Lack of tRNA Modification Isopentenyl-A37 Alters mRNA Decoding and Causes Metabolic Deficiencies in Fission Yeast

REFERENCES

• Phizicky EM, Hopper AK. 2010. tRNA biology charges to the front. Genes Dev. 24:1832–1860.
   PubMed Web of Science ®Google Scholar
• Bjork GR. 1995. Biosynthesis and function of modified nucleosides, p 165–206.InSöll D, RajBhandary UL (ed),tRNA: structure, biosynthesis, and function. ASM Press, Washington, DC.
   Google Scholar
• Yokoyama S, Nishimura S. 1995. Modified nucleosides and codon recognition, p 207–223.InSöll D, RajBhandary UL (ed),tRNA: structure, biosynthesis, and function. ASM Press, Washington, DC.
   Google Scholar
• Agris PF. 2008. Bringing order to translation: the contributions of transfer RNA anticodon-domain modifications. EMBO Rep. 9:629–635.
   PubMed Web of Science ®Google Scholar
• Agris PF, Vendeix FA, Graham WD. 2007. tRNA's wobble decoding of the genome: 40 years of modification. J. Mol. Biol. 366:1–13.
   PubMed Web of Science ®Google Scholar
• Begley U, Dyavaiah M, Patil A, Rooney JP, Direnzo D, Young CM, Conklin DS, Zitomer RS, Begley TJ. 2007. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol. Cell 28:860–870.
   PubMed Web of Science ®Google Scholar
• Bauer F, Matsuyama A, Candiracci J, Dieu M, Scheliga J, Wolf DA, Yoshida M, Hermand D. 2012. Translational control of cell division by elongator. Cell Rep. 1:424–433.
   PubMed Web of Science ®Google Scholar
• Yarus M. 1982. Translational efficiency of transfer RNA's: uses of an extended anticodon. Science 218:646–652.
   PubMed Web of Science ®Google Scholar
• Miyauchi K, Kimura S, Suzuki T. 2013. A cyclic form of N6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification. Nat. Chem. Biol. 9:105–111.
   PubMedGoogle Scholar
• Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunina-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Pruim R, Xiao R, Li XY, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abecasis GR, Pugh EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M. 2007. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316:1341–1345.
   PubMed Web of Science ®Google Scholar
• Wei F, Suzuki T, Watanabe S, Kimura S, Kaitsuka T, Fujimura A, Matsui H, Atta M, Michiue H, Fontecave M, Yamagata K, Suzuki T, KT. 2011. Deficit of tRNALys modification by Cdkal1 causes the development of type 2 diabetes in mice. J. Clin. Invest. 121:3598–3608.
   PubMed Web of Science ®Google Scholar
• Reynolds NM, Lazazzera BA, Ibba M. 2010. Cellular mechanisms that control mistranslation. Nat. Rev. Microbiol. 8:849–856.
   PubMed Web of Science ®Google Scholar
• Kramer EB, Vallabhaneni H, Mayer LM, Farabaugh PJ. 2010. A comprehensive analysis of translational missense errors in the yeast Saccharomyces cerevisiae. RNA 16:1797–1808.
   PubMed Web of Science ®Google Scholar
• Roy H, Ibba M. 2006. Molecular biology: sticky end in protein synthesis. Nature 443:41–42.
   PubMedGoogle Scholar
• Kramer EB, Farabaugh PJ. 2007. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13:87–96.
   PubMed Web of Science ®Google Scholar
• Iben JR, Maraia RJ. 2012. Yeast tRNAomics: tRNA gene copy number variation and codon use provide bioinformatics evidence of a new wobble pair in a eukaryote. RNA 18:1358–1372.
   PubMedGoogle Scholar
• Kwapisz M, Smagowicz WJ, Oficjalska D, Hatin I, Rousset JP, Zoladek T, Boguta M. 2002. Up-regulation of tRNA biosynthesis affects translational readthrough in maf1-delta mutant of Saccharomyces cerevisiae. Curr. Genet. 42:147–152.
   PubMedGoogle Scholar
• Lamichhane TN, Blewett NH, Maraia RJ. 2011. Plasticity and diversity of tRNA anticodon determinants of substrate recognition by eukaryotic A37 isopentenyltransferases. RNA 17:1846–1857.
