Mutual cross talk between the regulators Hac1 of the unfolded protein response and Gcn4 of the general amino acid control of Saccharomyces cerevisiae

Eukaryotic Cell

Volumn 12, Issue 8, 2013, Pages 1142-1154

  Herzog, Britta ^a   Popova, Blagovesta ^b   Jakobshagen, Antonia ^a   Shahpasandzadeh, Hedieh ^b   Braus, Gerhard H ^a  

^a Center for Nanoscale Microscopy and Molecular Physiology of the Brain (CNMPB)   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; GCN4 PROTEIN, S CEREVISIAE; HAC1 PROTEIN, S CEREVISIAE; MEMBRANE PROTEIN; MUC1 PROTEIN, S CEREVISIAE; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOSYNTHESIS; CELL ADHESION; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROMOTER REGION; UNFOLDED PROTEIN RESPONSE;

AMINO ACIDS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL ADHESION; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, FUNGAL; MEMBRANE GLYCOPROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; UNFOLDED PROTEIN RESPONSE;

EID: 84880792786     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00123-13     Document Type: Article

References (77)

1. Yang R, Wek SA, Wek RC. 2000. Glucose limitation induces GCN4 translation by activation of Gcn2 protein kinase. Mol. Cell. Biol. 20:2706-2717.
2. Mösch HU. 2000. Pseudohyphal development of Saccharomyces cerevisiae. Contrib. Microbiol. 5:185-200.
3. Meussdoerffer F, Fink GR. 1983. Structure and expression of two aminoacyl-tRNA synthetase genes from Saccharomyces cerevisiae. J. Biol. Chem. 258:6293-6299.
4. Ron D. 2002. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110:1383-1388.
5. Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332:462-464.
6. Schröder M, Kaufman RJ. 2005. ER stress and the unfolded protein response. Mutat. Res. 569:29-63.
7. Patil C, Walter P. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349-355.
8. Drysdale CM, Duenas E, Jackson BM, Reusser U, Braus GH, Hinnebusch AG. 1995. The transcriptional activator GCN4 contains multiple activation domains that are critically dependent on hydrophobic amino acids. Mol. Cell. Biol. 15:1220-1233.
9. Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, Marton MJ. 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.
10. Hinnebusch AG. 1984. Evidence for translational regulation of the activator of general amino acid control in yeast. Proc. Natl. Acad. Sci. U. S. A. 81:6442-6446.
11. Hinnebusch AG. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59:407-450.
12. Mösch HU, Scheier B, Lahti R, Mantsala P, Braus GH. 1991. Transcriptional activation of yeast nucleotide biosynthetic gene ADE4 by GCN4. J. Biol. Chem. 266:20453-20456.
13. Hope IA, Struhl K. 1986. Functional dissection of a eukaryotic transcriptional activator protein, GCN4 of yeast. Cell 46:885-894.
14. Oliphant AR, Brandl CJ, Struhl K. 1989. Defining the sequence specificity of DNA-binding proteins by selecting binding sites from randomsequence oligonucleotides: analysis of yeast GCN4 protein. Mol. Cell. Biol. 9:2944-2949.
15. Hollenbeck JJ, Oakley MG. 2000. GCN4 binds with high affinity to DNA sequences containing a single consensus half-site. Biochemistry 39:6380-6389.
16. Chan IS, Fedorova AV, Shin JA. 2007. The GCN4 bZIP targets noncognate gene regulatory sequences: quantitative investigation of binding at full and half sites. Biochemistry 46:1663-1671.
17. Herzog B, Streckfuss-Bömeke K, Braus GH. 2011. A feedback circuit between transcriptional activation and self-destruction of Gcn4 separates its metabolic and morphogenic response in diploid yeasts. J. Mol. Biol. 405:909-925.
18. Braus GH, Grundmann O, Brückner S, Mösch HU. 2003. Amino acid starvation and Gcn4p regulate adhesive growth and FLO11 gene expression in Saccharomyces cerevisiae. Mol. Biol. Cell 14:4272-4284.
19. Reynolds TB, Fink GR. 2001. Bakers' yeast, a model for fungal biofilm formation. Science 291:878-881.
20. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077-1090.
21. Brückner S, Mösch HU. 2012. Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 36:25-58.
