期刊论文详细信息
BMC Molecular Biology
The Saccharomyces cerevisiae Hot1p regulated gene YHR087W (HGI1) has a role in translation upon high glucose concentration stress
M del Olmo2  E Jiménez-Martí1  M Gomar-Alba2 
[1] Present address: Dept. Genètica, Fac. Biologia, Universitat de Barcelona, Barcelona, Spain;Departament de Bioquímica i Biologia Molecular, Facultat de Ciències Biològiques, Universitat de València, Dr. Moliner, 50. E-46100, Burjassot, Valencia, Spain
关键词: Polysomes;    Hog1p;    Hot1p;    Translation;    Gene expression;    Gene YHR087W;    High glucose osmotic stress;    Saccharomyces cerevisiae;   
Others  :  1091842
DOI  :  10.1186/1471-2199-13-19
 received in 2012-02-29, accepted in 2012-05-29,  发布年份 2012
PDF
【 摘 要 】

Background

While growing in natural environments yeasts can be affected by osmotic stress provoked by high glucose concentrations. The response to this adverse condition requires the HOG pathway and involves transcriptional and posttranscriptional mechanisms initiated by the phosphorylation of this protein, its translocation to the nucleus and activation of transcription factors. One of the genes induced to respond to this injury is YHR087W. It encodes for a protein structurally similar to the N-terminal region of human SBDS whose expression is also induced under other forms of stress and whose deletion determines growth defects at high glucose concentrations.

Results

In this work we show that YHR087W expression is regulated by several transcription factors depending on the particular stress condition, and Hot1p is particularly relevant for the induction at high glucose concentrations. In this situation, Hot1p, together to Sko1p, binds to YHR087W promoter in a Hog1p-dependent manner. Several evidences obtained indicate Yhr087wp’s role in translation. Firstly, and according to TAP purification experiments, it interacts with proteins involved in translation initiation. Besides, its deletion mutant shows growth defects in the presence of translation inhibitors and displays a slightly slower translation recovery after applying high glucose stress than the wild type strain. Analyses of the association of mRNAs to polysome fractions reveals a lower translation in the mutant strain of the mRNAs corresponding to genes GPD1, HSP78 and HSP104.

Conclusions

The data demonstrates that expression of Yhr087wp under high glucose concentration is controlled by Hot1p and Sko1p transcription factors, which bind to its promoter. Yhr087wp has a role in translation, maybe in the control of the synthesis of several stress response proteins, which could explain the lower levels of some of these proteins found in previous proteomic analyses and the growth defects of the deletion strain.

