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Hypomodified tRNA in evolutionarily distant yeasts can trigger rapid tRNA decay to activate the general amino acid control response, but with different consequences


Autoři: Thareendra De Zoysa aff001;  Eric M. Phizicky aff001
Působiště autorů: Department of Biochemistry and Biophysics, Center for RNA Biology, University of Rochester School of Medicine, Rochester, NY, United States of America aff001
Vyšlo v časopise: Hypomodified tRNA in evolutionarily distant yeasts can trigger rapid tRNA decay to activate the general amino acid control response, but with different consequences. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008893
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008893

Souhrn

All tRNAs are extensively modified, and modification deficiency often results in growth defects in the budding yeast Saccharomyces cerevisiae and neurological or other disorders in humans. In S. cerevisiae, lack of any of several tRNA body modifications results in rapid tRNA decay (RTD) of certain mature tRNAs by the 5’-3’ exonucleases Rat1 and Xrn1. As tRNA quality control decay mechanisms are not extensively studied in other eukaryotes, we studied trm8Δ mutants in the evolutionarily distant fission yeast Schizosaccharomyces pombe, which lack 7-methylguanosine at G46 (m7G46) of their tRNAs. We report here that S. pombe trm8Δ mutants are temperature sensitive primarily due to decay of tRNATyr(GUA) and that spontaneous mutations in the RAT1 ortholog dhp1+ restored temperature resistance and prevented tRNA decay, demonstrating conservation of the RTD pathway. We also report for the first time evidence linking the RTD and the general amino acid control (GAAC) pathways, which we show in both S. pombe and S. cerevisiae. In S. pombe trm8Δ mutants, spontaneous GAAC mutations restored temperature resistance and tRNA levels, and the trm8Δ temperature sensitivity was precisely linked to GAAC activation due to tRNATyr(GUA) decay. Similarly, in the well-studied S. cerevisiae trm8Δ trm4Δ RTD mutant, temperature sensitivity was closely linked to GAAC activation due to tRNAVal(AAC) decay; however, in S. cerevisiae, GAAC mutations increased tRNA loss and exacerbated temperature sensitivity. A similar exacerbated growth defect occurred upon GAAC mutation in S. cerevisiae trm8Δ and other single modification mutants that triggered RTD. Thus, these results demonstrate a conserved GAAC activation coincident with RTD in S. pombe and S. cerevisiae, but an opposite impact of the GAAC response in the two organisms. We speculate that the RTD pathway and its regulation of the GAAC pathway is widely conserved in eukaryotes, extending to other mutants affecting tRNA body modifications.

Klíčová slova:

Eukaryota – Northern blot – RNA analysis – RNA isolation – Saccharomyces cerevisiae – Schizosaccharomyces pombe – Transfer RNA – Northern analysis


Zdroje

1. Phizicky EM, Hopper AK. tRNA biology charges to the front. Genes Dev. 2010;24(17):1832–60. doi: 10.1101/gad.1956510 20810645

2. Ramos J, Fu D. The emerging impact of tRNA modifications in the brain and nervous system. Biochim Biophys Acta Gene Regul Mech. 2019;1862(3):412–28. doi: 10.1016/j.bbagrm.2018.11.007 30529455

3. Boccaletto P, Machnicka MA, Purta E, Piatkowski P, Baginski B, Wirecki TK, et al. MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Res. 2018;46(D1):D303–D7. doi: 10.1093/nar/gkx1030 29106616

4. Pereira M, Francisco S, Varanda AS, Santos M, Santos MAS, Soares AR. Impact of tRNA Modifications and tRNA-Modifying Enzymes on Proteostasis and Human Disease. Int J Mol Sci. 2018;19(12).

5. Hopper AK. Transfer RNA post-transcriptional processing, turnover, and subcellular dynamics in the yeast Saccharomyces cerevisiae. Genetics. 2013;194(1):43–67. doi: 10.1534/genetics.112.147470 23633143

6. Urbonavicius J, Qian O, Durand JMB, Hagervall TG, Bjork GR. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. 2001;20(17):4863–73. doi: 10.1093/emboj/20.17.4863 11532950

7. Lecointe F, Namy O, Hatin I, Simos G, Rousset JP, Grosjean H. Lack of pseudouridine 38/39 in the anticodon arm of yeast cytoplasmic tRNA decreases in vivo recoding efficiency. J Biol Chem. 2002;277(34):30445–53. doi: 10.1074/jbc.M203456200 12058040