   PubMedGoogle Scholar
• Dihanich ME, Najarian D, Clark R, Gillman EC, Martin NC, Hopper AK. 1987. Isolation and characterization of MOD5, a gene required for isopentenylation of cytoplasmic and mitochondrial tRNAs of Saccharomyces cerevisiae. Mol. Cell. Biol. 7:177–184.
   PubMed Web of Science ®Google Scholar
• Lemieux J, Lakowski B, Webb A, Meng Y, Ubach A, Bussiere F, Barnes T, Hekimi S. 2001. Regulation of physiological rates in Caenorhabditis elegans by a tRNA-modifying enzyme in the mitochondria. Genetics 159:147–157.
   PubMed Web of Science ®Google Scholar
• Soderberg T, Poulter CD. 2000. Escherichia coli dimethylallyl diphosphate:tRNA dimethylallyltransferase: essential elements for recognition of tRNA substrates within the anticodon stem-loop. Biochemistry 39:6546–6553.
   PubMedGoogle Scholar
• Spinola M, Galvan A, Pignatiello C, Conti B, Pastorino U, Nicander B, Paroni R, Dragani TA. 2005. Identification and functional characterization of the candidate tumor suppressor gene TRIT1 in human lung cancer. Oncogene 24:5502–5509.
   PubMed Web of Science ®Google Scholar
• Spinola M, Colombo F, Falvella FS, Dragani TA. 2007. N6-isopentenyladenosine: a potential therapeutic agent for a variety of epithelial cancers. Int. J. Cancer 120:2744–2748.
   PubMed Web of Science ®Google Scholar
• Persson BC, Esberg B, Olafsson O, Bjork GR. 1994. Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie 76:1152–1160.
   PubMed Web of Science ®Google Scholar
• Laten H, Gorman J, Bock RM. 1978. Isopentenyladenosine deficient tRNA from an antisuppressor mutant of Saccharomyces cerevisiae. Nucleic Acids Res. 5:4329–4342.
   PubMed Web of Science ®Google Scholar
• Gefter ML, Russell RL. 1969. Role modifications in tyrosine transfer RNA: a modified base affecting ribosome binding. J. Mol. Biol. 39:145–157.
   PubMed Web of Science ®Google Scholar
• Diaz I, Pedersen S, Kurland CG. 1987. Effects of miaA on translation and growth rates. Mol. Gen. Genet. 208:373–376.
   PubMedGoogle Scholar
• Ericson JU, Bjork GR. 1986. Pleiotropic effects induced by modification deficiency next to the anticodon of tRNA from Salmonella typhimurium LT2. J. Bacteriol. 166:1013–1021.
   PubMedGoogle Scholar
• Esberg B, Bjork GR. 1995. The methylthio group (ms2) of N6-(4-hydroxyisopentenyl)-2-methylthioadenosine (ms2io6A) present next to the anticodon contributes to the decoding efficiency of the tRNA. J. Bacteriol. 177:1967–1975.
   PubMed Web of Science ®Google Scholar
• Janner F, Vogeli G, Fluri R. 1980. The antisuppressor strain sin1 of Schizosaccharomyces pombe lacks the modification isopentenyladenosine in transfer RNA. J. Mol. Biol. 139:207–219.
   PubMedGoogle Scholar
• Kohli J, Munz P, Soll D. 1989. Informational suppression, transfer RNA, and intergenic conversion, p 75–96.InNasim A, Young P, Johnson BF (ed),Molecular biology of the fission yeast. Academic Press, Inc., San Diego, CA.
   Google Scholar
• Jenner LB, Demeshkina N, Yusupova G, Yusupov M. 2010. Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat. Struct. Mol. Biol. 17:555–560.
   PubMedGoogle Scholar
• Nielsen DA, Chou J, MacKrell AJ, Casadaban MJ, Steiner DF. 1983. Expression of a preproinsulin-beta-galactosidase gene fusion in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 80:5198–5202.
   PubMed Web of Science ®Google Scholar
• Yang R, Gaidamakov SA, Xie J, Lee J, Martino L, Kozlov G, Crawford AK, Russo AN, Conte MR, Gehring K, Maraia RJ. 2011. LARP4 binds poly(A), interacts with poly(A)-binding protein MLLE domain via a variant PAM2w motif and can promote mRNA stability. Mol. Cell. Biol. 31:542–556.
   PubMed Web of Science ®Google Scholar
• Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S, AmiGO Hub, Web Presence Working Group. 2009. AmiGO: online access to ontology and annotation data. Bioinformatics 25:288–289.
