Conserved motifs in the Msn2-activating domain are important for Msn2-mediated yeast stress response

Journal of Cell Science

Volumn 125, Issue 14, 2012, Pages 3333-3342

  Sadeh, Amit ^a   Baran, Dror ^a   Volokh, Misha ^a   Aharoni, Amir ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Msn2; Saccharomyces cerevisiae; Stress response; Transcriptional activation domain; Unstructured proteins

Indexed keywords

HEAT SHOCK PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MSN2; TRANSCRIPTION FACTOR MSN4; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CELL VIABILITY; CIRCULAR DICHROISM; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; MUTAGENESIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; STRESS; TRANSCRIPTION INITIATION; YEAST STRESS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; YEASTS;

SACCHAROMYCES CEREVISIAE;

EID: 84869136263     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.096446     Document Type: Article

References (37)

1. Beck, T. and Hall, M. N. (1999). The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402, 689-692.
2. Ben-Aroya, S., Coombes, C., Kwok, T., O'Donnell, K. A., Boeke, J. D. and Hieter, P. (2008). Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol. Cell 30, 248-258.
3. Boy-Marcotte, E., Perrot, M., Bussereau, F., Boucherie, H. and Jacquet, M. (1998). Msn2p and Msn4p control a large number of genes induced at the diauxic transition which are repressed by cyclic AMP in Saccharomyces cerevisiae. J. Bacteriol. 180, 1044-1052.
4. Boy-Marcotte, E., Garmendia, C., Garreau, H., Lallet, S., Mallet, L. and Jacquet, M. (2006). The transcriptional activation region of Msn2p, in Saccharomyces cerevisiae, is regulated by stress but is insensitive to the cAMP signalling pathway. Mol. Genet. Genomics 275, 277-287.
5. Causton, H. C., Ren, B., Koh, S. S., Harbison, C. T., Kanin, E., Jennings, E. G., Lee, T. I., True, H. L., Lander, E. S. and Young, R. A. (2001). Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell 12, 323- 337.
6. Dosztányi, Z., Csizmok, V., Tompa, P. and Simon, I. (2005). IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21, 3433-3434.
7. Durchschlag, E., Reiter, W., Ammerer, G. and Schüller, C. (2004). Nuclear localization destabilizes the stress-regulated transcription factor Msn2. J. Biol. Chem. 279, 55425-55432.
8. Dyson, H. J., Sayre, J. R., Merutka, G., Shin, H. C., Lerner, R. A. and Wright, P. E. (1992). Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding. II. Plastocyanin. J. Mol. Biol. 226, 819-835.
9. Garreau, H., Hasan, R. N., Renault, G., Estruch, F., Boy-Marcotte, E. and Jacquet, M. (2000). Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology 146, 2113-2120.
10. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D. and Brown, P. O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257.
11. Görner, W., Durchschlag, E., Martinez-Pastor, M. T., Estruch, F., Ammerer, G., Hamilton, B., Ruis, H. and Schüller, C. (1998). Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12, 586-597.
12. Görner, W., Durchschlag, E., Wolf, J., Brown, E. L., Ammerer, G., Ruis, H. and Schüller, C. (2002). Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J. 21, 135-144.
13. Gsponer, J., Futschik, M. E., Teichmann, S. A. and Babu, M. M. (2008). Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322, 1365-1368.
14. Hasan, R., Leroy, C., Isnard, A. D., Labarre, J., Boy-Marcotte, E. and Toledano, M. B. (2002). The control of the yeast H2O2 response by the Msn2/4 transcription factors. Mol. Microbiol. 45, 233-241.
15. Jacquet, M., Renault, G., Lallet, S., De Mey, J. and Goldbeter, A. (2003). Oscillatory nucleocytoplasmic shuttling of the general stress response transcriptional activators Msn2 and Msn4 in Saccharomyces cerevisiae. J. Cell Biol. 161, 497-505.
16. Kaida, D., Yashiroda, H., Toh-e, A. and Kikuchi, Y. (2002). Yeast Whi2 and Psr1- phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells 7, 543-552.
17. Kandror, O., Bretschneider, N., Kreydin, E., Cavalieri, D. and Goldberg, A. L. (2004). Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol. Cell 13, 771- 781.