8. Waas WF, de Crecy-Lagard V, Schimmel P. Discovery of a gene family critical to wyosine base formation in a subset of phenylalanine-specific transfer RNAs. J Biol Chem. 2005;280(45):37616–22. doi: 10.1074/jbc.M506939200 16162496

9. El Yacoubi B, Hatin I, Deutsch C, Kahveci T, Rousset JP, Iwata-Reuyl D, et al. A role for the universal Kae1/Qri7/YgjD (COG0533) family in tRNA modification. EMBO J. 2011;30(5):882–93. doi: 10.1038/emboj.2010.363 21285948

10. Gerber AP, Keller W. An adenosine deaminase that generates inosine at the wobble position of tRNAs. Science. 1999;286(5442):1146–9. doi: 10.1126/science.286.5442.1146 10550050

11. Murphy FVt, Ramakrishnan V. Structure of a purine-purine wobble base pair in the decoding center of the ribosome. Nat Struct Mol Biol. 2004;11(12):1251–2. doi: 10.1038/nsmb866 15558050

12. Bjork GR, Huang B, Persson OP, Bystrom AS. A conserved modified wobble nucleoside (mcm5s2U) in lysyl-tRNA is required for viability in yeast. RNA. 2007;13(8):1245–55. doi: 10.1261/rna.558707 17592039

13. Weixlbaumer A, Murphy FVt, Dziergowska A, Malkiewicz A, Vendeix FA, Agris PF, et al. Mechanism for expanding the decoding capacity of transfer RNAs by modification of uridines. Nat Struct Mol Biol. 2007;14(6):498–502. doi: 10.1038/nsmb1242 17496902

14. Muramatsu T, Nishikawa K, Nemoto F, Kuchino Y, Nishimura S, Miyazawa T, et al. Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature. 1988;336(6195):179–81. doi: 10.1038/336179a0 3054566

15. Putz J, Florentz C, Benseler F, Giege R. A single methyl group prevents the mischarging of a tRNA. Nat Struct Biol. 1994;1(9):580–2. doi: 10.1038/nsb0994-580 7634096

16. Helm M, Giege R, Florentz C. A Watson-Crick base-pair-disrupting methyl group (m1A9) is sufficient for cloverleaf folding of human mitochondrial tRNALys. Biochemistry. 1999;38(40):13338–46. doi: 10.1021/bi991061g 10529209

17. Kadaba S, Krueger A, Trice T, Krecic AM, Hinnebusch AG, Anderson J. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 2004;18(11):1227–40. doi: 10.1101/gad.1183804 15145828

18. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, et al. Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell. 2006;21(1):87–96. doi: 10.1016/j.molcel.2005.10.036 16387656

19. Anderson J, Phan L, Cuesta R, Carlson BA, Pak M, Asano K, et al. The essential Gcd10p-Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA. Genes Dev. 1998;12(23):3650–62. doi: 10.1101/gad.12.23.3650 9851972

20. Alexandrov A, Grayhack EJ, Phizicky EM. tRNA m7G methyltransferase Trm8p/Trm82p: evidence linking activity to a growth phenotype and implicating Trm82p in maintaining levels of active Trm8p. RNA. 2005;11(5):821–30. doi: 10.1261/rna.2030705 15811913

21. Kotelawala L, Grayhack EJ, Phizicky EM. Identification of yeast tRNA Um(44) 2'-O-methyltransferase (Trm44) and demonstration of a Trm44 role in sustaining levels of specific tRNA(Ser) species. RNA. 2008;14(1):158–69. doi: 10.1261/rna.811008 18025252

22. Dewe JM, Whipple JM, Chernyakov I, Jaramillo LN, Phizicky EM. The yeast rapid tRNA decay pathway competes with elongation factor 1A for substrate tRNAs and acts on tRNAs lacking one or more of several modifications. RNA. 2012;18(10):1886–96. doi: 10.1261/rna.033654.112 22895820

23. Gillis D, Krishnamohan A, Yaacov B, Shaag A, Jackman JE, Elpeleg O. TRMT10A dysfunction is associated with abnormalities in glucose homeostasis, short stature and microcephaly. J Med Genet. 2014;51(9):581–6. doi: 10.1136/jmedgenet-2014-102282 25053765

24. Cosentino C, Toivonen S, Diaz Villamil E, Atta M, Ravanat JL, Demine S, et al. Pancreatic beta-cell tRNA hypomethylation and fragmentation link TRMT10A deficiency with diabetes. Nucleic Acids Res. 2018;46(19):10302–18. doi: 10.1093/nar/gky839 30247717