   PubMed Web of Science ®Google Scholar
• Diaz I, Ehrenberg M. 1991. ms2i6A deficiency enhances proofreading in translation. J. Mol. Biol. 222:1161–1171.
   PubMedGoogle Scholar
• Ring M, Bader DE, Huber RE. 1988. Site-directed mutagenesis of beta-galactosidase (E. coli) reveals that tyr-503 is essential for activity. Biochem. Biophys. Res. Commun. 152:1050–1055.
   PubMedGoogle Scholar
• Ring M, Huber RE. 1990. Multiple replacements establish the importance of tyrosine-503 in beta-galactosidase (Escherichia coli). Arch. Biochem. Biophys. 283:342–350.
   PubMedGoogle Scholar
• Penner RM, Roth NJ, Rob B, Lay H, Huber RE. 1999. Tyr-503 of beta-galactosidase (Escherichia coli) plays an important role in degalactosylation. Biochem. Cell Biol. 77:229–236.
   PubMedGoogle Scholar
• Hagervall TG, Pomerantz SC, McCloskey JA. 1998. Reduced misreading of asparagine codons by Escherichia coli tRNALys with hypomodified derivatives of 5-methylaminomethyl-2-thiouridine in the wobble position. J. Mol. Biol. 284:33–42.
   PubMed Web of Science ®Google Scholar
• Chan PP, Lowe TM. 2009. GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res. 37:D93–D97.
   PubMed Web of Science ®Google Scholar
• Johansson M, Zhang J, Ehrenberg M. 2012. Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection. Proc. Natl. Acad. Sci. U. S. A. 109:131–136.
   PubMed Web of Science ®Google Scholar
• Weisman R, Choder M, Koltin Y. 1997. Rapamycin specifically interferes with the developmental response of fission yeast to starvation. J. Bacteriol. 179:6325–6334.
   PubMedGoogle Scholar
• Weisman R, Roitburg I, Nahari T, Kupiec M. 2005. Regulation of leucine uptake by tor1+ in Schizosaccharomyces pombe is sensitive to rapamycin. Genetics 169:539–550.
   PubMedGoogle Scholar
• Takahara T, Maeda T. 2012. TORC1 of fission yeast is rapamycin-sensitive. Genes Cells 17:698–708.
   PubMedGoogle Scholar
• Cherkasova V, Bahler J, Bacikova D, Pridham K, Maraia RJ. 2012. Altered nuclear tRNA metabolism in La-deleted Schizosaccharomyces pombe is accompanied by a nutritional stress response involving Atf1p and Pcr1p that is suppressible by Xpo-t/Los1p. Mol. Biol. Cell 23:480–491.
   PubMedGoogle Scholar
• Nurse P. 2004. Wee beasties. Nature 432:557.
   PubMedGoogle Scholar
• Nurse P, Thuriaux P. 1980. Regulatory genes controlling mitosis in the fission yeast Schizosaccharomyces pombe. Genetics 96:627–637.
   PubMed Web of Science ®Google Scholar
• Yanagida M, Ikai N, Shimanuki M, Sajiki K. 2011. Nutrient limitations alter cell division control and chromosome segregation through growth-related kinases and phosphatases. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366:3508–3520.
   PubMed Web of Science ®Google Scholar
• Kellogg DR. 2003. Wee1-dependent mechanisms required for coordination of cell growth and cell division. J. Cell Sci. 116:4883–4890.
   PubMed Web of Science ®Google Scholar
• Saracino F, Bassler J, Muzzini D, Hurt E, Agostoni Carbone ML. 2004. The yeast kinase Swe1 is required for proper entry into cell cycle after arrest due to ribosome biogenesis and protein synthesis defects. Cell Cycle 3:648–654.
   PubMedGoogle Scholar
• Vassarotti A, Boutry M, Colson AM, Goffeau A. 1984. Independent loci for the structural genes of the yeast mitochondrial alpha and beta ATPase subunits. J. Biol. Chem. 259:2845–2849.
   PubMedGoogle Scholar
• Gillman EC, Slusher LB, Martin NC, Hopper AK. 1991. MOD5 translation initiation sites determine N6-isopentenyladenosine modification of mitochondrial and cytoplasmic tRNA. Mol. Cell. Biol. 11:2382–2390.
   PubMedGoogle Scholar
• Murawski M, Szczesniak B, Zoladek T, Hopper AK, Martin NC, Boguta M. 1994. maf1 mutation alters the subcellular localization of the Mod5 protein in yeast. Acta Biochim. Pol. 41:441–448.
