This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Yie, J.
Right arrow Articles by Thanos, D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Yie, J.
Right arrow Articles by Thanos, D.

 Previous Article  |  Next Article 

Mol. Cell. Biol., Jul 1997, 3649-3662, Vol 17, No. 7
Copyright © 1997, American Society for Microbiology

Intra- and intermolecular cooperative binding of high-mobility-group protein I(Y) to the beta-interferon promoter

J Yie, S Liang, M Merika and D Thanos
Department of Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA.

The mammalian high-mobility-group protein I(Y) [HMG I(Y)], while not a typical transcriptional activator, is required for the expression of many eukaryotic genes. HMG I(Y) appears to recruit and stabilize complexes of transcriptional activators through protein-DNA and protein- protein interactions. The protein binds to the minor groove of DNA via three short basic repeats, preferring tracts of adenines and thymines arranged on the same face of the DNA helix. However, the mode by which these three basic repeats function together to recognize HMG I(Y) binding sites has remained unclear. Here, using deletion mutants of HMG I(Y), DNase I footprinting, methylation interference, and in vivo transcriptional assays, we have characterized the binding of HMG I(Y) to the model beta-interferon enhancer. We show that two molecules of HMG I(Y) bind to the enhancer in a highly cooperative fashion, each molecule using a distinct pair of basic repeats to recognize the tandem AT-rich regions of the binding sites. We have also characterized the function of each basic repeat, showing that only the central repeat accounts for specific DNA binding and that the presence of a second repeat bound to an adjacent AT-rich region results in intramolecular cooperativity in binding. Surprisingly, the carboxyl-terminal acidic tail of HMG I(Y) is also important for specific binding in the context of the full-length protein. Our results present a detailed examination of HMG I(Y) binding in an important biological context, which can be extended not only to HMG I(Y) binding in other systems but also to the binding mode of many other proteins containing homologous basic repeats, which have been conserved from bacteria to humans.


This article has been cited by other articles:

