Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins
Open accessAbstract
The helix-loop-helix (HLH) protein Id lacks the basic DNA-binding domain common to this class of proteins. In vitro experiments suggested that Id could associate tightly with two other HLH proteins encoded by the E2A gene, E12 and E47 (referred to here collectively as E proteins) and prevent their binding to a sequence present in the muscle creatine kinase (MCK) enhancer either as homo-oligomers or hetero-oligomers with MyoD. In this report we present evidence for the in vivo roles of Id and E proteins: (1) Id and E proteins co-fractionate and co-immunoprecipitate in whole-cell extracts prepared from myoblasts; (2) the loss of Id protein observed during the conversion of proliferating myoblasts into mature myotubes correlates with the formation of MyoD/E hetero-oligomeric complexes in whole-cell extracts (these complexes do not form when purified Id protein is added to the extracts); and (3) stable overexpression of Id mRNA and protein in the C2C12 muscle cell line inhibits differentiation in these cells 16 hr post-induction. The myotubes that do eventually form 48 hr post-induction have no detectable Id protein in the nucleus despite the persistence of exogenous Id mRNA. These data support a model in which Id can inhibit muscle cell differentiation by associating with E proteins and preventing them from forming active hetero-oligomeric complexes with the muscle determination gene products.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pax7+ cells in transcriptional cluster 4 show significant upregulation of Id1, Id2 and Id3, which inhibit differentiation, and of the cell-cycle gene Ccnd1, compared with Pax7− cells in the same cluster.
“When comparing Pax7+ cells in transcriptional cluster 4 with Pax7− cells in the same cluster, we found that Pax7+ cells showed significant upregulation of Id1, Id2 and Id3, which inhibit differentiation (Jen et al., 1992), and of the cell-cycle gene Ccnd1 (Fig. S3D).”
From Aging induces aberrant state transition kinetics in murine muscle stem cells (2020) · cites this paper as Jen et al., 1992
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Antibodies, a laboratory manual
(1989) · Biomedicine & Pharmacotherapy · doi:10.1016/0753-3322(89)90130-3 · Cited by 12,318 · see citing works
Smith, D. B., & Johnson, K. S. (1988) · Gene · doi:10.1016/0378-1119(88)90005-4 · Cited by 5,974 · see citing works
Expression of a single transfected cDNA converts fibroblasts to myoblasts
Davis, R. L., Weintraub, H. M., & Lassar, A. B. (1987) · Cell · doi:10.1016/0092-8674(87)90585-x · Cited by 3,388 · see citing works
Self-citationMurre, C., Page-McCaw, P., & Baltimore, D. (1989) · Cell · doi:10.1016/0092-8674(89)90682-x · Cited by 2,713 · see citing works
The protein Id: A negative regulator of helix-loop-helix DNA binding proteins
Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L., & Weintraub, H. M. (1990) · Cell · doi:10.1016/0092-8674(90)90214-y · Cited by 2,202 · see citing works
Self-citationMurre, C., Page-McCaw, P., Vaessin, H., Caudy, M. A., Jan, L. Y., Jan, Y. N., Cabrera, C. V., Buskin, J. N., Hauschka, S. D., Lassar, A. B., et al. (1989) · Cell · doi:10.1016/0092-8674(89)90434-0 · Cited by 1,815 · see citing works
Self-citationFavaloro, J. M., Treisman, R., & Kamen, R. (1980) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(80)65070-8 · Cited by 1,292 · see citing works
Ron, D., & Habener, J. F. (1992) · Genes & Development · doi:10.1101/gad.6.3.439 · Cited by 1,156 · see citing works
Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro.
