Molecular Mechanism Governing Heme Signaling in Yeast: a Higher-Order Complex Mediates Heme Regulation of the Transcriptional Activator HAP1

REFERENCES

• Bengal, E., O. Flores, P. N. Rangarajan, A. Chen, H. Weintraub, and I. M. Verma 1994. Positive control mutations in the MyoD basic region fail to show cooperative DNA binding and transcriptional activation in vitro. Proc. Natl. Acad. Sci. USA 91: 6221–6225.
   PubMed Web of Science ®Google Scholar
• Bohen, S. P., A. Kralli, and K. R. Yamamoto 1995. Hold ’em and fold ’em: chaperones and signal transduction. Science 268: 1303–1304 (Comment.)
   PubMed Web of Science ®Google Scholar
• Caplan, A. J., E. Langley, E. M. Wilson, and J. Vidal 1995. Hormone-dependent transactivation by the human androgen receptor is regulated by a dnaJ protein. J. Biol. Chem. 270: 5251–5257.
   PubMedGoogle Scholar
• Caplan, A. J., J. Tsai, P. J. Casey, and M. G. Douglas 1992. Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J. Biol. Chem. 267: 18890–18895.
   PubMed Web of Science ®Google Scholar
• Chang, H. C., D. F. Nathan, and S. Lindquist 1997. In vivo analysis of the Hsp90 cochaperone Sti1 (p60). Mol. Cell. Biol. 17: 318–325.
   PubMedGoogle Scholar
• Charnay, P., and T. Maniatis 1983. Transcriptional regulation of globin gene expression in the human erythroid cell line K562. Science 220: 1281–1283.
   PubMed Web of Science ®Google Scholar
• Chen, J. J., M. S. Throop, L. Gehrke, I. Kuo, J. K. Pal, M. Brodsky, and I. M. London 1991. Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2 alpha (eIF-2 alpha) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2 alpha kinase. Proc. Natl. Acad. Sci. USA 88: 7729–7733.
   PubMed Web of Science ®Google Scholar
• Creusot, F., J. Verdiere, M. Gaisne, and P. P. Slonimski 1988. CYP1 (HAP1) regulator of oxygen-dependent gene expression in yeast. I. Overall organization of the protein sequence displays several novel structural domains. J. Mol. Biol. 204: 263–276.
   PubMedGoogle Scholar
• Dean, A., T. J. Ley, R. K. Humphries, M. Fordis, and A. N. Schechter 1983. Inducible transcription of five globin genes in K562 human leukemia cells. Proc. Natl. Acad. Sci. USA 80: 5515–5519.
   PubMedGoogle Scholar
• Forsburg, S. L., and L. Guarente 1989. Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes Dev. 3: 1166–1178.
   PubMedGoogle Scholar
• Fytlovich, S., M. Gervais, C. Agrimonti, and B. Guiard 1993. Evidence for an interaction between the CYP1 (HAP1) activator and a cellular factor during heme-dependent transcriptional regulation in the yeast Saccharomyces cerevisiae. EMBO J. 12: 1209–1218.
   PubMedGoogle Scholar
• Gardner, K. H., S. F. Anderson, and J. E. Coleman 1995. Solution structure of the Kluyveromyces lactis LAC9 Cd2 Cys6 DNA-binding domain. Nat. Struct. Biol. 2: 898–905.
   PubMedGoogle Scholar
• Goldberg, M. A., S. P. Dunning, and H. F. Bunn 1988. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242: 1412–1415.
   PubMed Web of Science ®Google Scholar
• Gosink, K. K., T. Gaal, A. J. T. Bokal, and R. L. Gourse 1996. A positive control mutant of the transcription activator protein FIS. J. Bacteriol. 178: 5182–5187.
   PubMedGoogle Scholar
• Guarente, L., B. Lalonde, P. Gifford, and E. Alani 1984. Distinctly regulated tandem upstream activation sites mediate catabolite repression of the CYC1 gene of S. cerevisiae. Cell 36: 503–511.
   PubMed Web of Science ®Google Scholar
• Haldi, M. L., and L. Guarente 1995. Multiple domains mediate heme control of the yeast activator HAP1. Mol. Gen. Genet. 248: 229–235.