【 授权许可】

   
2012 Gomar-Alba et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150128174637764.pdf 1554KB PDF download
Figure 9. 25KB Image download
Figure 8. 43KB Image download
Figure 7. 65KB Image download
Figure 6. 59KB Image download
Figure 5. 26KB Image download
Figure 4. 22KB Image download
Figure 3. 27KB Image download
Figure 2. 34KB Image download
Figure 1. 23KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】
  • [1]Hohmann S, Mager WH: Yeast stress responses. Springer, Berlin, Heidelberg; 2003.
  • [2]Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO: Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11:4241-4257.
  • [3]Kobayashi N, McEntee K: Evidence for a heat shock transcription factor-independent mechanism for heat shock induction of transcription in Saccharomyces cerevisiae. PNAS 1990, 87:6550-6554.
  • [4]Martínez-Pastor MT, Marchler G, Schüller C, Marchler-Bauer A, Ruis H, Estruch F: The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J 1996, 15:2227-2235.
  • [5]Marchler G, Schüller C, Adam G, Ruis H: A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 1993, 12:1997-2003.
  • [6]Helliwell SB, Howald I, Barbe N, Hall MN: TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics 1998, 148:99-112.
  • [7]Alepuz PM, de Nadal E, Zapater M, Ammerer G, Posas F: Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II. EMBO J 2003, 22:2433-2442.
  • [8]de Nadal E, Casadome L, Posas F: Targeting the MEF2-like transcription factor Smp1 by the stress-activated Hog1 mitogen-activated protein kinase. Mol Cell Biol 2003, 23:229-237.
  • [9]Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nadal E, Ariño J: The transcriptional response of yeast to saline stress. J Biol Chem 2000, 275:17249-17255.
  • [10]Rep M, Krantz M, Thevelein J, Hohmann S: The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J Biol Chem 2000, 275:8290-8300.
  • [11]Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA: Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 2001, 12:323-337.
  • [12]Hirasawa T, Ashitani K, Yoshikawa K, Nagahisa K, Furusawa C, Katakura Y, Shimizu H, Shioya S: Comparison of the transcriptional responses to osmotic stress induced by NaCl and sorbitol additions in Saccharomyces cerevisiae using DNA microarray. J Biosc Bioeng 2006, 102:568-571.
  • [13]Kaeberlein M, Andalis AA, Fink GR, Guarente L: High osmolarity extends life span in Saccharomyces cerevisiae by a mechanism related to calorie restriction. Mol Cell Biol 2002, 22:8056-8066.
  • [14]Erasmus DJ, van der Merwe GK, van Vuuren HJJ: Genome-wide analyses, metabolic adaptation of Saccharomyces cerevisiae to high sugar stress. FEMS Yeast Res 2003, 3:375-399.
  • [15]Jiménez-Martí E, Zuzuarregui A, Gomar-Alba M, Gutiérrez D, Gil C, del Olmo M: Molecular response of Saccharomyces cerevisiae wine and laboratory strains to high sugar stress conditions. Int J Food Microbiol 2011, 145:211-220.
  • [16]Capaldi AP, Kaplan T, Liu Y, Habib N, Regev A, Friedman N, O'Shea EK: Structure and function of a transcriptional network activated by the MAPK Hog1. Nature Genet 2008, 40:1300-1306.
  • [17]Jiménez-Martí E, Zuzuarregui A, Ridaura I, Lozano N, del Olmo M: Genetic manipulation of HSP26 and YHR087W stress genes may improve fermentative behaviour in wine yeasts under vinification conditions. Int J Food Microbiol 2009, 130:122-130.
  • [18]Savchenko A, Krogan N, Cort JR, Evdokimova E, Lew JM, Yee AA, Sánchez-Pulido L, Andrade MA, Bochkarev A, Watson JD, et al.: The Shwachman-Bodian-Diamond syndrome protein family is involved in RNA metabolism. J Biol Chem 2005, 280:19213-19220.
  • [19]Bodian M, SHeldon W, Lightwood R: Congenital hypoplasia of the exocrine pancreas. Acta Paediatr 1964, 53:282-293.
  • [20]Shwachman H, Diamond LK, Oski FA, Khaw KT: The syndrome of pancreatic insufficiency and bone marrow dysfunction. J Pediatr 1964, 65:645-663.
  • [21]Ginzberg H, Shin J, Ellis L, Morrison J, Ip W, Dror Y, Freedman M, Heitlinger LA, Belt MA, Corey M, et al.: Shwachman syndrome: phenotypic manifestations of sibling sets and isolated cases in a large patient cohort are similar. J Pediatr 1999, 135:81-88.
  • [22]Boocock GRB, Marit MR, Rommens JM: Phylogeny, sequence conservation, and functional complementation of the SBDS protein family. Genomics 2006, 87:758-771.
  • [23]Shammas C, Menne TF, Hilcenko C, Michell SR, Goyenechea B, Boocock GR, Durie PR, Rommens JM, Warren AJ: Structural and mutational analysis of the SBDS protein family. Insight into the leukemia-associated Shwachman-Diamond Syndrome. J Biol Chem 2005, 280:19221-19229.
  • [24]Luz JS, Georg RC, Gomes CH, Machado-Santelli GM, Oliveira CC: Sdo1p, the yeast orthologue of Shwachman-Bodian-Diamond syndrome protein, binds RNA and interacts with nuclear rRNA processing factors. Yeast 2009, 26:287-298.
  • [25]Menne TF, Goyenechea B, Sánchez-Puig N, Wong CC, Tonkin LM, Ancliff PJ, Brost RL, Costanzo M, Boone C, Warren AJ: The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat Genet 2007, 4:486-495.
  • [26]Vitiello SP, Benedict JW, Padilla-López S, Pearce DA: Interaction between Sdo1p and Btn1p in the Saccharomyces cerevisiae model for Batten disease. Human Mol Genet 2010, 19:931-942.
  • [27]Addinall SG, Downey M, Yu M, Zubko M, Dewar J, Leake A, Hallinan J, Shaw O, James K, Wilkinson DJ, et al.: A genomewide suppressor and enhancer analysis of cdc13-1 reveals varied cellular processes influencing telomere capping in Saccharomyces cerevisiae. Genetics 2008, 180:2251-2266.
