Retinoblastoma protein and MyoD function together to effect the repression of Fra-1 and in turn cyclin D1 during terminal cell cycle arrest associated with myogenesis

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23417-23427

  Rajabi, Hasan N ^a   Takahashi, Chiaki ^a,b   Ewen, Mark E ^a,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b KANAZAWA UNIVERSITY   (Japan)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; TRANSCRIPTION FACTORS;

CELL-CYCLE ARREST; CELLULAR PROCESS; IMMEDIATE EARLY GENES; IMPORTANT FEATURES; INTRONIC ENHANCER; MYOGENIC DIFFERENTIATIONS; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSORS;

CELLS;

CYCLIN D1; MYOD PROTEIN; RETINOBLASTOMA PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR FRA 1; DNA; PRIMER DNA; PROTEIN C FOS;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; INTRON; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; 3T3 CELL LINE; ANIMAL; CELL CYCLE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSFORMED CELL LINE;

3T3 CELLS; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CYCLIN D1; DNA; DNA PRIMERS; MICE; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MYOD PROTEIN; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-FOS; RETINOBLASTOMA PROTEIN; RNA POLYMERASE II;

EID: 84906536747     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.532572     Document Type: Article

References (69)

1. Davis, R. L., Weintraub, H., and Lassar, A. B. (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987-1000
2. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T. K., Turner, D., Rupp, R., and Hollenberg, S. (1991) The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766
3. Zacksenhaus, E., Jiang, Z., Chung, D., Marth, J. D., Phillips, R. A., and Gallie, B. L. (1996) pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10, 3051-3064
4. Wu, L., de Bruin, A., Saavedra, H. I., Starovic, M., Trimboli, A., Yang, Y., Opavska, J., Wilson, P., Thompson, J. C., Ostrowski, M. C., Rosol, T. J., Woollett, L. A., Weinstein, M., Cross, J. C., Robinson, M. L., and Leone, G. (2003) Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421, 942-947
5. de Bruin, A., Wu, L., Saavedra, H. I., Wilson, P., Yang, W., Rosol, T. J., Weinstein, M., Rosinson, M. L., and Leone, G. (2003) Rb function in extraembryonic lineages suppresses apoptosis in CNS of Rb-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 100, 6546-6551
6. Takahashi, C., Bronson, R. T., Socolovsky, M., Contreras, B., Lee, K. Y., Jacks, T., Noda, M., Kucherlapati, R., and Ewen, M. E. (2003) Rb and N-ras function together to control differentiation in the mouse. Mol. Cell Biol. 23, 5256-5268
7. Schneider, J. W., Gu, W., Zhu, L., Mahdavi, V., and Nadal-Ginard, B. (1994) Reversal of terminal differentiation mediated by p107 in Rb-/-muscle cells. Science 264, 1467-1471
8. Novitch, B. G., Mulligan, G. J., Jacks, T., and Lassar, A. B. (1996) Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S andG2 phases of the cell cycle. J. Cell Biol. 135, 441-456
9. Chen, T.-T., and Wang, J. Y. (2000) Establishment of irreversible growth arrest in myogenic differentiation requires the RB LXCXE-binding function. Mol. Cell Biol. 20, 5571-5580
10. Takahashi, C., Contreras, B., Bronson, R. T., Loda, M., and Ewen, M. E. (2004) Genetic interaction between Rb and K-ras in the control of differentiation and tumor suppression. Mol. Cell Biol. 24, 10406-10415
11. Sellers, W. R., Novitch, B. G., Miyake, S., Heith, A., Otterson, G. A., Kaye, F. J., Lassar, A. B., and Kaelin, W. G., Jr. (1998) Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor growth. Genes Dev. 12, 95-106
12. Tsai, K. Y., Hu, Y., Macleod, K. F., Crowley, D., Yamasaki, L., and Jacks, T. (1998) Mutation of E2f-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol. Cell 2, 293-304
