Disrupting Vesicular Trafficking at the Endosome Attenuates Transcriptional Activation by Gcn4

REFERENCES

• Alani, E., L. Cao, and N. Kleckner. 1987. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116:541–545.
   PubMedGoogle Scholar
• Babst, M. 2005. A protein's final ESCRT. Traffic 6:2–9.
   PubMed Web of Science ®Google Scholar
• Babst, M., D. J. Katzmann, E. J. Estepa-Sabal, T. Meerloo, and S. D. Emr. 2002. Escrt-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev. Cell 3:271–282.
   PubMed Web of Science ®Google Scholar
• Babst, M., B. Wendland, E. J. Estepa, and S. D. Emr. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17:2982–2993.
   PubMed Web of Science ®Google Scholar
• Backer, J. M. 2008. The regulation and function of class III PI3Ks: novel roles for Vps34. Biochem. J. 410:1–17.
   PubMed Web of Science ®Google Scholar
• Balciunas, D., M. Hallberg, S. Bjorklund, and H. Ronne. 2003. Functional interactions within yeast mediator and evidence of differential subunit modifications. J. Biol. Chem. 278:3831–3839.
   PubMedGoogle Scholar
• Barwell, K. J., J. H. Boysen, W. Xu, and A. P. Mitchell. 2005. Relationship of DFG16 to the Rim101p pH response pathway in Saccharomyces cerevisiae and Candida albicans. Eukaryot. Cell 4:890–899.
   PubMedGoogle Scholar
• Bowers, K., and T. H. Stevens. 2005. Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1744:438–454.
   PubMed Web of Science ®Google Scholar
• Boysen, J. H., and A. P. Mitchell. 2006. Control of Bro1-domain protein Rim20 localization by external pH, ESCRT machinery, and the Saccharomyces cerevisiae Rim101 pathway. Mol. Biol. Cell 17:1344–1353.
   PubMedGoogle Scholar
• Burd, C. G., M. Peterson, C. R. Cowles, and S. D. Emr. 1997. A novel Sec18p/NSF-dependent complex required for Golgi-to-endosome transport in yeast. Mol. Biol. Cell 8:1089–1104.
   PubMedGoogle Scholar
• Cherkasova, V. A., and A. G. Hinnebusch. 2003. Translational control by TOR and TAP42 through dephosphorylation of eIF2α kinase GCN2. Genes Dev. 17:859–872.
   PubMed Web of Science ®Google Scholar
• Cigan, A. M., M. Foiani, E. M. Hannig, and A. G. Hinnebusch. 1991. Complex formation by positive and negative translational regulators of GCN4. Mol. Cell. Biol. 11:3217–3228.
   PubMedGoogle Scholar
• De Filippi, L., M. Fournier, E. Cameroni, P. Linder, C. De Virgilio, M. Foti, and O. Deloche. 2007. Membrane stress is coupled to a rapid translational control of gene expression in chlorpromazine-treated cells. Curr. Genet. 52:171–185.
   PubMed Web of Science ®Google Scholar
• Deloche, O., J. de la Cruz, D. Kressler, M. Doere, and P. Linder. 2004. A membrane transport defect leads to a rapid attenuation of translation initiation in Saccharomyces cerevisiae. Mol. Cell 13:357–366.
   PubMedGoogle Scholar
• Donahue, T. F., and A. M. Cigan. 1988. Genetic selection for mutations that reduce or abolish ribosomal recognition of the HIS4 translational initiator region. Mol. Cell. Biol. 8:2955–2963.
   PubMedGoogle Scholar
• Drysdale, C. M., E. Dueñas, B. M. Jackson, U. Reusser, G. H. Braus, and A. G. Hinnebusch. 1995. The transcriptional activator GCN4 contains multiple activation domains that are critically dependent on hydrophobic amino acids. Mol. Cell. Biol. 15:1220–1233.
   PubMed Web of Science ®Google Scholar
• Fuller, R. S., A. Brake, and J. Thorner. 1989. Yeast prohormone processing enzyme (KEX2 gene product) is a Ca2+-dependent serine protease. Proc. Natl. Acad. Sci. USA 86:1434–1438.
   PubMedGoogle Scholar
• Gao, M., and C. A. Kaiser. 2006. A conserved GTPase-containing complex is required for intracellular sorting of the general amino-acid permease in yeast. Nat. Cell Biol. 8:657–667.
   PubMedGoogle Scholar
• Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El-Bakkoury, R. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Guldener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C. Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391.