  • [28]Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, et al.: The genetic landscape of a cell. Science 2010, 327:425-431.
  • [29]McClellan AJ, Xia Y, Deutschbauer AM, Davis RW, Gerstein M, Frydman J: Diverse cellular functions of the hsp90 molecular chaperone uncovered using systems approaches. Cell 2007, 131:121-135.
  • [30]Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK: Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
  • [31]García R, Rodríguez-Peña JM, Bermejo C, Nombela C, Arroyo J: The high osmotic response and cell wall integrity pathways cooperate to regulate transcriptional responses to zymolyase-induced cell wall stress in Saccharomyces cerevisiae. J Biol Chem 2009, 284:10901-10911.
  • [32]Schüller C, Mamnun YM, Mollapour M, Krapf G, Schuster M, Bauer BE, Piper PW, Kuchler K: Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Mol Biol Cell 2004, 15:706-720.
  • [33]Alepuz PM, Jovanovic A, Reiser V, Ammerer G: Stress-induced MAP kinase Hog1 is part of transcription activation complexes. Mol Cell 2001, 7:767-777.
  • [34]Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, et al.: Global landscape of protein complexes in the yeast Saccharomyces cerevisie. Nature 2006, 440:637-643.
  • [35]Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, et al.: Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 2002, 415:180-183.
  • [36]Mašek T, Valášek L, Pospíšek M: Polysome analysis and RNA purification from sucrose gradients. Meth Mol Biol 2011, 703:293-309.
  • [37]Melamed D, Pnueli L, Arava Y: Yeast translational response to high salinity: Global analysis reveals regulation at multiple levels. RNA 2008, 14:1-15.
  • [38]Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bähler J: Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 2003, 14:214-229.
  • [39]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
  • [40]Altschul SF, Wootton JC, Gertz M, Agarwala R, Morgulis A, Schäffer AA, Yu Y-K: Protein database searches using compositionally adjusted substitution matrices. FEBS J 2005, 272:5101-5109.
  • [41]Wenzel TJ, Luttik MA, van den Berg JA, de Steensma HY: Regulation of the PDA1 gene encoding the E1 alpha subunit of the pyruvate dehydrogenase complex from Saccharomyces cerevisiae. Eur J Biochem 1993, 218:405-411.
  • [42]Rep M, Reiser V, Gartner U, Thevelein JM, Hohmann S, Ammerer G, Ruis H: Osmotic stress-induced gene expression in Saccharomyces cerevisiae requires Msn1p and the novel nuclear factor Hot1p. Mol Cell Biol 1999, 19:5474-5485.
  • [43]Garre E, Romero-Santacreu L, De Clercq N, Blasco-Angulo N, Sunnerhagen P, Alepuz P: Yeast mRNA cap-binding protein Cbc1/Sto1 is necessary for the rapid reprogramming of translation after hyperosmotic shock. Mol Biol Cell 2011, 23:133-150.
  • [44]Gietz RD, Schiestl RH, Willems AR, Woods RA: Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1995, 11:355-360.
  • [45]Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR: Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
  • [46]Carrasco P, Pérez-Ortín JE, del Olmo M: Arginase activity is a useful marker for nitrogen limitation during alcoholic fermentation. Syst Appl Microbiol 2003, 26:471-479.
  • [47]Jiménez-Martí E, del Olmo M: Addition of ammonia or amino acids to a nitrogen-depleted medium affects gene expression patterns in yeast cells during alcoholic fermentation. FEMS Yeast Res 2008, 8:245-256.
  • [48]Schmittgen T, Livak KJ: Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008, 3:1101-1108.
  • [49]Swaminathan S, Masek T, Molin C, Pospisek M, Sunnerhagen P: Rck2 is required for reprogramming of ribosomes during oxidative stress. Mol Biol Cell 2006, 17:1472-1482.
  • [50]Kuhn K, DeRisi JL, Brown PO, Sarnow P: Global and specific translational regulation in the genomic response of Saccharomyces cerevisiae to a rapid transfer from a fermentable to a nonfermentable carbon source. Mol Cell Biol 2001, 21:916-927.
  • [51]Meskauskas A, Petrov AN, Dinman JD: Identification of functionally important amino acids of ribosomal protein L3 by saturation mutagenesis. Mol Cell Biol 2005, 25:10863-10874.
  • [52]Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Séraphin B: The Tandem Affinity Purification (TAP) method: a general procedure for protein complex purification. Methods 2001, 24:218-229.
  • [53]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882.
  • [54]Castresana J: Selection of conserved blocks from multiple alignements for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552.
  • [55]Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot O, et al.: Phylogeny fr: robust analysis for the non-specialist. Nucleic Acids Res 2008, 36(suppl 2):W465-W469.
  • [56]Ben-Aroya S, Coombes C, Kwok T, O'Donnell KA, Boeke JD, Hieter P: Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol Cell 2008, 30:248-258.
  • [57]Estruch F, Carlson M: Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol 1993, 13:3872-3881.
  • [58]Hatfield L, Beelman CA, Stevens A, Parker R: Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol Cell Biol 1996, 16:5830-5838.
  • [59]Schwartz DC, Parker R: Mutations in Translation Initiation Factors Lead to Increased Rates of Deadenylation and Decapping of mRNAs in Saccharomyces cerevisiae. Mol Cell Biol 1999, 19:5247-5256.
  • [60]Thomas BJ, Rothstein R: Elevated recombination rates in transcriptionally active DNA. Cell 1989, 56:619-630.
  文献评价指标  
  下载次数:20次 浏览次数:2次