13. Ziebold, U., Reza, T., Caron, A., and Lees, J. A. (2001) E2F3 contributes both to the inappropriate proliferation and to the apoptosis arising in Rb mutant embryos. Genes Dev. 15, 386-391
14. Saavedra, H. I., Wu, L., de Bruin, A., Timmers, C., Rosol, T. J., Weinstein, M., Robinson, M. L., and Leone, G. (2002) Specificity of E2F1, E2F2 and E2F3 in mediating phenotypes induced by loss of Rb. Cell Growth Differ. 13, 215-225
15. Novitch, B. G., Spicer, D. B., Kim, P. S., Cheung, W. L., and Lassar, A. B. (1999) pRb is required for MEF2-dependent gene expression as well as cell-cycle arrest during skeletal muscle differentiation. Curr. Biol. 9, 449-459
16. Puri, P. L., Avantaggiati, M. L., Balsano, C., Sang, N., Graessmann, A., Giordano, A., and Levrero, M. (1997) p300 is required for MyoD-dependent cell cycle arrest and muscle-specific gene transcription. EMBO J. 16, 369-383
17. de la Serna, I. L., Roy, K., Carlson, K. A., and Imbalzano, A. N. (2001)MyoD can induce cell cycle arrest but not muscle differentiation in the presence of dominant negative SWI/SNF chromatin remodeling enzymes. J. Biol. Chem. 276, 41486-41491
18. Bergstrom, D. A., Penn, B. H., Strand, A., Perry, R. L., Rudnicki, M. A., and Tapscott, S. J. (2002) Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell 9, 587-600
19. Tomczak, K. K., Marinescu, V. D., Ramoni, M. F., Sanoudou, D., Montanaro, F., Han, M., Kunkel, L. M., Kohane, I. S., and Beggs, A. H. (2004) Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J. 18, 403-405
20. Moran, J. L., Li, Y., Hill, A. A., Mounts, W. M., and Miller, C. P. (2002) Gene expression changes during mouse skeletal myoblast differentiation revealed by transcriptional profiling. Physiol. Genomics 10, 103-111
21. Shen, X., Collier, J. M., Hlaing, M., Zhang, L., Delshad, E. H., Bristow, J., and Bernstein, H. S. (2003) Genome-wide examination of myoblast cell cycle withdrawal during differentiation. Dev. Dyn. 226, 128-138
22. Blais, A., Tsikitis, M., Acosta-Alvear, D., Sharan, R., Kluger, Y., and Dynlacht, B. D. (2005) An initial blueprint for myogenic differentiation. Genes Dev. 19, 553-569
23. Cao, Y., Kumar, R. M., Penn, B. H., Berkes, C. A., Kooperberg, C., Boyer, L. A., Young, R. A., and Tapscott, S. J. (2006) Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J. 25, 502-511
24. Mal, A., and Harter, M. L. (2003) MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 1735-1739
25. Gu, W., Schneider, J. W., Condorelli, G., Kaushal, S., Mahdavi, V., and Nadal-Ginard, B. (1993) Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72, 309-324
26. Trouche, D., Grigoriev, M., Lenormand, J.-L., Robin, P., Leibovitch, S. A., Sassone-Corsi, P., and Harel-Bellan, A. (1993) Repression of c-fos promoter by MyoD on muscle cell differentiation. Nature 363, 79-82
27. Halevy, O., Novitch, B. G., Spicer, D. B., Skapek, S. X., Rhee, J., Hannon, G. J., Beach, D., and Lassar, A. B. (1995) Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267, 1018-1021
28. Franklin, D. S., and Xiong, Y. (1996) Induction of p18INK4c and its predominant association with CDK4 and CDK6 during myogenic differentiation. Mol. Biol. Cell 7, 1587-1599
29. Zhang, J. M., Zhao, X., Wei, Q., and Paterson, B. M. (1999) Direct inhibition of G1 cdk kinase activity by MyoD promotes myoblast cell cycle withdrawal and terminal differentiation. EMBO J. 18, 6983-6993
30. Cenciarelli, C., De Santa, F., Puri, P. L., Mattei, E., Ricci, L., Bucci, F., Felsani, A., and Caruso, M. (1999) Critical role played by cyclin D3 in the MyoD-mediated arrest of cell cycle during myoblast differentiation. Mol. Cell Biol. 19, 5203-5217
31. Latella, L., Sacco, A., Pajalunga, D., Tiainen, M., Macera, D., D'Angelo, M., Felici, A., Sacchi, A., and Crescenzi, M. (2001) Reconstitution of cyclin D1-Associated kinase activity drives terminally differentiated cells into the cell cycle. Mol. Cell Biol. 21, 5631-5643
