66
Views
69
CrossRef citations to date
0
Altmetric
Cell Growth and Development

The MyoD-Inducible p204 Protein Overcomes the Inhibition of Myoblast Differentiation by Id Proteins

, , &
Pages 2893-2905 | Received 26 Jul 2001, Accepted 29 Jan 2002, Published online: 27 Mar 2023

REFERENCES

  • Atherton, G. T., H. Travers, R. Deed, and J. D. Norton. 1996. Regulation of cell differentiation in C2C12 myoblasts by the Id3 helix-loop-helix protein. Cell Growth Differ. 7: 1059–1066.
  • Bader, D., T. Masaki, and D. A. Fischman. 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 96: 763–770.
  • Belletti, B., M. Prisco, A. Morrione, B. Valentinis, M. Navarro, and R. Baserga. 2001. Regulation of Id2 gene expression by the insulin-like growth factor I receptor requires signaling by phosphatidylinositol 3-kinase. J. Biol. Chem. 276: 13867–13874.
  • Benezra, R., R. Davis, D. Lockshon, D. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61: 49–59.
  • Biggs, J. R., Y. Zhang, and E. V. Murphy. 1995. Repression of the Id2 (inhibitor of differentiation) gene promoter during exit from the cell cycle. J. Cell Physiol. 164: 249–258.
  • Bischoff, R. 1994. The satellite cell and muscle regeneration, p. 97–118. In A. G. Engel and C. Franzini-Armstrong (ed.), Myology, vol. 1. McGraw-Hill, Inc., New York, N.Y.
  • Bounpheng, M. A., J. J. Dimas, S. G. Dodds, and B. A. Christy. 1999. Degradation of Id proteins by the ubiquitin-proteasome pathway. FASEB J. 13: 2257–2264.
  • Briggs, J. A., G. R. Burrus, B. D. Stickney, and R. C. Briggs. 1992. Cloning and expression of the human myeloid cell nuclear differentiation antigen: regulation by interferon alpha. J. Cell. Biochem. 49: 82–92.
  • Buskin, J. N., and S. D. Hauschka. 1989. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol. Cell. Biol. 9: 2627–2640.
  • Choubey, D., and J. U. Gutterman. 1997. Inhibition of E2F-4/DP-1-stimulated transcription by p202. Oncogene 15: 291–301.
  • Choubey, D., and P. Lengyel. 1992. Interferon action: nucleolar and nucleoplasmic localization of the interferon-inducible 72-kD protein that is encoded by the Ifi204 gene from the gene 200 cluster. J. Cell Biol. 116: 1333–1341.
  • Choubey, D., and P. Lengyel. 1995. Binding of an interferon-inducible protein (p202) to the retinoblastoma protein. J. Biol. Chem. 270: 6134–6140.
  • Choubey, D., S.-J. Li, B. Datta, J. U. Gutterman, and P. Lengyel. 1996. Inhibition of E2F-mediated transcription by p202. EMBO J. 15: 5668–5678.
  • Choubey, D., J. Snoddy, V. Chaturvedi, E. Toniato, G. Opdenakker, A. Thakur, H. Samanta, D. A. Engel, and P. Lengyel. 1989. Interferons as gene activators. Indications for repeated gene duplication during the evolution of a cluster of interferon-activatable genes on murine chromosome 1. J. Biol. Chem. 264: 17182–17189.
  • Cooper, C. L., G. Brady, F. Bilia, N. N. Iscove, and P. J. Quesenberry. 1997. Expression of the Id family helix-loop-helix regulators during growth and development in the hematopoietic system. Blood 89: 3155–3165.
  • Datta, B., B. Li, D. Choubey, G. Nallur, and P. Lengyel. 1996. p202, an interferon-inducible modulator of transcription, inhibits transcriptional activation by the p53 tumor suppressor protein, and a segment from the p53-binding protein 1 that binds to p202 overcomes this inhibition. J. Biol. Chem. 271: 27544–27555.
  • Datta, B., W. Min, S. Burma, and P. Lengyel. 1998. Increase in p202 expression during skeletal muscle differentiation: inhibition of MyoD protein expression and activity by p202. Mol. Cell. Biol. 18: 1074–1083.