   PubMedGoogle Scholar
• Harlow, E., and D. Lane 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Hinnebusch, A. G. 1984. Evidence for translational regulation of the activator of general amino acid control in yeast. Proc. Natl. Acad. Sci. USA 81: 6442–6446.
   PubMed Web of Science ®Google Scholar
• Hortner, H., G. Ammerer, E. Hartter, B. Hamilton, J. Rytka, T. Bilinski, and H. Ruis 1982. Regulation of synthesis of catalases and iso-1-cytochrome c in Saccharomyces cerevisiae by glucose, oxygen and heme. Eur. J. Biochem. 128: 179–184.
   PubMedGoogle Scholar
• Kim, K. S., and L. Guarente 1989. Mutations that alter transcriptional activation but not DNA binding in the zinc finger of yeast activator HAPI. Nature 342: 200–203.
   PubMedGoogle Scholar
• Kimura, Y., I. Yahara, and S. Lindquist 1995. Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 268: 1362–1365.
   PubMedGoogle Scholar
• Kuwabara, K., S. Ogawa, M. Matsumoto, S. Koga, M. Clauss, D. J. Pinsky, P. Lyn, J. Leavy, L. Witte, J. Joseph-Silverstein, et al. 1995. Hypoxia-mediated induction of acidic/basic fibroblast growth factor and platelet-derived growth factor in mononuclear phagocytes stimulates growth of hypoxic endothelial cells. Proc. Natl. Acad. Sci. USA 92: 4606–4610.
   PubMed Web of Science ®Google Scholar
• Labbe-Rois, R., and P. Labbe 1990. Tetrapyrrole and heme biosynthesis in the yeast Saccharomyces cerevisiae Biosynthesis of heme and chlorophylls. In: Dailey, H. A.235–285Green Publishing Associates and Wiley-Interscience, New York, N.Y.
   Google Scholar
• Lathrop, J. T., and M. P. Timko 1993. Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259: 522–525.
   PubMed Web of Science ®Google Scholar
• Levy, A. P., N. S. Levy, J. Loscalzo, A. Calderone, N. Takahashi, K. T. Yeo, G. Koren, W. S. Colucci, and M. A. Goldberg 1995. Regulation of vascular endothelial growth factor in cardiac myocytes. Circ. Res. 76: 758–766.
   PubMed Web of Science ®Google Scholar
• Marczak, J. E., and M. C. Brandriss 1991. Analysis of constitutive and noninducible mutations of the PUT3 transcriptional activator. Mol. Cell. Biol. 11: 2609–2619.
   PubMedGoogle Scholar
• Marmorstein, R., M. Carey, M. Ptashne, and S. C. Harrison 1992. DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356: 408–414.
   PubMed Web of Science ®Google Scholar
• Marmorstein, R., and S. C. Harrison 1994. Crystal structure of a PPR1-DNA complex: DNA recognition by proteins containing a Zn2Cys6 binuclear cluster. Genes Dev. 8: 2504–2512.
   PubMed Web of Science ®Google Scholar
• Mattoon, J., W. Lancashire, H. Sanders, E. Carvajal, D. Malamud, G. Braz, and A. Panek 1979. Oxygen and catabolite regulation of hemoprotein biosynthesis in the yeast Saccharomyces cerevisiae Biosynthesis of heme and cholorophylls. In: Caughey, W. J.421–435Academic Press, New York, N.Y.
   Google Scholar
• Molkentin, J. D., B. L. Black, J. F. Martin, and E. N. Olson 1996. Mutational analysis of the DNA binding, dimerization, and transcriptional activation domains of MEF2C. Mol. Cell. Biol. 16: 2627–2636.
   PubMedGoogle Scholar
• Padmanaban, G., V. Venkateswar, and P. N. Rangarajan 1989. Haem as a multifunctional regulator. Trends Biochem. Sci. 14: 492–496.
   PubMed Web of Science ®Google Scholar
• Palma, J. F., X. Gao, C. H. Lin, S. Wu, and W. B. Solomon 1994. Iron protoporphyrin IX (hemin) but not tin or zinc protoporphyrin IX can stimulate gene expression in K562 cells from enhancer elements containing binding sites for NF-E2. Blood 84: 1288–1297.