  • Garcia-Heras, F., Padmanabhan, S., Murillo, F. J., Elias-Arnanz, M. (2009). Functional equivalence of HMGA- and histone H1-like domains in a bacterial transcriptional factor. Proc. Natl. Acad. Sci. USA 106: 13546-13551 [Abstract] [Full Text]  
  • Falvo, J. V., Lin, C. H., Tsytsykova, A. V., Hwang, P. K., Thanos, D., Goldfeld, A. E., Maniatis, T. (2008). A dimer-specific function of the transcription factor NFATp. Proc. Natl. Acad. Sci. USA 105: 19637-19642 [Abstract] [Full Text]  
  • Young, A. R.J., Narita, M. (2007). Oncogenic HMGA2: short or small?. Genes Dev. 21: 1005-1009 [Full Text]  
  • Metcalf, C. E., Wassarman, D. A. (2006). DNA Binding Properties of TAF1 Isoforms with Two AT-hooks. J. Biol. Chem. 281: 30015-30023 [Abstract] [Full Text]  
  • Murua Escobar, H., Soller, J. T., Richter, A., Meyer, B., Winkler, S., Bullerdiek, J., Nolte, I. (2005). "Best Friends" Sharing the HMGA1 Gene: Comparison of the Human and Canine HMGA1 to Orthologous Other Species. J Hered 96: 777-781 [Abstract] [Full Text]  
  • Dryer, R. L., Covey, L. R. (2005). A Novel NF-{kappa}B-Regulated Site within the Human I{gamma}1 Promoter Requires p300 for Optimal Transcriptional Activity. J. Immunol. 175: 4499-4507 [Abstract] [Full Text]  
  • Chau, K.-Y., Keane-Myers, A. M., Fedele, M., Ikeda, Y., Creusot, R. J., Menozzi, L., Cousins, D. J., Manfioletti, G., Feigenbaum, L., Fusco, A., Ono, S. J. (2005). IFN-{gamma} gene expression is controlled by the architectural transcription factor HMGA1. Int Immunol 17: 297-306 [Abstract] [Full Text]  
  • Crombez, K. R.M.O., Vanoirbeek, E. M.R., Van de Ven, W. J.M., Petit, M. M.R. (2005). Transactivation Functions of the Tumor-Specific HMGA2/LPP Fusion Protein Are Augmented by Wild-Type HMGA2. Mol Cancer Res 3: 63-70 [Abstract] [Full Text]  
  • Galbis-Martinez, M., Fontes, M., Murillo, F. J. (2004). The High-Mobility Group A-Type Protein CarD of the Bacterium Myxococcus xanthus as a Transcription Factor for Several Distinct Vegetative Genes. Genetics 167: 1585-1595 [Abstract] [Full Text]  
  • Harrer, M., Luhrs, H., Bustin, M., Scheer, U., Hock, R. (2004). Dynamic interaction of HMGA1a proteins with chromatin. J. Cell Sci. 117: 3459-3471 [Abstract] [Full Text]  
  • Hommura, F., Katabami, M., Leaner, V. D., Donninger, H., Sumter, T. F., Resar, L. M.S., Birrer, M. J. (2004). HMG-I/Y Is a c-Jun/Activator Protein-1 Target Gene and Is Necessary for c-Jun-Induced Anchorage-Independent Growth in Rat1a Cells. Mol Cancer Res 2: 305-314 [Abstract] [Full Text]  
  • McCarthy, K. M., McDevit, D., Andreucci, A., Reeves, R., Nikolajczyk, B. S. (2003). HMGA1 Co-activates Transcription in B Cells through Indirect Association with DNA. J. Biol. Chem. 278: 42106-42114 [Abstract] [Full Text]  
  • Beitzel, B., Bushman, F. (2003). Construction and analysis of cells lacking the HMGA gene family. Nucleic Acids Res 31: 5025-5032 [Abstract] [Full Text]  
  • Cayuela, M. L., Elias-Arnanz, M., Penalver-Mellado, M., Padmanabhan, S., Murillo, F. J. (2003). The Stigmatella aurantiaca Homolog of Myxococcus xanthus High-Mobility-Group A-Type Transcription Factor CarD: Insights into the Functional Modules of CarD and Their Distribution in Bacteria. J. Bacteriol. 185: 3527-3537 [Abstract] [Full Text]  
  • Chen-Park, F. E., Huang, D.-B., Noro, B., Thanos, D., Ghosh, G. (2002). The kappa B DNA Sequence from the HIV Long Terminal Repeat Functions as an Allosteric Regulator of HIV Transcription. J. Biol. Chem. 277: 24701-24708 [Abstract] [Full Text]  
  • Padmanabhan, S., Elias-Arnanz, M., Carpio, E., Aparicio, P., Murillo, F. J. (2001). Domain Architecture of a High Mobility Group A-type Bacterial Transcriptional Factor. J. Biol. Chem. 276: 41566-41575 [Abstract] [Full Text]  