32. Skapek, S. X., Rhee, J., Spicer, D. B., and Lassar, A. B. (1995) Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267, 1022-1024
33. Skapek, S. X., Rhee, J., Kim, P. S., Novitch, B. G., and Lassar, A. B. (1996) Cyclin-mediated inhibition of muscle gene expression via a mechanism that is independent of pRB hyperphosphorylation. Mol. Cell Biol. 16, 7043-7053
34. Rao, S. S., Chu, C., and Kohtz, D. S. (1994) Ectopic expression of cyclin D1 prevents activation of gene transcription by myogenic basic helix-loophelix regulators. Mol. Cell Biol. 14, 5259-5267
35. Lazaro, J. B., Bailey, P. J., and Lassar, A. B. (2002) Cyclin D-cdk4 activity modulates the subnuclear localization and interaction of MEF2 with SRCfamily coactivators during skeletal muscle differentiation. Genes Dev. 16, 1792-1805
36. Peeper, D. S., Upton, T. M., Ladha, M. H., Neuman, E., Zalvide, J., Bernards, R., DeCaprio, J. A., and Ewen, M. E. (1997) Ras signalling linked to the cell-cycle machinery by the retinoblastoma protein. Nature 386, 177-181
37. Blau, H. M., Pavlath, G. K., Hardeman, E. C., Chiu, C. P., Silberstein, L., Webster, S. G., Miller, S. C., and Webster, C. (1985) Plasticity of the differentiated state. Science 230, 758-766
38. Shapiro, G. I., Park, J. E., Edwards, C. D., Mao, L., Merlo, A., Sidransky, D., Ewen, M. E., and Rollins, B. J. (1995) Multiple mechanisms of p16INK4A inactivation in non-small cell lung cancer cell lines. Cancer Res. 55, 6200-6209
39. Lee, K. Y., Ladha, M. H., McMahon, C., and Ewen, M. E. (1999) The retinoblastoma protein is linked to the activation of Ras. Mol. Cell Biol. 19, 7724-7732
40. He, T.-C., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W., and Vogelstein, B. (1998) A simplified system for generation recombinant adenovirus. Proc. Natl. Acad. Sci. U.S.A. 95, 2509-2514
41. Schreiber, M., Poirier, C., Franchi, A., Kurzbauer, R., Guenet, J.-L., Carle, G. F., and Wagner, E. F. (1997) Structure and chromosomal assigment of the mouse fra-1 gene, and its exclusion as a candidate gene for oc (osteosclerosis). Oncogene 15, 1171-1178
42. Lamb, J., Ladha, M. H., McMahon, C., Sutherland, R. L., and Ewen, M. E. (2000) Regulation of the functional interaction between cyclin D1 and the estrogen receptor. Mol. Cell Biol. 20, 8667-8675
43. Wang, Q., Carroll, J. S., and Brown, M. (2005) Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol. Cell 19, 631-642
44. Berkes, C. A., Bergstrom, D. A., Penn, B. H., Seaver, K. J., Knoepfler, P. S., and Tapscott, S. J. (2004) Pbx marks genes for activation by MyoD indicating a role for a homeodomain protein in establishing myogenic potential. Mol. Cell 14, 465-477
45. Brown, J. R., Nigh, E., Lee, R. J., Ye, H., Thompson, M. A., Saudou, F., Pestell, R. G., and Greenberg, M. E. (1998) Fos family members induce cell cycle entry by activating cyclin D1. Mol. Cell Biol. 18, 5609-5619
46. Tiainen, M., Pajalunga, D., Ferrantelli, F., Soddu, S., Salvatori, G., Sacchi, A., and Crescenzi, M. (1996) Terminally differentiated skeletal myotubes are not confined to G0 but can enter G1 upon growth factor stimulation. Cell Growth Differ. 7, 1039-1050
47. Murphy, L. O., MacKeigan, J. P., and Blenis, J. (2004) A network of immediate early gene products propogates subtle differences in mitogen-Activated protein kinase signal amplitude and duration. Mol. Cell Biol. 24, 144-153
48. Burch, P. M., Yuan, Z., Loonen, A., and Heintz, N. H. (2004) An extracellular signal-regulated kinase 1-And 2-dependent program of chromatin trafficking of c-Fos and Fra-1 is required for cyclin D1 expression during cell cycle reentry. Mol. Cell Biol. 24, 4696-4709
49. Herrera, R. E., Sah, V. P., Williams, B. O., Mäkelä, T. P., Weinberg, R. A., and Jacks, T. (1996) Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblasts. Mol. Cell Biol. 16, 2402-2407