Bader, D. M., Masaki, Τ., & Fischman, D. A. (1982) · The Journal of Cell Biology · doi:10.1083/jcb.95.3.763 · Cited by 919 · see citing works
Blackwell, T. K., & Weintraub, H. M. (1990) · Science · doi:10.1126/science.2174572 · Cited by 912 · see citing works
Self-citationMyoD1: A Nuclear Phosphoprotein Requiring a Myc Homology Region to Convert Fibroblasts to Myoblasts
Tapscott, S. J., Davis, R. L., Thayer, M. J., Cheng, P.-F., Weintraub, H. M., & Lassar, A. B. (1988) · Science · doi:10.1126/science.3175662 · Cited by 845 · see citing works
Self-citationLassar, A. B., Davis, R. L., Wright, W. E., Kadesch, T. R., Murre, C., Voronova, A., Baltimore, D., & Weintraub, H. M. (1991) · Cell · doi:10.1016/0092-8674(91)90620-e · Cited by 836 · see citing works
Self-citationLassar, A. B., Buskin, J. N., Lockshon, D., Davis, R. L., Apone, S., Hauschka, S. D., & Weintraub, H. M. (1989) · Cell · doi:10.1016/0092-8674(89)90935-5 · Cited by 817 · see citing works
Self-citationThe MyoD DNA binding domain contains a recognition code for muscle-specific gene activation
Davis, R. L., Cheng, P.-F., Lassar, A. B., & Weintraub, H. (1990) · Cell · doi:10.1016/0092-8674(90)90088-v · Cited by 765 · see citing works
Self-citationId Proteins Id1 and Id2 Selectively Inhibit DNA Binding by One Class of Helix-Loop-Helix Proteins
Sun, X., Copeland, N. G., Jenkins, N. A., & Baltimore, D. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.11.5603 · Cited by 605 · see citing works
Villares, R., & Cabrera, C. V. (1987) · Cell · doi:10.1016/0092-8674(87)90495-8 · Cited by 479 · see citing works
Two Distinct Transcription Factors that Bind the Immunoglobulin Enhancer μE5/κE2 Motif
Henthorn, P. S., Kiledjian, M., & Kadesch, T. R. (1990) · Science · doi:10.1126/science.2105528 · Cited by 450 · see citing works
Ellis, H. M., Spann, D. R., & Posakony, J. W. (1990) · Cell · doi:10.1016/0092-8674(90)90212-w · Cited by 404 · see citing works
Garrell, J., & Modolell, J. (1990) · Cell · doi:10.1016/0092-8674(90)90213-x · Cited by 363 · see citing works
An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene.
Christy, B. A., Sanders, L. K., Lau, L. F., Copeland, N. G., Jenkins, N. A., & Nathans, D. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.5.1815 · Cited by 334 · see citing works
Buskin, J. N., & Hauschka, S. D. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.6.2627 · Cited by 326 · see citing works
Cabrera, C. V., Martínez-Arias, A., & Bate, M. (1987) · Cell · doi:10.1016/0092-8674(87)90496-x · Cited by 263 · see citing works
Inhibition of Myeloid Differentiation by the Helix-Loop-Helix Protein Id
Kreider, B. L., Benezra, R., Rovera, G., & Kadesch, T. R. (1992) · Science · doi:10.1126/science.1372755 · Cited by 253 · see citing works
Self-citationDoren, M. V., Ellis, H. M., & Posakony, J. W. (1991) · Development · doi:10.1242/dev.113.1.245 · Cited by 250 · see citing works
Schlissel, M. S., Voronova, A. F., & Baltimore, D. (1991) · Genes & Development · doi:10.1101/gad.5.8.1367 · Cited by 236 · see citing works
Cell proliferation inhibited by MyoD1 independently of myogenic differentiation
Sorrentino, V., Pepperkok, R., Davis, R. L., Ansorge, W. J., & Philipson, L. (1990) · Nature · doi:10.1038/345813a0 · Cited by 213 · see citing works
I-POU: a POU-domain protein that inhibits neuron-specific gene activation
Treacy, M. N., He, X., & Rosenfeld, M. G. (1991) · Nature · doi:10.1038/350577a0 · Cited by 208 · see citing works
Vaidya, T. B., Rhodes, S. J., Taparowsky, E. J., & Konieczny, S. F. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.8.3576-3579.1989 · Cited by 205 · see citing works
MyoD induces growth arrest independent of differentiation in normal and transformed cells.