  • Fedele, M., Battista, S., Manfioletti, G., Croce, C. M., Giancotti, V., Fusco, A. (2001). Role of the high mobility group A proteins in human lipomas. Carcinogenesis 22: 1583-1591 [Abstract] [Full Text]  
  • Fedele, M., Pierantoni, G. M., Berlingieri, M. T., Battista, S., Baldassarre, G., Munshi, N., Dentice, M., Thanos, D., Santoro, M., Viglietto, G., Fusco, A. (2001). Overexpression of Proteins HMGA1 Induces Cell Cycle Deregulation and Apoptosis in Normal Rat Thyroid Cells. Cancer Res. 61: 4583-4590 [Abstract] [Full Text]  
  • Shannon, M. F., Coles, L. S., Attema, J., Diamond, P. (2001). The role of architectural transcription factors in cytokine gene transcription. J. Leukoc. Biol. 69: 21-32 [Abstract] [Full Text]  
  • Henderson, A., Bunce, M., Siddon, N., Reeves, R., Tremethick, D. J. (2000). High-Mobility-Group Protein I Can Modulate Binding of Transcription Factors to the U5 Region of the Human Immunodeficiency Virus Type 1 Proviral Promoter. J. Virol. 74: 10523-10534 [Abstract] [Full Text]  
  • Chau, K.-Y., Munshi, N., Keane-Myers, A., Cheung-Chau, K.-W., Tai, A. K.-F., Manfioletti, G., Dorey, C. K., Thanos, D., Zack, D. J., Ono, S. J. (2000). The Architectural Transcription Factor High Mobility Group I(Y) Participates in Photoreceptor-Specific Gene Expression. J. Neurosci. 20: 7317-7324 [Abstract] [Full Text]  
  • Morisawa, G., Han-yama, A., Moda, I., Tamai, A., Iwabuchi, M., Meshi, T. (2000). AHM1, a Novel Type of Nuclear Matrix-Localized, MAR Binding Protein with a Single AT Hook and a J Domain-Homologous Region. Plant Cell 12: 1903-1916 [Abstract] [Full Text]  
  • Falvo, J. V., Parekh, B. S., Lin, C. H., Fraenkel, E., Maniatis, T. (2000). Assembly of a Functional Beta Interferon Enhanceosome Is Dependent on ATF-2-c-jun Heterodimer Orientation. Mol. Cell. Biol. 20: 4814-4825 [Abstract] [Full Text]  
  • Bagga, R., Michalowski, S., Sabnis, R., Griffith, J. D., Emerson, B. M. (2000). HMG I/Y regulates long-range enhancer-dependent transcription on DNA and chromatin by changes in DNA topology. Nucleic Acids Res 28: 2541-2550 [Abstract] [Full Text]  
  • Schwanbeck, R., Manfioletti, G., Wisniewski, J. R. (2000). Architecture of High Mobility Group Protein I-C{middle dot}DNA Complex and Its Perturbation upon Phosphorylation by Cdc2 Kinase. J. Biol. Chem. 275: 1793-1801 [Abstract] [Full Text]  
  • Powell, J. D., Lerner, C. G., Ewoldt, G. R., Schwartz, R. H. (1999). The -180 Site of the IL-2 Promoter Is the Target of CREB/CREM Binding in T Cell Anergy. J. Immunol. 163: 6631-6639 [Abstract] [Full Text]  
  • Hennig, Y., Deichert, U., Bonk, U., Thode, B., Bartnitzke, S., Bullerdiek, J. (1999). Chromosomal translocations affecting 12q14-15 but not deletions of the long arm of chromosome 7 associated with a growth advantage of uterine smooth muscle cells. Mol Hum Reprod 5: 1150-1154 [Abstract] [Full Text]  
  • Yie, J., Senger, K., Thanos, D. (1999). Mechanism by which the IFN-beta enhanceosome activates transcription. Proc. Natl. Acad. Sci. USA 96: 13108-13113 [Abstract] [Full Text]  
  • Bustin, M. (1999). Regulation of DNA-Dependent Activities by the Functional Motifs of the High-Mobility-Group Chromosomal Proteins. Mol. Cell. Biol. 19: 5237-5246 [Full Text]  
  • Zhang, X. M., Verdine, G. L. (1999). A Small Region in HMG I(Y) Is Critical for Cooperation with NF-kappa B on DNA. J. Biol. Chem. 274: 20235-20243 [Abstract] [Full Text]  
  • Bonnefoy, E., Bandu, M.-T., Doly, J. (1999). Specific Binding of High-Mobility-Group I (HMGI) Protein and Histone H1 to the Upstream AT-Rich Region of the Murine Beta Interferon Promoter: HMGI Protein Acts as a Potential Antirepressor of the Promoter. Mol. Cell. Biol. 19: 2803-2816 [Abstract] [Full Text]  