25. Najmabadi H, Hu H, Garshasbi M, Zemojtel T, Abedini SS, Chen W, et al. Deep sequencing reveals 50 novel genes for recessive cognitive disorders. Nature. 2011;478(7367):57–63. doi: 10.1038/nature10423 21937992

26. Davarniya B, Hu H, Kahrizi K, Musante L, Fattahi Z, Hosseini M, et al. The Role of a Novel TRMT1 Gene Mutation and Rare GRM1 Gene Defect in Intellectual Disability in Two Azeri Families. PloS One. 2015;10(8):e0129631. doi: 10.1371/journal.pone.0129631 26308914

27. Zhang K, Lentini JM, Prevost CT, Hashem MO, Alkuraya FS, Fu D. An intellectual disability-associated missense variant in TRMT1 impairs tRNA modification and reconstitution of enzymatic activity. Human Mutation. 2020;41(3):600–7. doi: 10.1002/humu.23976 31898845

28. Dewe JM, Fuller BL, Lentini JM, Kellner SM, Fu D. TRMT1-Catalyzed tRNA Modifications Are Required for Redox Homeostasis To Ensure Proper Cellular Proliferation and Oxidative Stress Survival. Mol Cell Biol. 2017;37(21).

29. Shaheen R, Abdel-Salam GM, Guy MP, Alomar R, Abdel-Hamid MS, Afifi HH, et al. Mutation in WDR4 impairs tRNA m(7)G46 methylation and causes a distinct form of microcephalic primordial dwarfism. Genome Biology. 2015;16(1):210.

30. Chen X, Gao Y, Yang L, Wu B, Dong X, Liu B, et al. Speech and language delay in a patient with WDR4 mutations. Eur J Med Genet. 2018;61(8):468–72. doi: 10.1016/j.ejmg.2018.03.007 29597095

31. Trimouille A, Lasseaux E, Barat P, Deiller C, Drunat S, Rooryck C, et al. Further delineation of the phenotype caused by biallelic variants in the WDR4 gene. Clinical Genetics. 2018;93(2):374–7. doi: 10.1111/cge.13074 28617965

32. Martinez FJ, Lee JH, Lee JE, Blanco S, Nickerson E, Gabriel S, et al. Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome. J Med Genet. 2012;49(6):380–5. doi: 10.1136/jmedgenet-2011-100686 22577224

33. Tuorto F, Liebers R, Musch T, Schaefer M, Hofmann S, Kellner S, et al. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol. 2012;19(9):900–5. doi: 10.1038/nsmb.2357 22885326

34. Abbasi-Moheb L, Mertel S, Gonsior M, Nouri-Vahid L, Kahrizi K, Cirak S, et al. Mutations in NSUN2 cause autosomal-recessive intellectual disability. Am J Hum Genet. 2012;90(5):847–55. doi: 10.1016/j.ajhg.2012.03.021 22541559

35. Kadaba S, Wang X, Anderson JT. Nuclear RNA surveillance in Saccharomyces cerevisiae: Trf4p-dependent polyadenylation of nascent hypomethylated tRNA and an aberrant form of 5S rRNA. RNA. 2006;12(3):508–21. doi: 10.1261/rna.2305406 16431988

36. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell. 2005;121(5):713–24. doi: 10.1016/j.cell.2005.04.029 15935758

37. Vanacova S, Wolf J, Martin G, Blank D, Dettwiler S, Friedlein A, et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 2005;3(6):e189. doi: 10.1371/journal.pbio.0030189 15828860

38. Gudipati RK, Xu Z, Lebreton A, Seraphin B, Steinmetz LM, Jacquier A, et al. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell. 2012;48(3):409–21. doi: 10.1016/j.molcel.2012.08.018 23000176

39. Chernyakov I, Whipple JM, Kotelawala L, Grayhack EJ, Phizicky EM. Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5'-3' exonucleases Rat1 and Xrn1. Genes Dev. 2008;22(10):1369–80. doi: 10.1101/gad.1654308 18443146

40. Whipple JM, Lane EA, Chernyakov I, D'Silva S, Phizicky EM. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev. 2011;25(11):1173–84. doi: 10.1101/gad.2050711 21632824

