C., Calabria E., Picard A., Walsh K., Schiaffino S., Lecker S.H., and Goldberg A.L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117 (2004) 399-412
64. Seale P., Sabourin L.A., Girgis-Gabardo A., Mansouri A., Gruss P., and Rudnicki M.A. Pax7 is required for the specification of myogenic satellite cells. Cell 102 (2000) 777-786
65. Seoane J., Le H.V., Shen L., Anderson S.A., and Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117 (2004) 211-223
66. Tapscott S.J. The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development 132 (2005) 2685-2695
67. Tothova Z., Kollipara R., Huntly B.J., Lee B.H., Castrillon D.H., Cullen D.E., McDowell E.P., Lazo-Kallanian S., Williams I.R., Sears C., et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128 (2007) 325-339
68. van der Heide L.P., Jacobs F.M., Burbach J.P., Hoekman M.F., and Smidt M.P. FoxO6 transcriptional activity is regulated by Thr26 and Ser184, independent of nucleo-cytoplasmic shuttling. Biochem. J. 391 (2005) 623-629
69. Wagers A.J., and Conboy I.M. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122 (2005) 659-667
70. Weintraub H., Tapscott S.J., Davis R.L., Thayer M.J., Adam M.A., Lassar A.B., and Miller A.D. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc. Natl. Acad. Sci. USA 86 (1989) 5434-5438
71. Weintraub H., Dwarki V.J., Verma I., Davis R., Hollenberg S., Snider L., Lassar A., and Tapscott S.J. Muscle-specific transcriptional activation by MyoD. Genes Dev. 5 (1991) 1377-1386
72. Wilson E.M., and Rotwein P. Control of MyoD function during initiation of muscle differentiation by an autocrine signaling pathway activated by insulin-like growth factor-II. J. Biol. Chem. 281 (2006) 29962-29971
73. Xuan Z., and Zhang M.Q. From worm to human: bioinformatics approaches to identify FOXO target genes. Mech. Ageing Dev. 126 (2005) 209-215
74. Yablonka-Reuveni Z., Rudnicki M.A., Rivera A.J., Primig M., Anderson J.E., and Natanson P. The transition from proliferation to differentiation is delayed in satellite cells from mice lacking MyoD. Dev. Biol. 210 (1999) 440-455
75. 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. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278 (2003) 8826-8836