   PubMed Web of Science ®Google Scholar
• Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534.
   PubMed Web of Science ®Google Scholar
• Govind, C. K., S. Yoon, H. Qiu, S. Govind, and A. G. Hinnebusch. 2005. Simultaneous recruitment of coactivators by Gcn4p stimulates multiple steps of transcription in vivo. Mol. Cell. Biol. 25:5626–5638.
   PubMedGoogle Scholar
• Grundmann, O., H. U. Mosch, and G. H. Braus. 2001. Repression of GCN4 mRNA translation by nitrogen starvation in Saccharomyces cerevisiae. J. Biol. Chem. 276:25661–25671.
   PubMedGoogle Scholar
• Gyuris, J., E. Golemis, H. Chertkov, and R. Brent. 1993. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75:791–803.
   PubMed Web of Science ®Google Scholar
• Han, G. S., A. Audhya, D. J. Markley, S. D. Emr, and G. M. Carman. 2002. The Saccharomyces cerevisiae LSB6 gene encodes phosphatidylinositol 4-kinase activity. J. Biol. Chem. 277:47709–47718.
   PubMed Web of Science ®Google Scholar
• Hanes, S. D., and R. Brent. 1989. DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell 57:1275–1283.
   PubMedGoogle Scholar
• Harashima, S., E. M. Hannig, and A. G. Hinnebusch. 1987. Interactions between positive and negative regulators of GCN4 controlling gene expression and entry into the yeast cell cycle. Genetics 117:409–419.
   PubMedGoogle Scholar
• Hayashi, M., T. Fukuzawa, H. Sorimachi, and T. Maeda. 2005. Constitutive activation of the pH-responsive Rim101 pathway in yeast mutants defective in late steps of the MVB/ESCRT pathway. Mol. Cell. Biol. 25:9478–9490.
   PubMedGoogle Scholar
• Hinnebusch, A. G. 1992. General and pathway-specific regulatory mechanisms controlling the synthesis of amino acid biosynthetic enzymes in Saccharomyces cerevisiae, p. 319-414. In J. R. Broach, E. W. Jones, and J. R. Pringle (ed.), The molecular and cellular biology of the yeast Saccharomyces: gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Hinnebusch, A. G. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59:407–450.
   PubMed Web of Science ®Google Scholar
• Hinnebusch, A. G., G. Lucchini, and G. R. Fink. 1985. A synthetic HIS4 regulatory element confers general amino acid control on the cytochrome c gene CYC1 of yeast. Proc. Natl. Acad. Sci. USA 82:498–502.
   PubMed Web of Science ®Google Scholar
• Hinnebusch, A. G., and K. Natarajan. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1:22–32.
   PubMedGoogle Scholar
• Jia, M. H., R. A. Larossa, J. M. Lee, A. Rafalski, E. Derose, G. Gonye, and Z. Xue. 2000. Global expression profiling of yeast treated with an inhibitor of amino acid biosynthesis, sulfometuron methyl. Physiol. Genomics 3:83–92.
   PubMedGoogle Scholar
• Jones, E. W. 1991. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 194:428–453.
   PubMedGoogle Scholar
• Kaksonen, M., C. P. Toret, and D. G. Drubin. 2005. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123:305–320.
   PubMed Web of Science ®Google Scholar
• Katzmann, D. J., G. Odorizzi, and S. D. Emr. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893–905.
   PubMed Web of Science ®Google Scholar
• Kihara, A., T. Noda, N. Ishihara, and Y. Ohsumi. 2001. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152:519–530.
   PubMed Web of Science ®Google Scholar
• Kim, S. J., M. J. Swanson, H. Qiu, C. K. Govind, and A. G. Hinnebusch. 2005. Activator Gcn4p and Cyc8p/Tup1p are interdependent for promoter occupancy at ARG1 in vivo. Mol. Cell. Biol. 25:11171–11183.
   PubMedGoogle Scholar
• Kornitzer, D. 2002. Monitoring protein degradation. Methods Enzymol. 351:639–647.
   PubMed Web of Science ®Google Scholar
• Li, Y., R. D. Moir, I. K. Sethy-Coraci, J. R. Warner, and I. M. Willis. 2000. Repression of ribosome and tRNA synthesis in secretion-defective cells is signaled by a novel branch of the cell integrity pathway. Mol. Cell. Biol. 20:3843–3851.
   PubMed Web of Science ®Google Scholar
• Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
   PubMed Web of Science ®Google Scholar
• Martin, C., and R. A. Young. 1989. KEX2 mutations suppress RNA polymerase II mutants and alter the temperature range of yeast cell growth. Mol. Cell. Biol. 9:2341–2349.
