Low level genome mistranslations deregulate the transcriptome and translatome and generate proteotoxic stress in yeast

BMC Biology

Volumn 10, Issue , 2012, Pages

  Paredes, João A ^a   Carreto, Laura ^a   Simões, João ^a   Bezerra, Ana R ^a   Gomes, Ana C ^a   Santamaria, Rodrigo ^b   Kapushesky, Misha ^b   Moura, Gabriela R ^a   Santos, Manuel A S ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Mistranslation; Mrna profiling; Protein misfolding; Protein synthesis; Proteotoxic stress; Stress; Trna; Unfolded protein response; Yeast

Indexed keywords

BACTERIA (MICROORGANISMS); FUNGI; MUS;

FUNGAL PROTEIN; FUNGAL RNA; TRANSCRIPTOME; TRANSFER RNA;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN SYNTHESIS; PROTEIN UNFOLDING; YEAST;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; PROTEIN BIOSYNTHESIS; PROTEIN UNFOLDING; RNA, FUNGAL; RNA, TRANSFER; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; YEASTS;

EID: 84862338006     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-10-55     Document Type: Article

References (101)

1. Farabaugh PJ, Bjork GR. How translational accuracy influences reading frame maintenance. EMBO J 1999, 18:1427-1434. 10.1093/emboj/18.6.1427, 1171232, 10075915.
2. Jakubowski H, Goldman E. Editing of errors in selection of amino acids for protein synthesis. Microbiol Rev 1992, 56:412-429. 372878, 1406490.
3. Loftfield RB, Vanderjagt D. The frequency of errors in protein biosynthesis. Biochem J 1972, 128:1353-1356. 1174024, 4643706.
4. Stansfield I, Jones KM, Herbert P, Lewendon A, Shaw WV, Tuite MF. Missense translation errors in Saccharomyces cerevisiae. J Mol Biol 1998, 282:13-24. 10.1006/jmbi.1998.1976, 9733638.
5. Elf J, Nilsson D, Tenson T, Ehrenberg M. Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 2003, 300:1718-1722. 10.1126/science.1083811, 12805541.
6. Kramer EB, Farabaugh PJ. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 2007, 13:87-96. 1705757, 17095544.
7. Valente L, Kinzy TG. Yeast as a sensor of factors affecting the accuracy of protein synthesis. Cell Mol Life Sci 2003, 60:2115-2130. 10.1007/s00018-003-2334-2, 14618259.
8. Menninger JR. Peptidyl transfer RNA dissociates during protein synthesis from ribosomes of Escherichia coli. J Biol Chem 1976, 251:3392-3398.
9. Buchan JR, Stansfield I. Halting a cellular production line: responses to ribosomal pausing during translation. Biol Cell 2007, 99:475-487. 10.1042/BC20070037, 17696878.
10. Gregersen N, Bross P, Vang S, Christensen JH. Protein misfolding and human disease. Annu Rev Genomics Hum Genet 2006, 7:103-124. 10.1146/annurev.genom.7.080505.115737, 16722804.
11. Bukau B, Weissman J, Horwich A. Molecular chaperones and protein quality control. Cell 2006, 125:443-451. 10.1016/j.cell.2006.04.014, 16678092.
12. Scheper GC, van der Knaap MS, Proud CG. Translation matters: protein synthesis defects in inherited disease. Nat Rev Genet 2007, 8:711-723. 10.1038/nrg2142, 17680008.
13. Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, Cook SA, Davisson MT, Sundberg JP, Schimmel P, Ackerman SL. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 2006, 443:50-55. 10.1038/nature05096, 16906134.
14. Jakubowski H. The pathophysiological hypothesis of homocysteine thiolactone-mediated vascular disease. J Physiol Pharmacol 2008, 59(Suppl 9):155-167.
15. Klipcan L, Moor N, Kessler N, Safro MG. Eukaryotic cytosolic and mitochondrial phenylalanyl-tRNA synthetases catalyze the charging of tRNA with the meta-tyrosine. Proc Natl Acad Sci USA 2009, 106:11045-11048. 10.1073/pnas.0905212106, 2700156, 19549855.
16. Shoffner JM, Lott MT, Lezza AM, Seibel P, Ballinger SW, Wallace DC. Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA(Lys) mutation. Cell 1990, 61:931-937. 10.1016/0092-8674(90)90059-N, 2112427.