  • Ping, D., Boekhoudt, G. H., Rogers, E. M., Boss, J. M. (1999). Nuclear Factor-{kappa}B p65 Mediates the Assembly and Activation of the TNF-Responsive Element of the Murine Monocyte Chemoattractant-1 Gene. J. Immunol. 162: 727-734 [Abstract] [Full Text]  
  • MUNSHI, N., YIE, J., MERIKA, M., SENGER, K., LOMVARDAS, S., AGALIOTI, T., THANOS, D. (1999). The IFN-{beta} Enhancer: A Paradigm for Understanding Activation and Repression of Inducible Gene Expression. Cold Spring Harb Symp Quant Biol 64: 149-160 [Abstract]  
  • Gobin, S. J. P., Keijsers, V., van Zutphen, M., van den Elsen, P. J. (1998). The Role of Enhancer A in the Locus-Specific Transactivation of Classical and Nonclassical HLA Class I Genes by Nuclear Factor {kappa}B. J. Immunol. 161: 2276-2283 [Abstract] [Full Text]  
  • Frank, O., Schwanbeck, R., Wisniewski, J. R. (1998). Protein Footprinting Reveals Specific Binding Modes of a High Mobility Group Protein I to DNAs of Different Conformation. J. Biol. Chem. 273: 20015-20020 [Abstract] [Full Text]  
  • Chin, M. T., Pellacani, A., Wang, H., Lin, S. S. J., Jain, M. K., Perrella, M. A., Lee, M.-E. (1998). Enhancement of Serum-response Factor-dependent Transcription and DNA Binding by the Architectural Transcription Factor HMG-I(Y). J. Biol. Chem. 273: 9755-9760 [Abstract] [Full Text]  
  • Amirand, C, Viari, A, Ballini, J., Rezaei, H, Beaujean, N, Jullien, D, Kas, E, Debey, P (1998). Three distinct sub-nuclear populations of HMG-I protein of different properties revealed by co-localization image analysis. J. Cell Sci. 111: 3551-3561 [Abstract]  
  • MANIATIS, T., FALVO, J.V., KIM, T.H., KIM, T.K., LIN, C.H., PAREKH, B.S., WATHELET, M.G. (1998). Structure and Function of the Interferon-{beta} Enhanceosome. Cold Spring Harb Symp Quant Biol 63: 609-620 [Abstract]  
  • Arlotta, P., Tai, A. K.-F., Manfioletti, G., Clifford, C., Jay, G., Ono, S. J. (2000). Transgenic Mice Expressing a Truncated Form of the High Mobility Group I-C Protein Develop Adiposity and an Abnormally High Prevalence of Lipomas. J. Biol. Chem. 275: 14394-14400 [Abstract] [Full Text]  
  • Vorachek, W. R., Steppan, C. M., Lima, M., Black, H., Bhattacharya, R., Wen, P., Kajiyama, Y., Locker, J. (2000). Distant Enhancers Stimulate the Albumin Promoter through Complex Proximal Binding Sites. J. Biol. Chem. 275: 29031-29041 [Abstract] [Full Text]  
  • Piekielko, A., Drung, A., Rogalla, P., Schwanbeck, R., Heyduk, T., Gerharz, M., Bullerdiek, J., Wisniewski, J. R. (2001). Distinct Organization of DNA Complexes of Various HMGI/Y Family Proteins and Their Modulation upon Mitotic Phosphorylation. J. Biol. Chem. 276: 1984-1992 [Abstract] [Full Text]  
  • Bing, Z., Huang, J. H., Liao, W. S.-L. (2000). NFkappa B Interacts with Serum Amyloid A3 Enhancer Factor to Synergistically Activate Mouse Serum Amyloid A3 Gene Transcription. J. Biol. Chem. 275: 31616-31623 [Abstract] [Full Text]  
  • Lewis, R. T., Andreucci, A., Nikolajczyk, B. S. (2001). PU.1-mediated Transcription Is Enhanced by HMG-I(Y)-dependent Structural Mechanisms. J. Biol. Chem. 276: 9550-9557 [Abstract] [Full Text]  
  • Yoo, J.-Y., Wang, W., Desiderio, S., Nathans, D. (2001). Synergistic Activity of STAT3 and c-Jun at a Specific Array of DNA Elements in the alpha 2-Macroglobulin Promoter. J. Biol. Chem. 276: 26421-26429 [Abstract] [Full Text]  
  • Schwanbeck, R., Gymnopoulos, M., Petry, I., Piekielko, A., Szewczuk, Z., Heyduk, T., Zechel, K., Wisniewski, J. R. (2001). Consecutive Steps of Phosphorylation Affect Conformation and DNA Binding of the Chironomus High Mobility Group A Protein. J. Biol. Chem. 276: 26012-26021 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»