   PubMedGoogle Scholar
• Tolerico LH, Benko AL, Aris JP, Stanford DR, Martin NC, Hopper AK. 1999. Saccharomyces cerevisiae Mod5p-II contains sequences antagonistic for nuclear and cytosolic locations. Genetics 151:57–75.
   PubMed Web of Science ®Google Scholar
• Zoladek T, Vaduva G, Hunter LA, Boguta M, Go BD, Martin NC, Hopper AK. 1995. Mutations altering the mitochondrial-cytoplasmic distribution of Mod5p implicate the actin cytoskeleton and mRNA 3′ ends and/or protein synthesis in mitochondrial delivery. Mol. Cell. Biol. 15:6884–6894.
   PubMedGoogle Scholar
• Motorin Y, Bec G, Tewari R, Grosjean H. 1997. Transfer RNA recognition by the Escherichia coli delta2-isopentenyl-pyrophosphate:tRNA delta2-isopentenyl transferase: dependence on the anticodon arm structure. RNA 3:721–733.
   PubMed Web of Science ®Google Scholar
• Bennetzen JL, Hall BD. 1982. Codon selection in yeast. J. Biol. Chem. 257:3026–3031.
   PubMed Web of Science ®Google Scholar
• Fuchs BB, Mylonakis E. 2009. Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot. Cell 8:1616–1625.
   PubMed Web of Science ®Google Scholar
• Marguerat S, Schmidt A, Codlin S, Chen W, Aebersold R, Bahler J. 2012. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151:671–683.
   PubMed Web of Science ®Google Scholar
• Bouadloun F, Srichaiyo T, Isaksson LA, Bjork GR. 1986. Influence of modification next to the anticodon in tRNA on codon context sensitivity of translational suppression and accuracy. J. Bacteriol. 166:1022–1027.
   PubMedGoogle Scholar
• Hartwell LH, McLaughlin CS. 1969. A mutant of yeast apparently defective in the initiation of protein synthesis. Proc. Natl. Acad. Sci. U. S. A. 62:468–474.
   PubMedGoogle Scholar
• Foiani M, Cigan AM, Paddon CJ, Harashima S, Hinnebusch AG. 1991. GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:3203–3216.
   PubMed Web of Science ®Google Scholar
• Nakashima A, Sato T, Tamanoi F. 2010. Fission yeast TORC1 regulates phosphorylation of ribosomal S6 proteins in response to nutrients and its activity is inhibited by rapamycin. J. Cell Sci. 123:777–786.
   PubMed Web of Science ®Google Scholar
• Nakashima A, Otsubo Y, Yamashita A, Sato T, Yamamoto M, Tamanoi F. 2012. Psk1, an AGC kinase family member in fission yeast, is directly phosphorylated and controlled by TORC1 and functions as S6 kinase. J. Cell Sci. 125:5840–5849.
   PubMed Web of Science ®Google Scholar
• Chan CT, Pang YL, Deng W, Babu IR, Dyavaiah M, Begley TJ, Dedon PC. 2012. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat. Commun. 3:937.
   PubMed Web of Science ®Google Scholar
• Olejniczak M, Dale T, Fahlman RP, Uhlenbeck OC. 2005. Idiosyncratic tuning of tRNAs to achieve uniform ribosome binding. Nat. Struct. Mol. Biol. 12:788–793.
   PubMedGoogle Scholar
• Small I, Peeters N, Legeai F, Lurin C. 2004. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590.
   PubMed Web of Science ®Google Scholar
• Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953–971.
   PubMed Web of Science ®Google Scholar
• Claros MG. 1995. MitoProt, a Macintosh application for studying mitochondrial proteins. Comput. Appl. Biosci. 11:441–447.
   PubMedGoogle Scholar
• Huang Y, Intine RV, Mozlin A, Hasson S, Maraia RJ. 2005. Mutations in the RNA polymerase III subunit Rpc11p that decrease RNA 3′ cleavage activity increase 3′-terminal oligo(U) length and La-dependent tRNA processing. Mol. Cell. Biol. 25:621–636.
   PubMed Web of Science ®Google Scholar
• Intine RVA, Sakulich AL, Koduru SB, Huang Y, Pierstorrf E, Goodier JL, Phan L, Maraia RJ. 2000. Control of transfer RNA maturation by phosphorylation of the human La antigen on serine 366. Mol. Cell 6:339–348.
   PubMed Web of Science ®Google Scholar