Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2

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Mol. Cell. Biol., 03 1996, 952-959, Vol 16, No. 3
Copyright © 1996, American Society for Microbiology

Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2

JJ Hsieh, T Henkel, P Salmon, E Robey, MG Peterson and SD Hayward
Department of Pharmacology and Molecular Sciences, The Johns Hopkins University of Medicine, Baltimore, Maryland 21205, USA.

The Notch/Lin-12/Glp-1 receptor family participates in cell-cell signaling events that influence cell fate decisions. Although several Notch homologs and receptor ligands have been identified, the nuclear events involved in this pathway remain incompletely understood. A truncated form of Notch, consisting only of the intracellular domain (NotchIC), localizes to the nucleus and functions as an activated receptor. Using both an in vitro binding assay and a cotransfection assay based on the two-hybrid principle, we show that mammalian NotchIC interacts with the transcriptional repressor CBF1, which is the human homolog of Drosophila Suppressor of Hairless. Cotransfection assays using segments of mouse NotchIC and CBF1 demonstrated that the N- terminal 114-amino-acid region of mouse NotchIC contains the CBF1 interactive domain and that the cdc10/ankyrin repeats are not essential for this interaction. This result was confirmed in immunoprecipation assays in which the N-terminal 114-amino-acid segment of NotchIC, but not the ankyrin repeat region, coprecipitated with CBF1. Mouse NotchIC itself is targeted to the transcriptional repression domain (aa179 to 361) of CBF1. Furthermore, transfection assays in which mouse NotchIC was targeted through Gal4-CBF1 or through endogenous cellular CBF1 indicated that NotchIC transactivates gene expression via CBF1 tethering to DNA. Transactivation by NotchIC occurs partially through abolition of CBF1-mediated repession. This same mechanism is used by Epstein-Barr virus EBNA2. Thus, mimicry of Notch signal transduction is involved in Epstein-Barr virus-driven immortalization.

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Kitagawa, M., Oyama, T., Kawashima, T., Yedvobnick, B., Kumar, A., Matsuno, K., Harigaya, K. (2001). A Human Protein with Sequence Similarity to Drosophila Mastermind Coordinates the Nuclear Form of Notch and a CSL Protein To Build a Transcriptional Activator Complex on Target Promoters. Mol. Cell. Biol. 21: 4337-4346 [Abstract] [Full Text]
Tang, Z., Kadesch, T. (2001). Identification of a novel activation domain in the Notch-responsive transcription factor CSL. Nucleic Acids Res 29: 2284-2291 [Abstract] [Full Text]
Zhang, J., Chen, H., Weinmaster, G., Hayward, S. D. (2001). Epstein-Barr Virus BamHI-A Rightward Transcript-Encoded RPMS Protein Interacts with the CBF1-Associated Corepressor CIR To Negatively Regulate the Activity of EBNA2 and NotchIC. J. Virol. 75: 2946-2956 [Abstract] [Full Text]
Tani, S., Kurooka, H., Aoki, T., Hashimoto, N., Honjo, T. (2001). The N- and C-terminal regions of RBP-J interact with the ankyrin repeats of Notch1 RAMIC to activate transcription. Nucleic Acids Res 29: 1373-1380 [Abstract] [Full Text]
Höfelmayr, H., Strobl, L. J., Marschall, G., Bornkamm, G. W., Zimber-Strobl, U. (2001). Activated Notch1 Can Transiently Substitute for EBNA2 in the Maintenance of Proliferation of LMP1-Expressing Immortalized B Cells. J. Virol. 75: 2033-2040 [Abstract] [Full Text]
Morimura, T., Miyatani, S., Kitamura, D., Goitsuka, R. (2001). Notch Signaling Suppresses IgH Gene Expression in Chicken B Cells: Implication in Spatially Restricted Expression of Serrate2/Notch1 in the Bursa of Fabricius. J. Immunol. 166: 3277-3283 [Abstract] [Full Text]
Ansieau, S., Strobl, L. J., Leutz, A. (2001). Activation of the Notch-regulated transcription factor CBF1/RBP-J{kappa} through the 13SE1A oncoprotein. Genes Dev. 15: 380-385 [Abstract] [Full Text]
Morrissette, J. J.D., Colliton, R. P., Spinner, N. B. (2001). Defective intracellular transport and processing of JAG1 missense mutations in Alagille syndrome. Hum Mol Genet 10: 405-413 [Abstract] [Full Text]
Dalbiès-Tran, R., Stigger-Rosser, E., Dotson, T., Sample, C. E. (2001). Amino Acids of Epstein-Barr Virus Nuclear Antigen 3A Essential for Repression of J{kappa}-Mediated Transcription and Their Evolutionary Conservation. J. Virol. 75: 90-99 [Abstract] [Full Text]
Peng, R., Tan, J., Ling, P. D. (2000). Conserved Regions in the Epstein-Barr Virus Leader Protein Define Distinct Domains Required for Nuclear Localization and Transcriptional Cooperation with EBNA2. J. Virol. 74: 9953-9963 [Abstract] [Full Text]
Krithivas, A., Young, D. B., Liao, G., Greene, D., Hayward, S. D. (2000). Human Herpesvirus 8 LANA Interacts with Proteins of the mSin3 Corepressor Complex and Negatively Regulates Epstein-Barr Virus Gene Expression in Dually Infected PEL Cells. J. Virol. 74: 9637-9645 [Abstract] [Full Text]
Tan-Pertel, H. T., Walker, L., Browning, D., Miyamoto, A., Weinmaster, G., Gasson, J. C. (2000). Notch Signaling Enhances Survival and Alters Differentiation of 32D Myeloblasts. J. Immunol. 165: 4428-4436 [Abstract] [Full Text]

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