  • Davis, R. H., H. Weintraub, and A. B. Lassar. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987–1000.
  • Deed, R. W., S. Armitage, and J. D. Norton. 1996. Nuclear localization and regulation of Id protein through an E protein-mediated chaperone mechanism. J. Biol. Chem. 271: 23603–23606.
  • Deftos, M. L., E. Huang, E. W. Ojala, K. A. Forbush, and M. J. Bevan. 2000. Notch1 signaling promotes the maturation of CD4 and CD8 SP thymocytes. Immunity 13: 73–84.
  • DeYoung, K. I., M. E. Ray, Y. A. Su, S. L. Anzick, R. W. Johnstone, J. A. Trapani, P. S. Meltzer, and J. M. Trent. 1997. Cloning a novel member of the human interferon-inducible gene family associated with control of tumorigenicity in a model of human melanoma. Oncogene 15: 453–457.
  • D'Souza, S., H. Xin, S. Walter, and D. Choubey. 2001. The gene encoding p202, an interferon-inducible negative regulator of the p53 tumor suppressor, is a target of p53-mediated transcriptional repression. J. Biol. Chem. 276: 298–305.
  • Edmondson, D. G., and E. N. Olson. 1989. A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev. 3: 628–640.
  • Geng, Y., S. D'Souza, H. Xin, S. Walter, and D. Choubey. 2000. p202 levels are negatively regulated by serum growth factors. Cell Growth Differ. 11:475–483.
  • Graham, F. L., J. Smiley, W. C. Russell, and R. Nairn. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 36: 59–74.
  • Halevy, O., B. G. Novitch, D. B. Spicer, S. X. Skapek, J. Rhee, G. J. Hannon, D. Beach, and A. B. Lassar. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267: 1018–1021.
  • Helin, K., J. A. Lees, M. Vidal, N. Dyson, E. Harlow, and A. Fattaey. 1992. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70: 337–350.
  • Hertel, L., M. DeAndrea, B. Azzimonti, A. Rolle, M. Gariglio, and S. Landolfo. 1999. The interferon-inducible 204 gene, a member of the Ifi200 family, is not involved in the antiviral state induction by IFN-alpha, but is required by the mouse cytomegalovirus for its replication. Virology 262: 1–8.
  • Hertel, L., S. Rolle, M. DeAndrea, B. Azzimonti, R. Osello, G. Gribaudo, M. Gariglio, and S. Landolfo. 2000. The retinoblastoma protein is an essential mediator that links the interferon-inducible 204 gene to cell-cycle regulation. Oncogene 19: 3598–3608.
  • Iavarone, A., P. Garg, A. Lasorella, J. Hsu, and M. A. Israel. 1994. The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8: 1270–1284.
  • Jen, Y., H. Weintraub, and R. Benezra. 1992. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev. 6: 1466–1479.
  • Johnstone, R. W., and J. A. Trapani. 1999. Transcription and growth regulatory functions of the HIN-200 family of proteins. Mol. Cell. Biol. 19: 5833–5838.
  • Kleeff, J., T. Ishiwata, H. Friess, M. W. Buchler, M. A. Israel, and M. Korc. 1998. The helix-loop-helix protein Id2 is overexpressed in human pancreatic cancer. Cancer Res. 58: 3769–3772.
  • Koul, D., R. Lapushin, H. J. Xu, G. B. Mills, J. U. Gutterman, and D. Choubey. 1998. p202 prevents apoptosis in murine AKR-2B fibroblasts. Biochem. Biophys. Res. Commun. 247: 379–382.
  • Kushner, D. B., and R. P. Ricciardi. 1999. Reduced phosphorylation of p50 is responsible for diminished NF-kappaB binding to the major histocompatibility complex class I enhancer in adenovirus type 12-transformed cells. Mol. Cell. Biol. 19: 2169–2179.
  • Landolfo, S., G. Gribaudo, and D. Lembo. 1998. The Ifi 200 genes: an emerging family of IFN-inducible genes. Biochimie 80: 721–728.
  • Langlands, K., X. Yin, G. Anand, and E. V. Prochownik. 1997. Differential interactions of Id proteins with basic-helix-loop-helix transcription factors. J. Biol. Chem. 272: 19785–19793.