Crescenzi, M., Fleming, T. P., Lassar, A. B., Weintraub, H. M., & Aaronson, S. A. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.21.8442 · Cited by 200 · see citing works
Self-citationc-myc Inhibition of MyoD and Myogenin-Initiated Myogenic Differentiation
Miner, J. H., & Wold, B. J. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.5.2842 · Cited by 179 · see citing works
Caudy, M. A., Grell, E. H., Dambly‐Chaudière, C., Ghysen, A., Jan, L. Y., & Jan, Y. N. (1988) · Genes & Development · doi:10.1101/gad.2.7.843 · Cited by 176 · see citing works
González, F., Romani, S., Cubas, P., Modolell, J., & Campuzano, S. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb08527.x · Cited by 171 · see citing works
Brennan, T. J., Edmondson, D. G., Li, L., & Olson, E. N. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.9.3822 · Cited by 161 · see citing works
Parkhurst, S. M., Bopp, D., & Ish‐Horowicz, D. (1990) · Cell · doi:10.1016/0092-8674(90)90414-a · Cited by 158 · see citing works
Cordle, S. R., Henderson, E., Masuoka, H. C., Weil, P. A., & Stein, R. W. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.3.1734 · Cited by 145 · see citing works
Wilson, R. B., Kiledjian, M., Shen, C.-P., Benezra, R., Zwollo, P., Dymecki, S. M., Desiderio, S. V., & Kadesch, T. R. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.12.6185 · Cited by 145 · see citing works
Self-citationPongubala, J. M. R., & Atchison, M. L. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.2.1040 · Cited by 123 · see citing works
Genetic regulation of theAchaete-scute complex ofDrosophila melanogaster
del Prado, J. M., & Garcı́a-Bellido, A. (1984) · Development Genes and Evolution · doi:10.1007/bf01260345 · Cited by 116 · see citing works
Vaidya, T. B., Rhodes, S. J., Taparowsky, E. J., & Konieczny, S. F. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.8.3576 · Cited by 115 · see citing works
Transforming growth factor beta induces myoblast differentiation in the presence of mitogens.
Zentella‐Dehesa, A., & Massagué, J. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.11.5176 · Cited by 95 · see citing works
Schneider, M. D., Perryman, M. B., Payne, P. A., Spizz, G., Roberts, R., & Olson, E. N. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.5.1973 · Cited by 87 · see citing works
Alonso, L. A. G., & Garc�a-Bellido, A. (1988) · Development Genes and Evolution · doi:10.1007/bf00375952 · Cited by 74 · see citing works
The determination of sense organs in Drosophila: interaction of scute with daughterless
Dambly‐Chaudière, C., Ghysen, A., Jan, L. Y., & Jan, Y. N. (1988) · Development Genes and Evolution · doi:10.1007/bf00398993 · Cited by 71 · see citing works
Genetic analysis ofHairy-wing mutations
Alonso, L. G., & Garcı́a-Bellido, A. (1986) · Development Genes and Evolution · doi:10.1007/bf02438959 · Cited by 59 · see citing works
Jun inhibits myogenic differentiation.
Su, H.-Y., Tj, B., Monteclaro, F. S., & Vogt, P. K. (1991) · PubMed · Cited by 33 · see citing works
Grossi, M., Calconi, A., & Tatò, F. (1991) · PubMed · Cited by 18 · see citing works
Herr, W. (1991) · Nature · doi:10.1038/350554a0 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Brennan, T.J. and E.N. Olson. 1991. TGF-{3 represses the actions of myogenin through a mechanism independent of DNA binding. Proc. Natl. Acad. Sci. 88: 3822-3826.
- Blau, T. Kelly, and B. Paterson). Raven Press, New York. (In press.)
- Zentella, A. and J. Massague. 1992. TGF-[3 induces myoblast differentiation in the presence of mitogens. Proc. Natl. Acad. Sci. 89: 5176-5180.
