BETA3, a Novel Helix-Loop-Helix Protein, Can Act as a Negative Regulator of BETA2 and MyoD-Responsive Genes

REFERENCES

• Akazawa, C., M. Ishibashi, C. Shimizu, S. Nakanishi, and R. Kageyama. 1995. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270:8730–8738.
   PubMed Web of Science ®Google Scholar
• Aplan, P. D., K. Nakahara, S. H. Orkin, and I. R. Kirsch. 1992. The SCL gene product: a positive regulator of erythroid differentiation. EMBO J. 11:4047–4081.
   PubMedGoogle Scholar
• Aronheim, A., H. Ohlsson, C. W. Park, T. Edlund, and M. D. Walker. 1991. Distribution and characterization of helix-loop-helix enhancer binding proteins from pancreatic β cells and lymphocytes. Nucleic Acids Res. 19:3893–3899.
   PubMedGoogle Scholar
• Begley, C. G., P. D. Aplan, S. M. Denning, B. F. Haynes, T. A. Waldmann, and I. R. Kirsch. 1989. The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc. Natl. Acad. Sci. USA 86:10128–10132.
   PubMed Web of Science ®Google Scholar
• Begley, C. G., S. Lipkowitz, V. Göbel, K. A. Mahon, V. Bertness, A. R. Green, N. M. Gough, and I. R. Kirsch. 1992. Molecular characterization of NSCL, a gene encoding a helix-loop-helix protein expressed in the developing nervous system. Proc. Natl. Acad. Sci. USA 89:38–42.
   PubMedGoogle Scholar
• Benezra, R., R. L. Davis, D. Lockshon, D. L. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61:49–59.
   PubMed Web of Science ®Google Scholar
• Boam, D. S. W., A. R. Clark, and K. Docherty. 1990. Positive and negative regulation of the human insulin gene by multiple trans-acting factors. J. Biol. Chem. 265:8285–8296.
   PubMedGoogle Scholar
• Brown, L., and R. Baer. 1994. HEN1 encodes a 20-kilodalton phosphoprotein that binds an extended E-box motif as a homodimer. Mol. Cell. Biol. 14:1245–1255.
   PubMedGoogle Scholar
• Catron, K. M., H. Zhang, S. C. Marshall, J. A. Inostroza, J. M. Wilson, and C. Abate. 1995. Transcriptional repression by Msx-1 does not require home-odomain DNA-binding sites. Mol. Cell. Biol. 15:861–871.
   PubMed Web of Science ®Google Scholar
• Chaney, W. G., D. R. Howard, J. W. Pollard, S. Sallustio, and P. Stanley. 1986. High-frequency transfection of CHO cells using polybrene. Somatic Cell Mol. Genet. 12:237–244.
   PubMedGoogle Scholar
• Cordle, S. R., E. Henderson, H. Masucha, P. A. Weil, and R. Stein. 1991. Pancreatic β-cell-type-specific transcription of the insulin gene is mediated by basic helix-loop-helix DNA-binding proteins. Mol. Cell. Biol. 11:1734–1738.
   PubMedGoogle Scholar
• Crowe, D. T., and M.-J. Tsai. 1989. Mutagenesis of the rat insulin II 5′-flanking region defines sequences important for expression in HIT cells. Mol. Cell. Biol. 9:1784–1789.
   PubMedGoogle Scholar
• Davis, R. L., H. Weintraub, and A. B. Lassar. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987–1000.
   PubMed Web of Science ®Google Scholar
• Davis, R. L., P.-F. Cheng, A. B. Lassar, and H. Weintraub. 1990. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60:733–746.
   PubMedGoogle Scholar
• de Pablo, F., and E. J. de la Rosa. 1995. The developing CNS: a scenario for the action of proinsulin, insulin, and insulin-like growth factors. Trends Neurosci. 18:143–150.
   PubMed Web of Science ®Google Scholar
• Edmondson, D. G., and E. N. Olson. 1989. A single 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.
   PubMedGoogle Scholar
• Ellenberger, T., D. Fass, M. Arnaud, and S. C. Harrison. 1994. Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8:970–980.