17. Borner GV, Zeviani M, Tiranti V, Carrara F, Hoffmann S, Gerbitz KD, Lochmuller H, Pongratz D, Klopstock T, Melberg A, Holme E, Pääbo S. Decreased aminoacylation of mutant tRNAs in MELAS but not in MERRF patients. Hum Mol Genet 2000, 9:467-475. 10.1093/hmg/9.4.467, 10699170.
18. Enriquez JA, Chomyn A, Attardi G. MtDNA mutation in MERRF syndrome causes defective aminoacylation of tRNA(Lys) and premature translation termination. Nat Genet 1995, 10:47-55. 10.1038/ng0595-47, 7647790.
19. Pezo V, Metzgar D, Hendrickson TL, Waas WF, Hazebrouck S, Doring V, Marliere P, Schimmel P, De Crecy-Lagard V. Artificially ambiguous genetic code confers growth yield advantage. Proc Natl Acad Sci USA 2004, 101:8593-8597. 10.1073/pnas.0402893101, 423239, 15163798.
20. Silva RM, Paredes JA, Moura GR, Manadas B, Lima-Costa T, Rocha R, Miranda I, Gomes AC, Koerkamp MJ, Perrot M, Holstege FC, Boucherie H, Santos MA. Critical roles for a genetic code alteration in the evolution of the genus Candida. EMBO J 2007, 26:4555-4565. 10.1038/sj.emboj.7601876, 2063480, 17932489.
21. Santos MA, Cheesman C, Costa V, Moradas-Ferreira P, Tuite MF. Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. Mol Microbiol 1999, 31:937-947. 10.1046/j.1365-2958.1999.01233.x, 10048036.
22. Bacher JM, Waas WF, Metzgar D, de Crecy-Lagard V, Schimmel P. Genetic code ambiguity confers a selective advantage on Acinetobacter baylyi. J Bacteriol 2007, 189:6494-6496. 10.1128/JB.00622-07, 1951902, 17616603.
23. True HL, Berlin I, Lindquist SL. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 2004, 431:184-187. 10.1038/nature02885, 15311209.
24. True HL, Lindquist SL. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 2000, 407:477-483. 10.1038/35035005, 11028992.
25. Namy O, Galopier A, Martini C, Matsufuji S, Fabret C, Rousset JP. Epigenetic control of polyamines by the prion [PSI(+)]. Nat Cell Biol 2008, 10:1069-1075. 10.1038/ncb1766, 19160487.
26. Gomes AC, Miranda I, Silva RM, Moura GR, Thomas B, Akoulitchev A, Santos MA. A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. Genome Biol 2007, 8:R206. 10.1186/gb-2007-8-10-r206, 2246281, 17916231.
27. Miranda I, Rocha R, Santos MC, Mateus DD, Moura GR, Carreto L, Santos MA. A genetic code alteration is a phenotype diversity generator in the human pathogen Candida albicans. PLoS One 2007, 2:e996. 10.1371/journal.pone.0000996, 1991585, 17912373.
28. Li L, Boniecki MT, Jaffe JD, Imai BS, Yau PM, Luthey-Schulten ZA, Martinis SA. Naturally occurring aminoacyl-tRNA synthetases editing-domain mutations that cause mistranslation in Mycoplasma parasites. Proc Natl Acad Sci USA 2011, 108:9378-9383. 10.1073/pnas.1016460108, 3111296, 21606343.
29. Al Mamun AA, Marians KJ, Humayun MZ. DNA polymerase III from Escherichia coli cells expressing mutA mistranslator tRNA is error-prone. J Biol Chem 2002, 277:46319-46327. 10.1074/jbc.M206856200, 12324458.
30. Balashov S, Humayun MZ. Mistranslation induced by streptomycin provokes a RecABC/RuvABC-dependent mutator phenotype in Escherichia coli cells. J Mol Biol 2002, 315:513-527. 10.1006/jmbi.2001.5273, 11812126.
31. Grant CM, Firoozan M, Tuite MF. Mistranslation induces the heat-shock response in the yeast Saccharomyces cerevisiae. Mol Microbiol 1989, 3:215-220. 10.1111/j.1365-2958.1989.tb01810.x, 2548059.
32. Al Mamun AA, Gautam S, Humayun MZ. Hypermutagenesis in mutA cells is mediated by mistranslational corruption of polymerase, and is accompanied by replication fork collapse. Mol Microbiol 2006, 62:1752-1763. 10.1111/j.1365-2958.2006.05490.x, 17427291.
33. Grant CM, Tuite MF. Mistranslation of human phosphoglycerate kinase in yeast in the presence of paromomycin. Curr Genet 1994, 26:95-99. 10.1007/BF00313794, 8001177.
34. Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 2008, 135:679-690. 10.1016/j.cell.2008.09.038, 2684502, 19013277.
35. Nagel R, Chan A. Mistranslation and genetic variability: the effect of streptomycin. Mutat Res 2006, 601:162-170. 10.1016/j.mrfmmm.2006.06.012, 16904706.