Cited by
Sorted by citations
Understanding Adipocyte Differentiation
Gregoire, F. M., Smas, C. M., & Sul, H. S. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.3.783 · Cited by 2,357 · see citing works
Ying, Q.-L., Nichols, J., Chambers, I., & Smith, A. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00847-x · Cited by 2,114 · see citing works
Katagiri, T. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.127.6.1755 · Cited by 1,452 · see citing works
Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts
Lyden, D. C., Young, A. Z., Zagzag, D., Yan, W. X., Gerald, W. L., O'Reilly, R., Bader, B., Hynes, R. O., Zhuang, Y., Manova, K., et al. (1999) · Nature · doi:10.1038/44334 · Cited by 912 · see citing works
Self-citationKorchynskyi, O., & ten Dijke, P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111023200 · Cited by 876 · see citing works
The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription
Tapscott, S. J. (2005) · Development · doi:10.1242/dev.01874 · Cited by 766 · see citing works
Olson, E. N., & Klein, W. H. (1994) · Genes & Development · doi:10.1101/gad.8.1.1 · Cited by 684 · see citing works
ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis
Norton, J. D. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.22.3897 · Cited by 665 · see citing works
Identification of a novel mechanism of regulation of Ah (dioxin) receptor functionPreprint
Mimura, J., Ema, M., Sogawa, K., & Fujii‐Kuriyama, Y. (1999) · Genes & Development · doi:10.1101/gad.13.1.20 · Cited by 584 · see citing works
A Self-Enabling TGFβ Response Coupled to Stress Signaling
Kang, Y., Chen, C.-R., & Massagué, J. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00109-6 · Cited by 548 · see citing works
Id family of helix-loop-helix proteins in cancer
Perk, J., Iavarone, A., & Benezra, R. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1673 · Cited by 532 · see citing works
Self-citationId Genes Are Direct Targets of Bone Morphogenetic Protein Induction in Embryonic Stem Cells
Hollnagel, A., Oehlmann, V. D., Heymer, J., Rüther, U., & Nordheim, A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.28.19838 · Cited by 522 · see citing works
Genome-wide MyoD Binding in Skeletal Muscle Cells: A Potential for Broad Cellular Reprogramming
Cao, Y., Yao, Z., Sarkar, D., Lawrence, M., Sanchez, G. J., Parker, M. H., MacQuarrie, K. L., Davison, J., Morgan, M. T., Ruzzo, W. L., et al. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.02.014 · Cited by 480 · see citing works
The MyoD family of transcription factors and skeletal myogenesis
Rudnicki, M. A., & Jaenisch, R. (1995) · BioEssays · doi:10.1002/bies.950170306 · Cited by 450 · see citing works
Ellenberger, T., Fass, D., Arnaud, M., & Harrison, S. C. (1994) · Genes & Development · doi:10.1101/gad.8.8.970 · Cited by 445 · see citing works
Id helix—loop—helix proteins in cell growth and differentiation
Norton, J. D., Deed, R. W., Craggs, G., & Sablitzky, F. (1998) · Trends in Cell Biology · doi:10.1016/s0962-8924(98)80013-5 · Cited by 410 · see citing works
Liu, D., Black, B. L., & Derynck, R. (2001) · Genes & Development · doi:10.1101/gad.925901 · Cited by 399 · see citing works
Ishibashi, M., Moriyoshi, K., Sasai, Y., Shiota, K., Nakanishi, S., & Kageyama, R. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06448.x · Cited by 388 · see citing works
Nakashima, K., Takizawa, T., Ochiai, W., Yanagisawa, M., Hisatsune, T., Nakafuku, M., Miyazono, K., Kishimoto, T., Kageyama, R., & Taga, T. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101109698 · Cited by 375 · see citing works
Iavarone, A., Garg, P. P., Lasorella, A., Hsu, J. C., & Israel, M. A. (1994) · Genes & Development · doi:10.1101/gad.8.11.1270 · Cited by 365 · see citing works
Yun, K., & Wold, B. J. (1996) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(96)80091-3 · Cited by 358 · see citing works
Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal
Lassar, A. B., Skapek, S. X., & Novitch, B. G. (1994) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(94)90046-9 · Cited by 337 · see citing works