   PubMed Web of Science ®Google Scholar
• Fairman, R., R. K. Beran-Steed, S. J. Anthony-Cahill, J. D. Lear, W. F. Stafford III, W. F. DeGrado, P. A. Benfield, and S. L. Brenner. 1993. Multiple oligomeric states regulate the DNA binding of helix-loop-helix peptides. Proc. Natl. Acad. Sci. USA 90:10429–10433.
   PubMed Web of Science ®Google Scholar
• German, M., S. Ashcroft, K. Docherty, H. Edlund, T. Edlund, S. Goodison, G. Kennedy, O. Madsen, D. Melloul, L. Moss, K. Olson, A. Permutt, J. Phillippe, R. P. Robertson, W. J. Rutter, P. Serup, R. Stein, D. Steiner, M.-J. Tsai, and M. D. Walker. 1995. The insulin gene promoter: a simplified nomenclature. Diabetes 44:1002–1004.
   PubMedGoogle Scholar
• German, M. S., M. A. Blanar, C. Nelson, L. G. Moss, and W. J. Rutter. 1991. Two related helix-loop-helix proteins participate in separate cell-specific complexes that bind the insulin enhancer. Mol. Endocrinol. 5:292–299.
   PubMedGoogle Scholar
• Gilman, M.. 1987. Ribonuclease protection assay, p. 4.7.1–4.7.8. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. John Wiley & Sons, New York.
   Google Scholar
• Gobel, V., S. Lipkowitz, C. A. Kozak, and I. R. Kirsch. 1992. NSCL-2: a basic domain helix-loop-helix gene expressed in early neurogenesis. Cell Growth Differ. 3:143–148.
   PubMedGoogle Scholar
• Han, K., and J. L. Manley. 1993. Functional domains of the Drosophila Engrailed protein. EMBO J. 12:2723–2733.
   PubMedGoogle Scholar
• Han, K., and J. L. Manley. 1993. Transcription repression by the Drosophila Even-skipped protein: definition of a minimal repression domain. Genes Dev. 7:491–503.
   PubMedGoogle Scholar
• Henthorn, P., M. Kiledjian, and T. Kadesch. 1990. Two distinct transcription factors that bind the immunoglobulin enhancer mE5/kE2 motif. Science 247:467–470.
   PubMed Web of Science ®Google Scholar
• Hollenberg, S. M., R. Sternglanz, P. F. Cheng, and H. Weintraub. 1995. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol. 15:3813–3822.
   PubMedGoogle Scholar
• Hopwood, N. D., A. Pluck, and J. B. Gurdon. 1989. A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59:893–903.
   PubMed Web of Science ®Google Scholar
• Hsu, H.-L., J.-T. Cheng, Q. Chen, and R. Baer. 1991. Enhancer-binding activity of the tal-1 oncoprotein in association with the E47/E12 helix-loophelix proteins. Mol. Cell. Biol. 11:3037–3042.
   PubMed Web of Science ®Google Scholar
• Hsu, H.-L., L. Huang, J. T. Tsan, W. Funk, W. E. Wright, J.-S. Hu, R. E. Kingston, and R. Baer. 1994. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol. Cell. Biol. 14:1256–1265.
   PubMedGoogle Scholar
• Hu, J.-S., E. N. Olson, and R. E. Kingston. 1992. HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors. Mol. Cell. Biol. 12:1031–1042.
   PubMed Web of Science ®Google Scholar
• Hwung, Y.-P., D. T. Crowe, L.-H. Wang, S. Y. Tsai, and M.-J. Tsai. 1988. The COUP transcription factor binds to an upstream promoter element of the rat insulin II gene. Mol. Cell. Biol. 8:2070–2077.
   PubMed Web of Science ®Google Scholar
• Hwung, Y.-P., Y.-Z. Gu, and M.-J. Tsai. 1990. Cooperativity of sequence elements mediates tissue specificity of the rat insulin II gene. Mol. Cell. Biol. 10:1784–1788.
   PubMedGoogle Scholar
• Jarman, A. P., Y. Grau, L. Y. Jan, and Y. N. Jan. 1993. atonal is a proneural gene that directs organ formation in the Drosophila peripheral nervous system. Cell 73:1307–1321.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Johnson, J. E., S. J. Birren, and D. J. Anderson. 1990. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature (London) 346:858–861.