  • Lasorella, A., M. Noseda, M. Beyna, and A. Iavarone. 2000. Id2 is a retinoblastoma protein target and mediates signaling by Myc oncoprotein. Nature 407: 592–598.
  • Lassar, A. B., R. L. Davis, W. E. Wright, T. Kadesch, C. Murre, A. Voronova, D. Baltimore, and H. Weintraub. 1991. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell 66: 305–315.
  • Lassar, A. B., S. X. Skapek, and B. Novitch. 1994. Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6: 788–794.
  • Lau, J. F., J. P. Parisien, and C. M. Horvath. 2000. Interferon regulatory factor subcellular localization is determined by a bipartite nuclear localization signal in the DNA-binding domain and interaction with cytoplasmic retention factors. Proc. Natl. Acad. Sci. USA 97: 7278–7283.
  • Lee, W. S., C. C. Kao, G. O. Bryant, X. Liu, and A. J. Berk. 1991. Adenovirus E1A activation domain binds the basic repeat in the TATA box transcription factor. Cell 67: 365–376.
  • Lembo, M., C. Sacchi, C. Zappador, G. Bellomo, M. Gaboli, P. P. Pandolfi, M. Gariglio, and S. Landolfo. 1998. Inhibition of cell proliferation by the interferon-inducible 204 gene, a member of the Ifi 200 cluster. Oncogene 16: 1543–1551.
  • Lengyel, P., D. Choubey, S.-J. Li, and B. Datta. 1995. The interferon-activatable gene 200 cluster: from structure toward function. Semin. Virol. 6: 203–213.
  • Liu, C. J., S. D. Dib-Hajj, and S. G. Waxman. 2001. Fibroblast growth factor homologous factor 1B binds to the C terminus of the tetrodotoxin-resistant sodium channel rNa(v)1.9a (NaN) J. Biol. Chem. 276: 18925–18933.
  • Liu, C. J., H. Wang, and P. Lengyel. 1999. The interferon-inducible nucleolar p204 protein binds the ribosomal RNA-specific UBF1 transcription factor and inhibits ribosomal RNA transcription. EMBO J. 18: 2845–2854.
  • Liu, C. J., H. Wang, Z. Zhao, S. Yu, Y. Lu, J. Meyer, G. Chatterjee, S. Deschamps, B. A. Roe, and P. Lengyel. 2000. MyoD-dependent induction during myoblast differentiation of p204, a protein also inducible by interferon. Mol. Cell. Biol. 20: 7024–7036.
  • Lyden, D., A. Z. Young, D. Zagzag, W. Yan, W. Gerald, R. O'Reilly, B. L. Bader, R. O. Hynes, Y. Zhuang, K. Manova, and R. Benezra. 1999. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401: 670–677.
  • Massari, M. E., and C. Murre. 2000. Helix-loop-helix proteins: regulation of transcription in eucaryotic organisms. Mol. Cell. Biol. 20: 429–440.
  • McKinsey, T. A., C. L. Zhang, and E. N. Olson. 2000. Activation of the myocyte enhance factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc. Natl. Acad. Sci. USA 97: 14400–14405.
  • Melnikova, I. N., M. Bounpheng, G. C. Schatteman, D. Gilliam, and B. A. Christy. 1999. Differential biological activities of mammalian Id proteins in muscle cells. Exp. Cell Res. 247: 94–104.
  • Min, W., S. Ghosh, and P. Lengyel. 1996. The interferon-inducible p202 protein as a modulator of transcription: inhibition of NF-κB, c-Fos, and c-Jun activities. Mol. Cell. Biol. 16: 359–368.
  • Mori, S., S. I. Nishikawa, and Y. Yokota. 2000. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO, J. 19: 5772-5781
  • Norton, J. D., R. W. Deed, G. Craggs, and F. Sablitzky. 1998. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8: 58–65.
  • Olson, E. N., and W. H. Klein. 1994. bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8: 1–8.
  • Opdenakker, G., J. Snoddy, D. Choubey, E. Toniato, D. D. Pravtcheva, M. F. Seldin, F. Ruddle, and P. Lengyel. 1989. Interferons as gene activators: a cluster of six interferon-activatable genes is linked to the erythroid alpha-spectrin locus on murine chromosome 1. Virol. 171: 568–578.