Berkes, C. A., Bergstrom, D. A., Penn, B. H., Seaver, K. J., Knoepfler, P. S., & Tapscott, S. J. (2004) · Molecular Cell · doi:10.1016/s1097-2765(04)00260-6 · Cited by 332 · see citing works
Inhibition of Myogenic bHLH and MEF2 Transcription Factors by the bHLH Protein Twist
Spicer, D. B., Rhee, J., Cheung, W. L., & Lassar, A. B. (1996) · Science · doi:10.1126/science.272.5267.1476 · Cited by 324 · see citing works
Regulation of the Expression of Cyclin-Dependent Kinase Inhibitor p21 by E2A and Id Proteins
Prabhu, S., Ignatova, A., Park, S. T., & Sun, X.-H. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.10.5888 · Cited by 320 · see citing works
Hara, E., Yamaguchi, T., Nojima, H., Ide, T., Campisi, J., Okayama, H., & Oda, K. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)42146-6 · Cited by 311 · see citing works
Novitch, B. G., Mulligan, G., Jacks, T., & Lassar, A. B. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.2.441 · Cited by 303 · see citing works
Gallea, S., Lallemand, F., Atfi, A., Rawadi, G., Ramez, V., Spinella-Jaegle, S., Kawai, S., Faucheu, C., Huet, L., Baron, R., et al. (2001) · Bone · doi:10.1016/s8756-3282(01)00415-x · Cited by 301 · see citing works
Puri, P., & Sartorelli, V. (2000) · Journal of Cellular Physiology · doi:10.1002/1097-4652(200011)185:2 · Cited by 290 · see citing works
Deciphering the multi-scale, quantitative cis-regulatory code
Kim, S., & Wysocka, J. (2023) · Molecular Cell · doi:10.1016/j.molcel.2022.12.032 · Cited by 282 · see citing works
Id proteins in cell cycle control and cellular senescence
Zebedee, Z., & Hara, E. (2001) · Oncogene · doi:10.1038/sj.onc.1205092 · Cited by 277 · see citing works
Riechmann, V., van Crüchten, I., & Sablitzky, F. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.5.749 · Cited by 272 · see citing works
Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle
Stevenson, E. J., Giresi, P. G., Koncarevic, A., & Kandarian, S. C. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00033.x · Cited by 270 · see citing works
Oatley, M. J., Kaucher, A. V., Racicot, K. E., & Oatley, J. M. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.091330 · Cited by 245 · see citing works
Id2 Specifically Alters Regulation of the Cell Cycle by Tumor Suppressor Proteins
Lasorella, A., Iavarone, A., & Israel, M. A. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.6.2570 · Cited by 239 · see citing works
Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells
Itoh, F., Itoh, S., Goumans, M., Valdimarsdóttir, G., Iso, T., Dotto, G. P., Hamamori, Y., Kedes, L., Kato, M., & ten Dijke, P. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600065 · Cited by 238 · see citing works
High Incidence of T-Cell Tumors in E2A-Null Mice and E2A/Id1 Double-Knockout Mice
Yan, W. X., Young, A. Z., Soares, V., Kelley, R., Benezra, R., & Zhuang, Y. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.12.7317 · Cited by 230 · see citing works
Self-citationDifferential Interactions of Id Proteins with Basic-Helix-Loop-Helix Transcription Factors
Langlands, K., Yin, X., Anand, G., & Prochownik, E. V. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.32.19785 · Cited by 226 · see citing works
Id proteins control growth induction in mammalian cells.
Barone, M. V., Pepperkok, R., Peverali, F. A., & Philipson, L. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.11.4985 · Cited by 225 · see citing works
The Id proteins and angiogenesis
Benezra, R., Rafii, S., & Lyden, D. (2001) · Oncogene · doi:10.1038/sj.onc.1205160 · Cited by 222 · see citing works
Self-citationYokota, Y. (2001) · Oncogene · doi:10.1038/sj.onc.1205090 · Cited by 222 · see citing works
Beger, C., Pierce, L. N., Krüger, M., Marcusson, E. G., Robbins, J. M., Welcsh, P. L., Welch, P. J., Welte, K., King, M., Barber, J. R., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.1.130 · Cited by 219 · see citing works
Consequences of heteromeric interactions among helix-loop-helix proteins.