   PubMedGoogle Scholar
• Nanduri, J., S. Mitra, C. Andrei, Y. Liu, Y. Yu, M. Hitomi, and A. M. Tartakoff. 1999. An unexpected link between the secretory path and the organization of the nucleus. J. Biol. Chem. 274:33785–33789.
   PubMedGoogle Scholar
• Nanduri, J., and A. M. Tartakoff. 2001. The arrest of secretion response in yeast: signaling from the secretory path to the nucleus via Wsc proteins and Pkc1p. Mol. Cell 8:281–289.
   PubMedGoogle Scholar
• Natarajan, K., B. M. Jackson, E. Rhee, and A. G. Hinnebusch. 1998. yTAFII61 has a general role in RNA polymerase II transcription and is required by Gcn4p to recruit the SAGA coactivator complex. Mol. Cell 2:683–692.
   PubMedGoogle Scholar
• Natarajan, K., M. R. Meyer, B. M. Jackson, D. Slade, C. Roberts, A. G. Hinnebusch, and M. J. Marton. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21:4347–4368.
   PubMed Web of Science ®Google Scholar
• Nierras, C. R., and J. R. Warner. 1999. Protein kinase C enables the regulatory circuit that connects membrane synthesis to ribosome synthesis in Saccharomyces cerevisiae. J. Biol. Chem. 274:13235–13241.
   PubMedGoogle Scholar
• Nobukuni, T., M. Joaquin, M. Roccio, S. G. Dann, S. Y. Kim, P. Gulati, M. P. Byfield, J. M. Backer, F. Natt, J. L. Bos, F. J. Zwartkruis, and G. Thomas. 2005. Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OH-kinase. Proc. Natl. Acad. Sci. USA 102:14238–14243.
   PubMed Web of Science ®Google Scholar
• Nothwehr, S. F., E. Conibear, and T. H. Stevens. 1995. Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane. J. Cell Biol. 129:35–46.
   PubMedGoogle Scholar
• Peplowska, K., D. F. Markgraf, C. W. Ostrowicz, G. Bange, and C. Ungermann. 2007. The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev. Cell 12:739–750.
   PubMed Web of Science ®Google Scholar
• Pries, R., K. Bomeke, S. Irniger, O. Grundmann, and G. H. Braus. 2002. Amino acid-dependent Gcn4p stability regulation occurs exclusively in the yeast nucleus. Eukaryot. Cell 1:663–672.
   PubMedGoogle Scholar
• Puria, R., S. A. Zurita-Martinez, and M. E. Cardenas. 2008. Nuclear translocation of Gln3 in response to nutrient signals requires Golgi-to-endosome trafficking in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 105:7194–7199.
   PubMed Web of Science ®Google Scholar
• Qiu, H., C. Hu, S. Yoon, K. Natarajan, M. J. Swanson, and A. G. Hinnebusch. 2004. An array of coactivators is required for optimal recruitment of TATA binding protein and RNA polymerase II by promoter-bound Gcn4p. Mol. Cell. Biol. 24:4104–4117.
   PubMedGoogle Scholar
• Qiu, H., C. Hu, F. Zhang, G. J. Hwang, M. J. Swanson, C. Boonchird, and A. G. Hinnebusch. 2005. Interdependent recruitment of SAGA and Srb mediator by transcriptional activator Gcn4p. Mol. Cell. Biol. 25:3461–3474.
   PubMed Web of Science ®Google Scholar
• Raymond, C. K., I. Howald-Stevenson, C. A. Vater, and T. H. Stevens. 1992. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3:1389–1402.
   PubMed Web of Science ®Google Scholar
• Reid, G. A., and G. Schatz. 1982. Import of proteins into mitochondria. J. Biol. Chem. 257:13062–13067.
   PubMed Web of Science ®Google Scholar
• Ron, D., and H. P. Harding. 2000. PERK and translational control by stress in the endoplasmic reticulum, p. 547-560. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Rubio-Texeira, M., and C. A. Kaiser. 2006. Amino acids regulate retrieval of the yeast general amino acid permease from the vacuolar targeting pathway. Mol. Biol. Cell 17:3031–3050.
   PubMedGoogle Scholar
• Rue, S. M., S. Mattei, S. Saksena, and S. D. Emr. 2008. Novel ist1-did2 complex functions at a late step in multivesicular body sorting. Mol. Biol. Cell 19:475–484.