   PubMed Web of Science ®Google Scholar
• Karlsson, L., T. Edlund, J. B. Moss, W. J. Rutter, and M. D. Walker. 1987. A mutational analysis of the insulin gene transcription control region; expression in beta cells is dependent on two related sequences within the enhancer. Proc. Natl. Acad. Sci. USA 84:8819–8823.
   PubMedGoogle Scholar
• Kozak, M.. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125–8132.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lee, J. E., S. M. Hollenberg, L. Snider, D. L. Turner, N. Lipnick, and H. Weintraub. 1995. Conversion of Xenopus ectoderm into neurons by neuroD, a basic helix-loop-helix protein. Science 268:836–844.
   PubMed Web of Science ®Google Scholar
• Licht, J. D., M. J. Grossel, J. Figge, and U. M. Hansen. 1990. Drosophila Kruppel protein is a transcriptional repressor. Nature (London) 346:76–79.
   PubMedGoogle Scholar
• Madden, S. L., D. M. Cook, and F. J. Tauscher III. 1993. A structure-function analysis of transcriptional repression mediated by the WT1, Wilms tumor suppressor protein. Oncogene 8:1713–1720.
   PubMed Web of Science ®Google Scholar
• Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Mellentin, J. D., S. D. Smith, and M. L. Cleary. 1989. lyl-1, a novel gene altered by chromosomal translocation in T cell leukemia, codes for a protein with a helix-loop-helix DNA binding motif. Cell 58:77–83.
   PubMed Web of Science ®Google Scholar
• Murre, C., P. S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD and myc proteins. Cell 56:777–783.
   PubMed Web of Science ®Google Scholar
• Murre, C., P. S. McCaw, H. Vaessin, M. Caudy, L. Y. Jan, Y. N. Jan, C. V. Cabrera, J. N. Buskin, S. D. Hauschka, A. B. Lassar, H. Weintraub, and D. Baltimore. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537–544.
   PubMed Web of Science ®Google Scholar
• Murre, C., A. Voronova, and D. Baltimore. 1991. B-cell- and myocyte-specific E2-box-binding factors contain E12/E47-like subunits. Mol. Cell. Biol. 11: 1156–1160.
   PubMedGoogle Scholar
• Naya, F. J., C. M. M. Stellrecht, and M.-J. Tsai. 1995. Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev. 8:1009–1019.
   Google Scholar
• Nelson, C., L.-P. Shen, A. Meister, E. Fodor, and W. J. Rutter. 1990. Pan: a transcriptional regulator that binds chymotrypsin, insulin, and AP-4 enhancer motifs. Genes Dev. 4:1035–1043.
   PubMedGoogle Scholar
• Ohsako, S., J. Hyer, G. Panganiban, I. Oliver, and M. Caudy. 1994. hairy functions as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 8:2743–2755.
   PubMedGoogle Scholar
• Peyton, M., L. Moss, and M.-J. Tsai. 1994. Two distinct class A helix-loop-helix transcription factors, E2A and BETA1, form separate DNA binding complexes on the insulin gene E-box. J. Biol. Chem. 269:25936.
   PubMedGoogle Scholar
• Rashbass, J., M. V. Taylor, and J. B. Gurdon. 1992. The DNA-binding protein E12 co-operates with XMyoD in the activation of muscle-specific gene expression in Xenopus embryos. EMBO J. 11:2981–2990.
   PubMedGoogle Scholar
• Saiki, R. K., D. H. Gelfand, S. Stoffel, S. J. Scharf, R. Higuchi, G. T. Horn, K. B. Mullins, and H. A. Erlich. 1988. Primer-directed enzymatic amplification of DNA with thermostable DNA polymerase. Science 239:487–491.
   PubMed Web of Science ®Google Scholar
• Santerre, R. F., R. A. Cook, R. M. D. Crisel, J. D. Sharp, R. J. Schmidt, D. C. Williams, and C. P. Wilson. 1981. Insulin synthesis in a clonal cell line of simian virus 40-transformed hamster pancreatic beta cells. Proc. Natl. Acad. Sci. USA 78:4339–4343.