36. Santos MA, Perreau VM, Tuite MF. Transfer RNA structural change is a key element in the reassignment of the CUG codon in Candida albicans. EMBO J 1996, 15:5060-5068. 452245, 8890179.
37. Santos MA, Tuite MF. The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. Nucleic Acids Res 1995, 23:1481-1486. 10.1093/nar/23.9.1481, 306886, 7784200.
38. Suzuki T, Ueda T, Watanabe K. The 'polysemous' codon--a codon with multiple amino acid assignment caused by dual specificity of tRNA identity. EMBO J 1997, 16:1122-1134. 10.1093/emboj/16.5.1122, 1169711, 9118950.
39. Dingermann T, Frank-Stoll U, Werner H, Wissmann A, Hillen W, Jacquet M, Marschalek R. RNA polymerase III catalysed transcription can be regulated in Saccharomyces cerevisiae by the bacterial tetracycline repressor-operator system. EMBO J 1992, 11:1487-1492. 556597, 1563352.
40. Branscomb EW, Galas DJ. Progressive decrease in protein synthesis accuracy induced by streptomycin in Escherichia coli. Nature 1975, 254:161-163. 10.1038/254161a0, 1090848.
41. Finkelstein DB, Strausberg S. Heat shock-regulated production of Escherichia coli beta-galactosidase in Saccharomyces cerevisiae. Mol Cell Biol 1983, 3:1625-1633. 370016, 6415404.
42. 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. 15070, 11102521.
43. Liberek K, Lewandowska A, Zietkiewicz S. Chaperones in control of protein disaggregation. EMBO J 2008, 27:328-335. 10.1038/sj.emboj.7601970, 2234349, 18216875.
44. Tadi D, Hasan RN, Bussereau F, Boy-Marcotte E, Jacquet M. Selection of genes repressed by cAMP that are induced by nutritional limitation in Saccharomyces cerevisiae. Yeast 1999, 15:1733-1745. 10.1002/(SICI)1097-0061(199912)15:16<1733::AID-YEA490>3.0.CO;2-L, 10590462.
45. Malys N, Carroll K, Miyan J, Tollervey D, McCarthy JE. The 'scavenger' m7GpppX pyrophosphatase activity of Dcs1 modulates nutrient-induced responses in yeast. Nucleic Acids Res 2004, 32:3590-3600. 10.1093/nar/gkh687, 484174, 15240832.
46. Halbeisen RE, Gerber AP. Stress-dependent coordination of transcriptome and translatome in yeast. PLoS Biol 2009, 7:e105. 10.1371/journal.pbio.1000105, 2675909, 19419242.
47. Helgstrand M, Mandava CS, Mulder FA, Liljas A, Sanyal S, Akke M. The ribosomal stalk binds to translation factors IF2, EF-Tu, EF-G and RF3 via a conserved region of the L12 C-terminal domain. J Mol Biol 2007, 365:468-479. 10.1016/j.jmb.2006.10.025, 17070545.
48. Krokowski D, Boguszewska A, Abramczyk D, Liljas A, Tchorzewski M, Grankowski N. Yeast ribosomal P0 protein has two separate binding sites for P1/P2 proteins. Mol Microbiol 2006, 60:386-400. 10.1111/j.1365-2958.2006.05117.x, 16573688.
49. Stevens SW, Abelson J. Purification of the yeast U4/U6.U5 small nuclear ribonucleoprotein particle and identification of its proteins. Proc Natl Acad Sci USA 1999, 96:7226-7231. 10.1073/pnas.96.13.7226, 22060, 10377396.
50. Dobbyn HC, O'Keefe RT. Analysis of Snu13p mutations reveals differential interactions with the U4 snRNA and U3 snoRNA. RNA 2004, 10:308-320. 10.1261/rna.5970404, 1370542, 14730029.
51. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 2003, 100:13207-13212. 10.1073/pnas.2135385100, 263752, 14576278.
52. Reinders J, Zahedi RP, Pfanner N, Meisinger C, Sickmann A. Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J Proteome Res 2006, 5:1543-1554. 10.1021/pr050477f, 16823961.
53. Preiss T, Baron-Benhamou J, Ansorge W, Hentze MW. Homodirectional changes in transcriptome composition and mRNA translation induced by rapamycin and heat shock. Nat Struct Biol 2003, 10:1039-1047. 10.1038/nsb1015, 14608375.
54. Smirnova JB, Selley JN, Sanchez-Cabo F, Carroll K, Eddy AA, McCarthy JE, Hubbard SJ, Pavitt GD, Grant CM, Ashe MP. Global gene expression profiling reveals widespread yet distinctive translational responses to different eukaryotic translation initiation factor 2B-targeting stress pathways. Mol Cell Biol 2005, 25:9340-9349. 10.1128/MCB.25.21.9340-9349.2005, 1265828, 16227585.