Kadesch, T. R. (1993) · PubMed · Cited by 217 · see citing works
Role of Id family proteins in growth control
Yokota, Y., & Mori, S. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.10042 · Cited by 214 · see citing works
Yokoyama, S., Ito, Y., Ueno-Kudoh, H., Shimizu, H., Uchibe, K., Albini, S., Mitsuoka, K., Miyaki, S., Kiso, M., Nagai, A., et al. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.10.011 · Cited by 213 · see citing works
Sekido, R., Murai, K., Funahashi, J., Kamachi, Y., Fujisawa‐Sehara, A., Nabeshima, Y., & Kondoh, H. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.9.5692 · Cited by 211 · see citing works
Deficiency in Rhabdomyosarcomas of a Factor Required for MyoD Activity and Myogenesis
Tapscott, S. J., Thayer, M. J., & Weintraub, H. M. (1993) · Science · doi:10.1126/science.8383879 · Cited by 210 · see citing works
Self-citationJen, Y., Manova, K., & Benezra, R. (1997) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199701)208:1 · Cited by 210 · see citing works
Self-citationThe Id-protein family in developmental and cancer-associated pathways
Roschger, C., & Cabrele, C. (2017) · Cell Communication and Signaling · doi:10.1186/s12964-016-0161-y · Cited by 208 · see citing works
Controlling cell fate by bone morphogenetic protein receptors
ten Dijke, P., Korchynskyi, O., Valdimarsdóttir, G., & Goumans, M. (2003) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2003.09.016 · Cited by 199 · see citing works
The Id4 HLH protein and the timing of oligodendrocyte differentiation
Kondo, T., & RAFF, M. C. (2000) · The EMBO Journal · doi:10.1093/emboj/19.9.1998 · Cited by 199 · see citing works
Ono, Y., Calhabeu, F., Morgan, J. E., Katagiri, T., Amthor, H., & Zammit, P. S. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.95 · Cited by 198 · see citing works
E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle‐specific gene transcription
Lluı́s, F., Ballestar, E., Suelves, M., Esteller, M., & Muñoz‐Cánoves, P. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600528 · Cited by 197 · see citing works
Regulation of G1 progression by E2A and Id helix‐loop‐helix proteins.
Peverali, F. A., Ramqvist, T., Saffrich, R., Pepperkok, R., Barone, M. V., & Philipson, L. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06749.x · Cited by 197 · see citing works
The SCL Gene: From Case Report to Critical Hematopoietic Regulator
Begley, C. G., & Green, A. R. (1999) · Blood · doi:10.1182/blood.v93.9.2760 · Cited by 191 · see citing works
Rao, S. S., Chu, C. Y., & Kohtz, D. S. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.8.5259 · Cited by 190 · see citing works
Coupling of Cell Growth Control and Apoptosis Functions of Id Proteins
Norton, J. D., & Atherton, G. T. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.4.2371 · Cited by 186 · see citing works
Jen, Y., Manova, K., & Benezra, R. (1996) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199611)207:3 · Cited by 184 · see citing works
Self-citationSuppression of Mammary Epithelial Cell Differentiation by the Helix-Loop-Helix Protein Id-1
Desprez, P., Hara, E., Bissell, M. J., & Campisi, J. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.6.3398 · Cited by 183 · see citing works
Multiple steps in the regulation of transcription-factor level and activity
Calkhoven, C. F., & Geert, A. B. (1996) · Biochemical Journal · doi:10.1042/bj3170329 · Cited by 180 · see citing works
Yu, L., Liu, C., VanDeusen, J. B., Becknell, B., Dai, Z., Wu, Y.-Z., Raval, A., Liu, T.-H., Ding, W., Mao, C., et al. (2005) · Nature Genetics · doi:10.1038/ng1521 · Cited by 174 · see citing works
Sawada, S., & Littman, D. R. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.9.5620 · Cited by 174 · see citing works
Commitment to natural killer cells requires the helix–loop–helix inhibitor Id2
Ikawa, T., Fujimoto, S., Kawamoto, H., Katsura, Y., & Yokota, Y. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091537598 · Cited by 172 · see citing works
Impaired Immune Responses and B-Cell Proliferation in Mice Lacking the Id3 Gene
Pan, L., Sato, S., Frederick, J. P., Sun, X.-H., & Zhuang, Y. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.9.5969 · Cited by 166 · see citing works