   PubMed Web of Science ®Google Scholar
• Seed, B., and J.-Y. Sheen. 1988. A simple phase-extraction assay for chloramphenicol acyltransferase activity. Gene 67:271–277.
   PubMed Web of Science ®Google Scholar
• Shieh, S.-Y., and M.-J. Tsai. 1991. Cell-specific and ubiquitous factors are responsible for the enhancer activity of the rat insulin II gene. J. Biol. Chem. 266:16707–16714.
   Google Scholar
• Steiner, D. F., S. J. Chan, J. M. Welsh, and S. C. M. Kwok. 1985. Structure and evolution of the insulin gene. Annu. Rev. Genet. 19:463–484.
   PubMed Web of Science ®Google Scholar
• Stellrecht, C. M. M., F. J. Naya, H.-P. Huang, M. Peyton, and M.-T. Tsai. Unpublished data.
   Google Scholar
• Sternberg, E. A., G. Spizz, W. M. Perry, D. Vizard, T. Weil, and E. N. Olson. 1988. Identification of upstream and intragenic regulatory elements that confer cell-type-restricted and differentiation-specific expression on the muscle creatine kinase gene. Mol. Cell. Biol. 8:2896–2909.
   PubMedGoogle Scholar
• Sun, X.-H., and D. Baltimore. 1991. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell 64:459–470.
   PubMed Web of Science ®Google Scholar
• Thisse, B., C. Stoetzel, C. Gorostiza-Thisse, and F. Perrin-Schmitt. 1988. Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J. 7:2175–2183.
   PubMed Web of Science ®Google Scholar
• Van Doren, M., H. Ellis, and J. W. Posakony. 1991. The Drosophila extram-acrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 113:245–255.
   PubMedGoogle Scholar
• Van Doren, M., A. M. Bailey, J. Esnayra, K. Ede, and J. W. Puma. 1994. Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes Dev. 8:2729–2742.
   PubMedGoogle Scholar
• Villares, R., and C. V. Cabrera. 1987. The achaete-scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50:415–424.
   PubMed Web of Science ®Google Scholar
• Voronova, A., and D. Baltimore. 1990. Mutations that disrupt DNA binding and dimer formation in the E47 helix-loop-helix protein map to distinct domains. Proc. Natl. Acad. Sci. USA 87:4722–4726.
   PubMed Web of Science ®Google Scholar
• Walker, M. D., C. W. Park, A. Rosen, and A. Aronheim. 1990. A cDNA from a mouse pancreatic β cell encoding a putative transcription factor of the insulin gene. Nucleic Acids Res. 18:1159–1166.
   PubMedGoogle Scholar
• Wang, Y., B. W. O’Malley, Jr., S. Y. Tsai, and B. W. O’Malley. 1994. A regulatory system for use in gene transfer. Proc. Natl. Acad. Sci. USA 91:8180–8184.
   PubMed Web of Science ®Google Scholar
• Whelan, J., D. Poon, P. A. Weil, and R. Stein. 1989. Pancreatic β-cell-type-specific expression of the rat insulin II gene is controlled by positive and negative cellular transcriptional elements. Mol. Cell. Biol. 9:3253–3259.
   PubMedGoogle Scholar
• Wolf, C., C. Thisse, C. Stoetzel, B. Thisse, P. Gerlinger, and F. Perrin-Schmitt. 1991. The m-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus x-twist and the Drosophila twist genes. Dev. Biol. 143:363–373.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Xia, Y., L. Brown, C. Y.-C. Yang, J. T. Tsan, M. J. Siciliano, R. Espinosa III, M. M. LeBeau, and R. J. Baer. 1991. TAL2, a helix-loop-helix gene activated by the (7;9)(q34;q32) translocation in human T-cell leukemia. Proc. Natl. Acad. Sci. USA 88:11416–11420.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., J. Babin, A. L. Feldhaus, H. Singh, P. A. Sharp, and M. Bina. 1991. HTF4: a new human helix-loop-helix protein. Nucleic Acids Res. 19:4555.
   PubMed Web of Science ®Google Scholar