   PubMedGoogle Scholar
• Pfeifer, K., K. S. Kim, S. Kogan, and L. Guarente 1989. Functional dissection and sequence of yeast HAP1 activator. Cell 56: 291–301.
   PubMed Web of Science ®Google Scholar
• Pfeifer, K., T. Prezant, and L. Guarente 1987. Yeast HAP1 activator binds to two upstream activation sites of different sequence. Cell 49: 19–27.
   PubMedGoogle Scholar
• Picard, D., B. Khursheed, M. J. Garabedian, M. G. Fortin, S. Lindquist, and K. R. Yamamoto 1990. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348: 166–168.
   PubMed Web of Science ®Google Scholar
• Rangarajan, P. N., and G. Padmanaban 1989. Regulation of cytochrome P-450b/e gene expression by a heme- and phenobarbitone-modulated transcription factor. Proc. Natl. Acad. Sci. USA 86: 3963–3967.
   PubMed Web of Science ®Google Scholar
• Reddy, S. V., O. Alcantara, G. D. Roodman, and D. H. Boldt 1996. Inhibition of tartrate-resistant acid phosphatase gene expression by hemin and protoporphyrin IX. Identification of a hemin-responsive inhibitor of transcription. Blood 88: 2288–2297.
   PubMed Web of Science ®Google Scholar
• Reece, R. J., and M. Ptashne 1993. Determinants of binding-site specificity among yeast C6 zinc cluster proteins. Science 261: 909–911.
   PubMedGoogle Scholar
• Siddiqui, A. H., and M. C. Brandriss 1989. The Saccharomyces cerevisiae PUT3 activator protein associates with proline-specific upstream activation sequences. Mol. Cell. Biol. 9: 4706–4712.
   PubMedGoogle Scholar
• Smith, D. F., L. E. Faber, and D. O. Toft 1990. Purification of unactivated progesterone receptor and identification of novel receptor-associated proteins. J. Biol. Chem. 265: 3996–4003.
   PubMedGoogle Scholar
• Sze, J. Y., E. Remboutsika, and G. B. Kohlhaw 1993. Transcriptional regulator Leu3 of Saccharomyces cerevisiae: separation of activator and repressor functions. Mol. Cell. Biol. 13: 5702–5709.
   PubMedGoogle Scholar
• Turcotte, B., and L. Guarente 1992. HAP1 positive control mutants specific for one of two binding sites. Genes Dev. 6: 2001–2009.
   PubMedGoogle Scholar
• Williams, F. E., U. Varanasi, and R. J. Trumbly 1991. The CYC8 and TUP1 proteins involved in glucose repression in Saccharomyces cerevisiae are associated in a protein complex. Mol. Cell. Biol. 11: 3307–3316.
   PubMed Web of Science ®Google Scholar
• Zhang, L., M. O. Bermingham, B. Turcotte, and L. Guarente 1993. Antibody-promoted dimerization bypasses the regulation of DNA binding by the heme domain of the yeast transcriptional activator HAP1. Proc. Natl. Acad. Sci. USA 90: 2851–2855.
   PubMedGoogle Scholar
• Zhang, L., and L. Guarente 1996. The C6 zinc cluster dictates asymmetric binding by HAP1. EMBO J. 15: 4676–4681.
   PubMed Web of Science ®Google Scholar
• Zhang, L., and L. Guarente 1994. Evidence that TUP1/SSN6 has a positive effect on the activity of the yeast activator HAP1. Genetics 136: 813–817.
   PubMedGoogle Scholar
• Zhang, L., and L. Guarente 1994. HAP1 is nuclear but is bound to a cellular factor in the absence of heme. J. Biol. Chem. 269: 14643–14647.
   PubMedGoogle Scholar
• Zhang, L., and L. Guarente 1995. Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J. 14: 313–320.
   PubMed Web of Science ®Google Scholar
• Zhang, L., and L. Guarente 1994. The yeast activator HAP1—a GAL4 family member—binds DNA in a directly repeated orientation. Genes Dev. 8: 2110–2119.
   PubMedGoogle Scholar
• Zitomer, R. S., and C. V. Lowry 1992. Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol. Rev. 56: 1–11.
   PubMedGoogle Scholar