55. Melamed D, Pnueli L, Arava Y. Yeast translational response to high salinity: global analysis reveals regulation at multiple levels. RNA 2008, 14:1337-1351. 10.1261/rna.864908, 2441982, 18495938.
56. Patil C, Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 2001, 13:349-355. 10.1016/S0955-0674(00)00219-2, 11343907.
57. Spear E, Ng DT. The unfolded protein response: no longer just a special teams player. Traffic 2001, 2:515-523. 10.1034/j.1600-0854.2001.20801.x, 11489209.
58. Rose MD, Misra LM, Vogel JP. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 1989, 57:1211-1221. 10.1016/0092-8674(89)90058-5, 2661018.
59. Okamura K, Kimata Y, Higashio H, Tsuru A, Kohno K. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem Biophys Res Commun 2000, 279:445-450. 10.1006/bbrc.2000.3987, 11118306.
60. Kimata Y, Kimata YI, Shimizu Y, Abe H, Farcasanu IC, Takeuchi M, Rose MD, Kohno K. Genetic evidence for a role of BiP/Kar2 that regulates Ire1 in response to accumulation of unfolded proteins. Mol Biol Cell 2003, 14:2559-2569. 10.1091/mbc.E02-11-0708, 194903, 12808051.
61. Kohno K, Normington K, Sambrook J, Gething MJ, Mori K. The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol Cell Biol 1993, 13:877-890. 358971, 8423809.
62. Mori K, Ogawa N, Kawahara T, Yanagi H, Yura T. Palindrome with spacer of one nucleotide is characteristic of the cis-acting unfolded protein response element in Saccharomyces cerevisiae. J Biol Chem 1998, 273:9912-9920. 10.1074/jbc.273.16.9912, 9545334.
63. Mori K, Sant A, Kohno K, Normington K, Gething MJ, Sambrook JF. A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J 1992, 11:2583-2593. 556733, 1628622.
64. Cox JS, Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 1996, 87:391-404. 10.1016/S0092-8674(00)81360-4, 8898193.
65. Sidrauski C, Walter P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 1997, 90:1031-1039. 10.1016/S0092-8674(00)80369-4, 9323131.
66. Chapman RE, Walter P. Translational attenuation mediated by an mRNA intron. Curr Biol 1997, 7:850-859. 10.1016/S0960-9822(06)00373-3, 9382810.
67. Kawahara T, Yanagi H, Yura T, Mori K. Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol Biol Cell 1997, 8:1845-1862. 25627, 9348528.
68. Ruegsegger U, Leber JH, Walter P. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 2001, 107:103-114. 10.1016/S0092-8674(01)00505-0, 11595189.
69. Gorner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, Hamilton B, Ruis H, Schuller C. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev 1998, 12:586-597. 10.1101/gad.12.4.586, 316529, 9472026.
70. Beck T, Hall MN. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 1999, 402:689-692. 10.1038/45287, 10604478.
71. Thevelein JM. Fermentable sugars and intracellular acidification as specific activators of the RAS-adenylate cyclase signalling pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol 1991, 5:1301-1307. 10.1111/j.1365-2958.1991.tb00776.x, 1664904.
72. Geymonat M, Wang L, Garreau H, Jacquet M. Ssa1p chaperone interacts with the guanine nucleotide exchange factor of ras Cdc25p and controls the cAMP pathway in Saccharomyces cerevisiae. Mol Microbiol 1998, 30:855-864. 10.1046/j.1365-2958.1998.01118.x, 10094633.
73. Estruch F. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 2000, 24:469-486. 10.1111/j.1574-6976.2000.tb00551.x, 10978547.
74. Sorger PK. Heat shock factor and the heat shock response. Cell 1991, 65:363-366. 10.1016/0092-8674(91)90452-5, 2018972.
75. Craig EA, Weissman JS, Horwich AL. Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 1994, 78:365-372. 10.1016/0092-8674(94)90416-2, 7914834.
76. Mannhaupt G, Schnall R, Karpov V, Vetter I, Feldmann H. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett 1999, 450:27-34. 10.1016/S0014-5793(99)00467-6, 10350051.