Alway, S. E., Degens, H., Krishnamurthy, G., & Smith, C. A. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00598.2001 · Cited by 165 · see citing works
Ogata, T., Wozney, J. M., Benezra, R., & Noda, M. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.19.9219 · Cited by 164 · see citing works
Self-citationTumor‐associated Carbonic Anhydrases and Their Clinical Significance
Pastoreková, S., Parkkila, S., & Závada, J. (2006) · Advances in clinical chemistry · doi:10.1016/s0065-2423(06)42005-9 · Cited by 159 · see citing works
Regulation of Myostatin on the Growth and Development of Skeletal Muscle
Chen, M., Zhao, Y.-P., Zhao, Y., Deng, S., & Yu, K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.785712 · Cited by 158 · see citing works
Wiring diagrams: regulatory circuits and the control of skeletal myogenesis
Lassar, A. B., & Münsterberg, A. (1994) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(94)90037-x · Cited by 153 · see citing works
Neuhold, L. A., & Wold, B. J. (1993) · Cell · doi:10.1016/0092-8674(93)90725-6 · Cited by 152 · see citing works
Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation
Koyano‐Nakagawa, N., Kim, J., Anderson, D. J., & Kintner, C. R. (2000) · Development · doi:10.1242/dev.127.19.4203 · Cited by 149 · see citing works
A Novel Pathway for Mammary Epithelial Cell Invasion Induced by the Helix-Loop-Helix Protein Id-1
Desprez, P., Lin, C. Q., Thomasset, N., Sympson, C. J., Bissell, M. J., & Campisi, J. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.8.4577 · Cited by 147 · see citing works
Cortactin Associates with the Cell-Cell Junction Protein ZO-1 in both Drosophila and Mouse
Katsube, T., Takahisa, M., Ueda, R., Hashimoto, N., Kobayashi, M., & Togashi, S. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.45.29672 · Cited by 146 · see citing works
I-mf, a Novel Myogenic Repressor, Interacts with Members of the MyoD Family
Chen, C.-M. A., Kraut, N., Groudine, M. T., & Weintraub, H. M. (1996) · Cell · doi:10.1016/s0092-8674(00)80148-8 · Cited by 145 · see citing works
Self-citation4 Genetics of Muscle Determination and Development
Arnold, H.-H., & Braun, T. W. (1999) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60756-5 · Cited by 145 · see citing works
Neural Crest Specification Regulated by the Helix-Loop-Helix Repressor Id2
Martinsen, B. J., & Bronner-Fraser, M. E. (1998) · Science · doi:10.1126/science.281.5379.988 · Cited by 143 · see citing works
Jones, J. M., Montcouquiol, M., Dabdoub, A., Woods, C., & Kelley, M. W. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3859-05.2006 · Cited by 139 · see citing works
Katagiri, T., Akiyama, S., Namiki, M., Komaki, M., Yamaguchi, A., Rosen, V., Wozney, J. M., Fujisawa‐Sehara, A., & Suda, T. (1997) · Experimental Cell Research · doi:10.1006/excr.1996.3432 · Cited by 139 · see citing works
The cdk inhibitor p27Xic1 is required for differentiation of primary neurones inXenopus
Vernon, A. E., Devine, C., & Philpott, A. (2002) · Development · doi:10.1242/dev.00193 · Cited by 137 · see citing works
Skapek, S. X., Rhee, J., Kim, P. S., Novitch, B. G., & Lassar, A. B. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.12.7043 · Cited by 137 · see citing works
Immortalization of primary human keratinocytes by the helix–loop–helix protein, Id-1
Alani, R. M., Hasskarl, J., Grace, M. R., Hernandez, M.-C., Israel, M. A., & Münger, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9637 · Cited by 137 · see citing works
Therrien, M., & Drouin, J. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.4.2342 · Cited by 136 · see citing works
Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD
Friday, B. B., Mitchell, P. O., Kegley, K. M., & Pavlath, G. K. (2003) · Differentiation · doi:10.1046/j.1432-0436.2003.710303.x · Cited by 135 · see citing works
Overexpression of the Helix–Loop–Helix protein Id2 blocks T cell development at multiple stages
Morrow, M. A., Mayer, E. W., Perez, C. A., Adlam, M., & Siu, G. (1999) · Molecular Immunology · doi:10.1016/s0161-5890(99)00071-1 · Cited by 135 · see citing works
Formation of in vivo complexes between the TAL1 and E2A polypeptides of leukemic T cells.