18. Kriwacki, R. W., Hengst, L., Tennant, L., Reed, S. I. and Wright, P. E. (1996). Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc. Natl. Acad. Sci. USA 93, 11504-11509.
19. Lallet, S., Garreau, H., Garmendia-Torres, C., Szestakowska, D., Boy-Marcotte, E., Quevillon-Chéruel, S. and Jacquet, M. (2006). Role of Gal11, a component of the RNA polymerase II mediator in stress-induced hyperphosphorylation of Msn2 in Saccharomyces cerevisiae. Mol. Microbiol. 62, 438-452.
20. Laser, H., Bongards, C., Schüller, J., Heck, S., Johnsson, N. and Lehming, N. (2000). A new screen for protein interactions reveals that the Saccharomyces cerevisiae high mobility group proteins Nhp6A/B are involved in the regulation of the GAL1 promoter. Proc. Natl. Acad. Sci. USA 97, 13732-13737.
21. Lee, P., Cho, B. R., Joo, H. S. and Hahn, J. S. (2008). Yeast Yak1 kinase, a bridge between PKA and stress-responsive transcription factors, Hsf1 and Msn2/Msn4. Mol. Microbiol. 70, 882-895.
22. Lim, M. K., Tang, V., Le Saux, A., Schüller, J., Bongards, C. and Lehming, N. (2007). Gal11p dosage-compensates transcriptional activator deletions via Taf14p. J. Mol. Biol. 374, 9-23.
23. Martínez-Pastor, M. T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H. and Estruch, F. (1996). The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15, 2227-2235.
24. Medvedik, O., Lamming, D. W., Kim, K. D. and Sinclair, D. A. (2007). MSN2 and MSN4 link calorie restriction and TOR to sirtuin-mediated lifespan extension in Saccharomyces cerevisiae. PLoS Biol. 5, e261.
25. Menon, B. B., Sarma, N. J., Pasula, S., Deminoff, S. J., Willis, K. A., Barbara, K. E., Andrews, B. and Santangelo, G. M. (2005). Reverse recruitment: the Nup84 nuclear pore subcomplex mediates Rap1/Gcr1/Gcr2 transcriptional activation. Proc. Natl. Acad. Sci. USA 102, 5749-5754.
26. Nelson, J. W. and Kallenbach, N. R. (1986). Stabilization of the ribonuclease S-peptide alpha-helix by trifluoroethanol. Proteins 1, 211-217.
27. Oldfield, C. J., Cheng, Y., Cortese, M. S., Romero, P., Uversky, V. N. and Dunker, A. K. (2005). Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry 44, 12454-12470.
28. Orlando, J. S. and Ornelles, D. A. (1999). An arginine-faced amphipathic alpha helix is required for adenovirus type 5 e4orf6 protein function. J. Virol. 73, 4600-4610.
29. Pacheco, A., Pereira, C., Almeida, M. J. and Sousa, M. J. (2009). Small heat-shock protein Hsp12 contributes to yeast tolerance to freezing stress. Microbiology 155, 2021-2028.
30. Roccatano, D., Colombo, G., Fioroni, M. and Mark, A. E. (2002). Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study. Proc. Natl. Acad. Sci. USA 99, 12179-12184.
31. Roetzer, A., Gregori, C., Jennings, A. M., Quintin, J., Ferrandon, D., Butler, G., Kuchler, K., Ammerer, G. and Schüller, C. (2008). Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol. Microbiol. 69, 603-620.
32. Sadeh, A., Movshovich, N., Volokh, M., Gheber, L. and Aharoni, A. (2011). Fine- tuning of the Msn2/4-mediated yeast stress responses as revealed by systematic deletion of Msn2/4 partners. Mol. Biol. Cell 22, 3127-3138.
33. Schmid, M., Arib, G., Laemmli, C., Nishikawa, J., Durussel, T. and Laemmli, U. K. (2006). Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol. Cell 21, 379-391.
34. Smith, A., Ward, M. P. and Garrett, S. (1998). Yeast PKA represses Msn2p/Msn4p- dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J. 17, 3556-3564.
35. Snider, J., Kittanakom, S., Damjanovic, D., Curak, J., Wong, V. and Stagljar, I. (2010). Detecting interactions with membrane proteins using a membrane two-hybrid assay in yeast. Nat. Protoc. 5, 1281-1293.
36. Welker, S., Rudolph, B., Frenzel, E., Hagn, F., Liebisch, G., Schmitz, G., Scheuring, J., Kerth, A., Blume, A., Weinkauf, S. et al. (2010). Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol. Cell 39, 507-520.
37. Wright, P. E. and Dyson, H. J. (1999). Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293, 321-331.