50. Cohen, D. R., Ferreira, P. C., Gentz, R., Franza, B. R., Jr., and Curran, T. (1989) The product of the fos-related gene, fra-1, binds cooperatively to the AP-1 site with Jun: transcription factor AP-1 is comprised of multiple protein complexes. Genes Dev. 3, 173-184
51. Wisdon, R., and Verma, I. M. (1993) Transformation by Fos proteins requires a C-terminal transactivation domain. Mol. Cell Biol. 13, 7429-7438
52. Bergers, G., Graninger, P., Braselmann, S., Wrighton, C., and Busslinger, M. (1995) Transcriptional activation of the fra-1 gene by AP-1 is mediated by regulatory sequences in the first intron. Mol. Cell Biol. 15, 3748-3758
53. Casalino, L., De Cesare, D., and Verde, P. (2003) Accumulation of Fra-1 in ras-transformed cells depends on both transcriptional autoregulation and MEK-dependent postranslational stabilization. Mol. Cell Biol. 23, 4401-4415
54. Zhu, J., Liu, J. S., and Lawrence, C. E. (1998) Bayesian adaptive sequence alignment algorithms. Bioinformatics 14, 25-39
55. Frolov, M. V., and Dyson, N. J. (2004) Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci. 117, 2173-2181
56. Bulger, M., and Groudine, M. (2011) Functional and mechanistic diversity of distal transcription enhancers. Cell 144, 327-339
57. Spizz, G., Roman, D., Strauss, A., and Olson, E. N. (1986) Serum and fibroblast growth factor inhibit myogenic differentiation through a mechanism dependent on protein synthesis and independent of cell proliferation. J. Biol. Chem. 261, 9483-9488
58. Weintraub, H., Davis, R., Lockshon, D., and Lassar, A. (1990) MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc. Natl. Acad. Sci. U.S.A. 87, 5623-5627
59. Odelberg, S. J., Kollhoff, A., and Keating, M. T. (2000) Dedifferentiation of mammalian myotubes induced by msx1. Cell 103, 1099-1109
60. Huh, M. S., Parker, M. H., Scimè, A., Parks, R., and Rudnicki, M. A. (2004) Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J. Cell Biol. 166, 865-876
61. Camarda, G., Siepi, F., Pajalunga, D., Bernardini, C., Rossi, R., Montecucco, A., Meccia, E., and Crescenzi, M. (2004)ApRb-independent mechanism preserves the postmitotic state in terminally differentiated skeletal muscle cells. J. Cell Biol. 167, 417-423
62. Blais, A., van Oevelen, C. J., Margueron, R., Acosta-Alvear, D., and Dynlacht, B. D. (2007) Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit. J. Cell Biol. 179, 1399-1412
63. Guo, K., Wang, J., Andrés, V., Smith, R. C., and Walsh, K. (1995) MyoDinduced expression of p21 inhibits cyclin-dependent kinase activity upon myoctye terminal differentiation. Mol. Cell Biol. 15, 3823-3829
64. Zhang, P., Wong, C., Liu, D., Finegold, M., Harper, J. W., and Elledge, S. J. (1999) p21CIP1 and p57KIP2 control muscle differentiation at the myogenin step. Genes Dev. 13, 213-224
65. Lassar, A. B., Skapek, S. X., and Novitch, B. (1994) Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6, 788-794
66. Ait-Si-Ali, S., Guasconi, V., Fritsch, L., Yahi, H., Sekhri, R., Naguibneva, I., Robin, P., Cabon, F., Polesskaya, A., and Harel-Bellan, A. (2004)ASuv39hdependent mechanism for silencing S-phase genes in differentiating but not cycling cells. EMBO J. 23, 605-615
67. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., Jaenisch, R., Wagschal, A., Feil, R., Schreiber, S. L., and Lander, E. S. (2006)Abivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326
68. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T. K., Koche, R. P., Lee, W., Mendenhall, E., O'Donovan, A., Presser, A., Russ, C., Xie, X., Meissner, A., Wernig, M., Jaenisch, R., Nusbaum, C., Lander, E. S., and Bernstein, B. E. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560
69. Bengal, E., Ransone, L., Scharfmann, R., Dwarki, V. J., Tapscott, S. J., Weintraub, H., and Verma, I. M. (1992) Functional antagonism between c-Jun and MyoD proteins: a direct physical association. Cell 68, 507-519