Hsu, H. L., Wadman, I., & Baer, R. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.8.3181 · Cited by 131 · see citing works
Cdk2‐dependent phosphorylation of Id2 modulates activity of E2A‐related transcription factors
Hara, E., Hall, M., & Peters, G. (1997) · The EMBO Journal · doi:10.1093/emboj/16.2.332 · Cited by 128 · see citing works
Lemercier, C., To, R. Q., Carrasco, R. A., & Konieczny, S. F. (1998) · The EMBO Journal · doi:10.1093/emboj/17.5.1412 · Cited by 127 · see citing works
Cadherins Promote Skeletal Muscle Differentiation in Three-dimensional Cultures
Redfield, A. R., Nieman, M. T., & Knudsen, K. A. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.138.6.1323 · Cited by 127 · see citing works
Cell cell interactions in vascular development
Darland, D. C., & D'Amore, P. A. (2001) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(01)52010-4 · Cited by 126 · see citing works
XAP2, a novel hepatitis B virus X-associated protein that inhibits X transactivation
Kuzhandaivelu, N. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.23.4741 · Cited by 123 · see citing works
Inhibitor of Differentiation 1 (Id1) in Cancer and Cancer Therapy
Zhao, Z., Bo, Z., Gong, W., & Guo, Y. (2020) · International Journal of Medical Sciences · doi:10.7150/ijms.42805 · Cited by 122 · see citing works
Myotube formation on gelatin nanofibers – Multi-walled carbon nanotubes hybrid scaffolds
Ostrovidov, S., Shi, X., Zhang, L., Liang, X., Kim, S. B., Fujie, T., Ramalingam, M., Chen, M. W., Nakajima, K., Al-Hazmi, F., et al. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.04.021 · Cited by 119 · see citing works
Tournay, O., & Benezra, R. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.5.2418 · Cited by 118 · see citing works
Self-citationMultiplicity of BMP Signaling in Skeletal Development
Wu, X., Shi, W., & Cao, X. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1402.053 · Cited by 117 · see citing works
Moran, J. L., Li, Y., Hill, A. A. V., Mounts, W. M., & Miller, C. P. (2002) · Physiological Genomics · doi:10.1152/physiolgenomics.00011.2002 · Cited by 117 · see citing works
Hatoum, O. A., Gross-Mesilaty, S., Breitschopf, K., Hoffman, A., Gonen, H., Ciechanover, A. J., & Bengal, E. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.10.5670 · Cited by 116 · see citing works
Mechanisms of Binding Specificity among bHLH Transcription Factors
de Martin, X., Sodaei, R., & Santpere, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179150 · Cited by 114 · see citing works
Regulation of MyoD function in the dividing myoblast
Wei, Q., & Paterson, B. M. (2001) · FEBS Letters · doi:10.1016/s0014-5793(01)02120-2 · Cited by 113 · see citing works
Id-1 expression and cell survival
Wong, Y. C., Wang, X., & Ling, M. T. (2004) · APOPTOSIS · doi:10.1023/b:appt.0000025804.25396.79 · Cited by 112 · see citing works
Simon, H., Nelson, C. E., Goff, D., Laufer, E., Morgan, B. A., & Tabin, C. J. (1995) · Developmental Dynamics · doi:10.1002/aja.1002020102 · Cited by 112 · see citing works
- Authors
- Jen, Y., Weintraub, H., & Benezra, R.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- ORCID
- Benezra, R
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 1992-08
- Volume
- 6
- Issue
- 8
- Pages
- 1466-1479
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- OpenAlex
- W2101927529
- Cited by
- 471
- References
- 47
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 5 · 2023: 1 · 2022: 5 · 2021: 10 · 2020: 9 · 2019: 7 · 2018: 9 · 2017: 9 · 2016: 6 · 2015: 7 · 2014: 15 · 2013: 4 · 2012: 8
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- Id proteins, E12, E47, helix-loop-helix proteins, myogenesis, MyoD, hetero-oligomeric complexes, C2C12 myoblasts, transcriptional repression, myotubes
- MeSH terms
- Animals, Cell Differentiation, Cell Line, DNA-Binding Proteins, Fluorescent Antibody Technique, Muscles, Precipitin Tests, Repressor Proteins, Transcription Factors, Blotting, Northern, Inhibitor of Differentiation Protein 1, TCF Transcription Factors, Transcription Factor 7-Like 1 Protein
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review