77. Xie Y, Varshavsky A. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc Natl Acad Sci USA 2001, 98:3056-3061. 10.1073/pnas.071022298, 30606, 11248031.
78. Shahi P, Gulshan K, Moye-Rowley WS. Negative transcriptional regulation of multidrug resistance gene expression by an Hsp70 protein. J Biol Chem 2007, 282:26822-26831. 10.1074/jbc.M704772200, 17636264.
79. Hallstrom TC, Moye-Rowley WS. Hyperactive forms of the Pdr1p transcription factor fail to respond to positive regulation by the hsp70 protein Pdr13p. Mol Microbiol 2000, 36:402-413. 10.1046/j.1365-2958.2000.01858.x, 10792726.
80. Liu Z, Butow RA. Mitochondrial retrograde signaling. Annu Rev Genet 2006, 40:159-185. 10.1146/annurev.genet.40.110405.090613, 16771627.
81. Albanese V, Reissmann S, Frydman J. A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J Cell Biol 2010, 189:69-81. 10.1083/jcb.201001054, 2854368, 20368619.
82. Koplin A, Preissler S, Ilina Y, Koch M, Scior A, Erhardt M, Deuerling E. A dual function for chaperones SSB-RAC and the NAC nascent polypeptide-associated complex on ribosomes. J Cell Biol 2010, 189:57-68. 10.1083/jcb.200910074, 2854369, 20368618.
83. Albanese V, Yam AY, Baughman J, Parnot C, Frydman J. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 2006, 124:75-88. 10.1016/j.cell.2005.11.039, 16413483.
84. Temple MD, Perrone GG, Dawes IW. Complex cellular responses to reactive oxygen species. Trends Cell Biol 2005, 15:319-326. 10.1016/j.tcb.2005.04.003, 15953550.
85. Rutherford SL. Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 2003, 4:263-274. 10.1038/nrg1041, 12671657.
86. Cowen LE, Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005, 309:2185-2189. 10.1126/science.1118370, 16195452.
87. Queitsch C, Sangster TA, Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002, 417:618-624. 10.1038/nature749, 12050657.
88. Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998, 396:336-342. 10.1038/24550, 9845070.
89. Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S. Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS One 2007, 2:e648. 10.1371/journal.pone.0000648, 1920555, 17653275.
90. Gietz RD, Woods RA. Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol Biol 2006, 313:107-120.
91. Taxis C, Knop M. System of centromeric, episomal, and integrative vectors based on drug resistance markers for Saccharomyces cerevisiae. Biotechniques 2006, 40:73-78. 10.2144/000112040, 16454043.
92. Rand JD, Grant CM. The thioredoxin system protects ribosomes against stress-induced aggregation. Mol Biol Cell 2006, 17:387-401. 1345676, 16251355.
93. van de Peppel J, Kemmeren P, van Bakel H, Radonjic M, van Leenen D, Holstege FC. Monitoring global messenger RNA changes in externally controlled microarray experiments. EMBO Rep 2003, 4:387-393. 10.1038/sj.embor.embor798, 1319154, 12671682.
94. Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2003, 100:3889-3894. 10.1073/pnas.0635171100, 153018, 12660367.
95. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
96. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. TM4 microarray software suite. Methods Enzymol 2006, 411:134-193.
97. Shamir R, Maron-Katz A, Tanay A, Linhart C, Steinfeld I, Sharan R, Shiloh Y, Elkon R. EXPANDER--an integrative program suite for microarray data analysis. BMC Bioinformatics 2005, 6:232. 10.1186/1471-2105-6-232, 1261157, 16176576.
98. Teixeira MC, Monteiro P, Jain P, Tenreiro S, Fernandes AR, Mira NP, Alenquer M, Freitas AT, Oliveira AL, Sa-Correia I. The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 2006, 34:(Database issue):D446-451.
99. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007, 23:257-258. 10.1093/bioinformatics/btl567, 17098774.
100. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 10.1093/nar/29.9.e45, 55695, 11328886.
101. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36. 10.1093/nar/30.9.e36, 113859, 11972351.