   PubMedGoogle Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Singer-Kruger, B., H. Stenmark, A. Dusterhoft, P. Philippsen, J. S. Yoo, D. Gallwitz, and M. Zerial. 1994. Role of three rab5-like GTPases, Ypt51p, Ypt52p, and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast. J. Cell Biol. 125:283–298.
   PubMed Web of Science ®Google Scholar
• Slessareva, J. E., S. M. Routt, B. Temple, V. A. Bankaitis, and H. G. Dohlman. 2006. Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein alpha subunit at the endosome. Cell 126:191–203.
   PubMedGoogle Scholar
• Swanson, M. J., H. Qiu, L. Sumibcay, A. Krueger, S.-J. Kim, K. Natarajan, S. Yoon, and A. G. Hinnebusch. 2003. A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol. Cell. Biol. 23:2800–2820.
   PubMed Web of Science ®Google Scholar
• Tu, J., L. G. Vallier, and M. Carlson. 1993. Molecular and genetic analysis of the SNF7 gene in Saccharomyces cerevisiae. Genetics 135:17–23.
   PubMedGoogle Scholar
• Valenzuela, L., C. Aranda, and A. Gonzalez. 2001. TOR modulates GCN4-dependent expression of genes turned on by nitrogen limitation. J. Bacteriol. 183:2331–2334.
   PubMedGoogle Scholar
• Wek, R. C., J. F. Cannon, T. E. Dever, and A. G. Hinnebusch. 1992. Truncated protein phosphatase GLC7 restores translational activation of GCN4 expression in yeast mutants defective for the eIF-2α kinase GCN2. Mol. Cell. Biol. 12:5700–5710.
   PubMedGoogle Scholar
• Winzeler, E. A., D. D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J. D. Boeke, H. Bussey, A. M. Chu, C. Connelly, K. Davis, F. Dietrich, S. W. Dow, M. E. Bakkoury, F. Foury, S. H. Friend, E. Gentalen, G. Giaever, J. H. J. Hegemann, T., M. Laub, H. Liao, N. Liebundguth, D. J. Lockhart, A. Lucau-Danila, M. Lussier, N. M'Rabet, P. Menard, M. Mittmann, C. Pai, C. Rebischung, J. L. Revuelta, L. Riles, C. J. Roberts, P. Ross-McDonald, B. Scherens, M. Snyder, S. Sookhai-Mahadeo, R. K. Storms, S. Veronneau, M. Voet, G. Volckaert, T. R. Ward, R. Wysocki, G. S. Yen, K. Yu, K. Zimmermann, P. Philippsen, M. Johnston, and R. W. Davis. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901–906.
   PubMed Web of Science ®Google Scholar
• Wolfner, M., D. Yep, F. Messenguy, and G. R. Fink. 1975. Integration of amino acid biosynthesis into the cell cycle of Saccharomyces cerevisiae. J. Mol. Biol. 96:273–290.
   PubMed Web of Science ®Google Scholar
• Xu, W., and A. P. Mitchell. 2001. Yeast PalA/AIP1/Alix homolog Rim20p associates with a PEST-like region and is required for its proteolytic cleavage. J. Bacteriol. 183:6917–6923.
   PubMedGoogle Scholar
• Xu, W., F. J. Smith, Jr., R. Subaran, and A. P. Mitchell. 2004. Multivesicular body-ESCRT components function in pH response regulation in Saccharomyces cerevisiae and Candida albicans. Mol. Biol. Cell 15:5528–5537.
   PubMedGoogle Scholar
• Yeghiayan, P., J. Tu, L. G. Vallier, and M. Carlson. 1995. Molecular analysis of the SNF8 gene of Saccharomyces cerevisiae. Yeast 11:219–224.
   PubMedGoogle Scholar
• Yoon, S., H. Qiu, M. J. Swanson, and A. G. Hinnebusch. 2003. Recruitment of SWI/SNF by Gcn4p does not require Snf2p or Gcn5p but depends strongly on SWI/SNF integrity, SRB mediator, and SAGA. Mol. Cell. Biol. 23:8829–8845.
   PubMed Web of Science ®Google Scholar
• Zhang, F., L. Sumibcay, A. G. Hinnebusch, and M. J. Swanson. 2004. A triad of subunits from the Gal11/tail domain of Srb mediator is an in vivo target of transcriptional activator Gcn4p. Mol. Cell. Biol. 24:6871–6886.
   PubMed Web of Science ®Google Scholar