  • Pan, L., S. Sato, J. P. Frederick, X. H. Sun, and Y. Zhuang. 1999. Impaired immune responses and B-cell proliferation in mice lacking the Id3 gene. Mol. Cell. Biol. 19: 5969–5980.
  • Parker, S. B., G. Eichele, P. Zhang, A. Rawls, A. T. Sands, A. Bradley, E. N. Olson, J. W. Harper, and S. J. Elledge. 1995. p-53-independent expression of p21 Cip1 in muscle and other terminally differentiating cells. Science 267: 1024–1027.
  • Perez-Moreno, M. A., A. Locascio, I. Rodrigo, G. Dhondt, F. Portillo, M. A. Nieto, and A. Cano. 2001. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J. Biol. Chem. 276: 27424–27431.
  • Reznikoff, C. A., D. W. Brankow, and C. Heidelberger. 1973. Establishment and characterization of a cloned line of C3H mouse embryo cells sensitive to postconfluence inhibition of division. Cancer Res. 33: 3231–3238.
  • Rosin-Arbesfeld, R., F. Townsley, and M. Bienz. 2000. The APC tumour suppressor has a nuclear export function. Nature 406: 1009–1012.
  • Rozzo, S. J., J. D. Allard, D. Choubey, T. J. Vyse, S. Izui, G. Peltz, and B. L. Kotzin. 2001. Evidence for an interferon-inducible gene, Ifi202, in the susceptibility to systemic lupus. Immunity 15: 435–443.
  • Schultz, E. 1996. Satellite cell proliferative compartments in growing skeletal muscles. Dev. Biol. 175: 84–94.
  • Sen, G. C., and R. M. Ransohoff. 1998. Transcriptional regulation in the interferon system. Chapman and Hall, New York, N.Y.
  • Stark, G. R., B. R. G. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227–262.
  • Sun, X. H., N. G. Copeland, N. A. Jenkins, and D. Baltimore. 1991. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11: 5603–5611.
  • Trapani, J. A., M. Dawson, V. A. Apostolidis, and K. A. Browne. 1994. Genomic organization of IFI16, an interferon-inducible gene whose expression is associated with human myeloid cell differentiation: correlation of predicted protein domains with exon organization. Immunogenetics 40: 415–424.
  • Wang, H., G. Chatterjee, J. J. Meyer, C. J. Liu, N. A. Manjunath, P. Bray-Ward, and P. Lengyel. 1999. Characterics of three homologous 202 genes (Ifi202a, Ifi202b, and Ifi202c) from the murine interferon-activatable gene 200 cluster. Genomics 60: 281–294.
  • Wang, H., C. J. Liu, Y. Lu, G. Chatterjee, X. Ma, R. N. Eisenman, and P. Lengyel. 2000. The interferon- and differentiation-inducible p202a protein inhibits the transcriptional activity of c-Myc by blocking its association with Max. J. Biol. Chem. 275: 27377–27385.
  • Wang, S., A. Sdrulla, J. E. Johnson, Y. Yokota, and B. A. Barres. 2001. A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development. Neuron 29: 603–614.
  • Weintraub, H., S. D. Hauschka, and S. J. Tapscott. 1991. The MCK enhancer contains a p53 responsive element. Proc. Natl. Acad. Sci. USA 88: 4570–4571.
  • Weintraub, H., S. J. Tapscott, R. L. Davis, M. J. Thayer, M. A. Adam, A. B. Lassar, and A. D. Miller. 1989. 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: 5434–5438.
  • Wright, W. E., D. A. Sassoon, and V. K. Lin. 1989. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56: 607–617.
  • Xin, H., S. D'Souza, L. Fang, P. Lengyel, and D. Choubey. 2001. p202, an interferon-inducible negative regulator of cell growth, is a target of the adenovirus E1A protein. Oncogene 20: 6828–6839.
  • Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725–727.
  • Yokota, Y., A. Mansouri, S. Mori, S. Sugawara, S. Adachi, S. Nishikawa, and P. Gruss. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397: 702–706.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.