22. Lambrechts MG, Bauer FF, Marmur J, Pretorius IS. 1996. Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc. Natl. Acad. Sci. U. S. A. 93:8419-8424.
23. Mori K, Kawahara T, Yoshida H, Yanagi H, Yura T. 1996. Signalling from endoplasmic reticulum to nucleus: transcription factor with a basicleucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1:803-817.
24. Weiss MA, Ellenberger T, Wobbe CR, Lee JP, Harrison SC, Struhl K. 1990. Folding transition in the DNA-binding domain of GCN4 on specific binding to DNA. Nature 347:575-578.
25. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249-258.
26. Cox JS, Shamu CE, Walter P. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197-1206.
27. Mori K, Ma W, Gething MJ, Sambrook J. 1993. A transmembrane protein with a cdc2 /CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74:743-756.
28. van Anken E, Braakman I. 2005. Endoplasmic reticulum stress and the making of a professional secretory cell. Crit. Rev. Biochem. Mol. Biol. 40:269-283.
29. Kawaguchi S, Ng DT. 2011. Sensing ER stress. Science 333:1830-1831.
30. Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081-1086.
31. Liu CY, Wong HN, Schauerte JA, Kaufman RJ. 2002. The protein kinase/endoribonuclease IRE1α that signals the unfolded protein response has a luminal N-terminal ligand-independent dimerization domain. J. Biol. Chem. 277:18346-18356.
32. Nikawa J, Yamashita S. 1992. IRE1 encodes a putative protein kinase containing a membrane-spanning domain and is required for inositol phototrophy in Saccharomyces cerevisiae. Mol. Microbiol. 6:1441-1446.
33. Sidrauski C, Walter P. 1997. The transmembrane kinase Ire1p is a sitespecific endonuclease that initiatesmRNAsplicing in the unfolded protein response. Cell 90:1031-1039.
34. Shamu CE, Walter P. 1996. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15:3028-3039.
35. Tirasophon W, Welihinda AA, Kaufman RJ. 1998. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 12:1812-1824.
36. Kohno K. 2007. How transmembrane proteins sense endoplasmic reticulum stress. Antioxid. Redox Signal. 9:2295-2303.
37. Ruegsegger U, Leber JH, Walter P. 2001. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107:103-114.
38. Kawahara T, Yanagi H, Yura T, Mori K. 1997. Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 8:1845-1862.
39. Chapman RE, Walter P. 1997. Translational attenuation mediated by an mRNA intron. Curr. Biol. 7:850-859.
40. Cox JS, Walter P. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404.
41. Irniger S, Braus GH. 2003. Controlling transcription by destruction: the regulation of yeast Gcn4p stability. Curr. Genet. 44:8-18.
42. Kornitzer D, Raboy B, Kulka RG, Fink GR. 1994. Regulated degradation of the transcription factor Gcn4. EMBO J. 13:6021-6030.
43. Shemer R, Meimoun A, Holtzman T, Kornitzer D. 2002. Regulation of the transcription factor Gcn4 by Pho85 cyclin PCL5. Mol. Cell. Biol. 22: 5395-5404.
44. Pal B, Chan NC, Helfenbaum L, Tan K, Tansey WP, Gething MJ. 2007. SCFCdc4-mediated degradation of the Hac1p transcription factor regulates the unfolded protein response in Saccharomyces cerevisiae. Mol. Biol. Cell 18:426-440.
45. Patil CK, Li H, Walter P. 2004. Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response. PLoS Biol. 2:E246. doi:10.1371/journal.pbio.0020246.
46. Fordyce PM, Pincus D, Kimmig P, Nelson CS, El-Samad H, Walter P, DeRisi JL. 2012. Basic leucine zipper transcription factor Hac1 binds DNA in two distinct modes as revealed by microfluidic analyses. Proc. Natl. Acad. Sci. U. S. A. 109:E3084-3093.
47. Ito H, Fukuda Y, Murata K, Kimura A. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
48. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
49. Southern EM. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503-517.
50. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
51. Roberts RL, Fink GR. 1994. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev. 8:2974-2985.
52. Rose M, Botstein D. 1983. Construction and use of gene fusions to lacZ (β-galactosidase) that are expressed in yeast. Methods Enzymol. 101:167-180.
53. Rupp S, Summers E, Lo HJ, Madhani H, Fink G. 1999. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 18:1257-1269.
54. Kleinschmidt M, Grundmann O, Bluthgen N, Mösch HU, Braus GH. 2005. Transcriptional profiling of Saccharomyces cerevisiae cells under adhesion-inducing conditions. Mol. Genet. Genomics 273:382-393.
55. Klopotowski T, Wiater A. 1965. Synergism of aminotriazole and phosphate on the inhibition of yeast imidazole glycerol phosphate dehydratase. Arch. Biochem. Biophys. 112:562-566.
56. Mortimer RK. 2000. Evolution and variation of the yeast (Saccharomyces) genome. Genome Res. 10:403-409.
57. Albrecht G, Mösch HU, Hoffmann B, Reusser U, Braus GH. 1998. Monitoring the Gcn4 protein-mediated response in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 273:12696-12702.
58. Grundmann O, Mösch HU, Braus GH. 2001. Repression of GCN4 mRNA translation by nitrogen starvation in Saccharomyces cerevisiae. J. Biol. Chem. 276:25661-25671.
59. Hinnebusch AG. 1985. A hierarchy of trans-acting factors modulates translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 5:2349-2360.
60. Octavio LM, Gedeon K, Maheshri N. 2009. Epigenetic and conventional regulation is distributed among activators of FLO11 allowing tuning of population-level heterogeneity in its expression. PLoS Genet. 5:e1000673. doi:10.1371/journal.pgen.1000673.
61. Nikolaev Y, Deillon C, Hoffmann SR, Bigler L, Friess S, Zenobi R, Pervushin K, Hunziker P, Gutte B. 2010. The leucine zipper domains of the transcription factors GCN4 and c-Jun have ribonuclease activity. PLoS One 5:e10765. doi:10.1371/journal.pone.0010765.
62. Wimalasena TT, Enjalbert B, Guillemette T, Plumridge A, Budge S, Yin Z, Brown AJ, Archer DB. 2008. Impact of the unfolded protein response upon genome-wide expression patterns, and the role of Hac1 in the polarized growth, of Candida albicans. Fungal Genet. Biol. 45: 1235-1247.
63. Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller KK, Miley MD, White S, McCarthy JW, Latge JP, Feldmesser M, Rhodes JC, Askew DS. 2009. A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog. 5:e1000258. doi:10.1371/journal.ppat.1000258.
64. Krappmann S, Bignell EM, Reichard U, Rogers T, Haynes K, Braus GH. 2004. The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Mol. Microbiol. 52:785-799.
65. Tripathi G, Wiltshire C, Macaskill S, Tournu H, Budge S, Brown AJ. 2002. Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J. 21:5448-5456.
66. Gildor T, Shemer R, Atir-Lande A, Kornitzer D. 2005. Coevolution of cyclin Pcl5 and its substrate Gcn4. Eukaryot. Cell 4:310-318.
67. Saito S, Furuno A, Sakurai J, Sakamoto A, Park HR, Shin-Ya K, Tsuruo T, Tomida A. 2009. Chemical genomics identifies the unfolded protein response as a target for selective cancer cell killing during glucose deprivation. Cancer Res. 69:4225-4234.
68. Wang G, Yang ZQ, Zhang K. 2010. Endoplasmic reticulum stress response in cancer: molecular mechanism and therapeutic potential. Am. J. Transl. Res. 2:65-74.
69. Shajahan AN, Riggins RB, Clarke R. 2009. The role of X-box binding protein-1 in tumorigenicity. Drug News Perspect. 22:241-246.
70. Pan X, Heitman J. 2002. Protein kinase A operates a molecular switch that governs yeast pseudohyphal differentiation. Mol. Cell. Biol. 22:3981-3993.
71. Amoutzias GD, Robertson DL, Van de Peer Y, Oliver SG. 2008. Choose your partners: dimerization in eukaryotic transcription factors. Trends Biochem. Sci. 33:220-229.
72. Strittmatter AW, Fischer C, Kleinschmidt M, Braus GH. 2006. FLO11 mediated filamentous growth of the yeast Saccharomyces cerevisiae depends on the expression of the ribosomal RPS26 genes. Mol. Genet. Genomics 276:113-125.
73. Mueller PP, Hinnebusch AG. 1986. Multiple upstream AUG codons mediate translational control of GCN4. Cell 45:201-207.
74. Goldstein AL, McCusker JH. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541-1553.
75. Mumberg D, Müller R, Funk M. 1994. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22:5767-5768.
76. Guarente L, Ptashne M. 1981. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 78:2199-2203.
77. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.