41. Guy MP, Young DL, Payea MJ, Zhang X, Kon Y, Dean KM, et al. Identification of the determinants of tRNA function and susceptibility to rapid tRNA decay by high-throughput in vivo analysis. Genes Dev. 2014;28(15):1721–32. doi: 10.1101/gad.245936.114 25085423

42. Payea MJ, Sloma MF, Kon Y, Young DL, Guy MP, Zhang X, et al. Widespread temperature sensitivity and tRNA decay due to mutations in a yeast tRNA. RNA. 2018;24(3):410–22. doi: 10.1261/rna.064642.117 29259051

43. Murguia JR, Belles JM, Serrano R. The yeast HAL2 nucleotidase is an in vivo target of salt toxicity. J Biol Chem. 1996;271(46):29029–33. doi: 10.1074/jbc.271.46.29029 8910555

44. Dichtl B, Stevens A, Tollervey D. Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J. 1997;16(23):7184–95. doi: 10.1093/emboj/16.23.7184 9384595

45. Yun JS, Yoon JH, Choi YJ, Son YJ, Kim S, Tong L, et al. Molecular mechanism for the inhibition of DXO by adenosine 3',5'-bisphosphate. Biochem Biophys Res Comm. 2018;504(1):89–95. doi: 10.1016/j.bbrc.2018.08.135 30180947

46. Lin S, Liu Q, Lelyveld VS, Choe J, Szostak JW, Gregory RI. Mettl1/Wdr4-Mediated m(7)G tRNA Methylome Is Required for Normal mRNA Translation and Embryonic Stem Cell Self-Renewal and Differentiation. Mol Cell. 2018;71(2):244–55 e5.

47. Okamoto M, Fujiwara M, Hori M, Okada K, Yazama F, Konishi H, et al. tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa Cells. PLoS Genetics. 2014;10(9):e1004639. doi: 10.1371/journal.pgen.1004639 25233213

48. Frendewey DA, Kladianos DM, Moore VG, Kaiser II. Loss of tRNA 5-methyluridine methyltransferase and pseudouridine synthetase activities in 5-fluorouracil and 1-(tetrahydro-2-furanyl)-5-fluorouracil (ftorafur)-treated Escherichia coli. Biochim Biophys Acta. 1982;697(1):31–40. doi: 10.1016/0167-4781(82)90042-2 6805514

49. Santi DV, Hardy LW. Catalytic mechanism and inhibition of tRNA (uracil-5-)methyltransferase: evidence for covalent catalysis. Biochemistry. 1987;26(26):8599–606. doi: 10.1021/bi00400a016 3327525

50. Huang L, Pookanjanatavip M, Gu X, Santi DV. A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry. 1998;37(1):344–51. doi: 10.1021/bi971874+ 9425056

51. Watanabe K, Miyagawa R, Tomikawa C, Mizuno R, Takahashi A, Hori H, et al. Degradation of initiator tRNAMet by Xrn1/2 via its accumulation in the nucleus of heat-treated HeLa cells. Nucleic Acids Res. 2013;41(8):4671–85. doi: 10.1093/nar/gkt153 23471000

52. Parfrey LW, Lahr DJ, Knoll AH, Katz LA. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A. 2011;108(33):13624–9. doi: 10.1073/pnas.1110633108 21810989

53. Alexandrov A, Martzen MR, Phizicky EM. Two proteins that form a complex are required for 7-methylguanosine modification of yeast tRNA. RNA. 2002;8(10):1253–66. doi: 10.1017/s1355838202024019 12403464

54. Leulliot N, Chaillet M, Durand D, Ulryck N, Blondeau K, van Tilbeurgh H. Structure of the yeast tRNA m7G methylation complex. Structure. 2008;16(1):52–61. doi: 10.1016/j.str.2007.10.025 18184583

55. Pandolfini L, Barbieri I, Bannister AJ, Hendrick A, Andrews B, Webster N, et al. METTL1 Promotes let-7 MicroRNA Processing via m7G Methylation. Mol Cell. 2019;74(6):1278–90 e9.

56. Zhang LS, Liu C, Ma H, Dai Q, Sun HL, Luo G, et al. Transcriptome-wide Mapping of Internal N(7)-Methylguanosine Methylome in Mammalian mRNA. Mol Cell. 2019;74(6):1304–16 e8.

57. McCutchan T, Silverman S, Kohli J, Soll D. Nucleotide sequence of phenylalanine transfer RNA from Schizosaccharomyces pombe: implications for transfer RNA recognition by yeast phenylalanyl-tRNA synthetase. Biochemistry. 1978;17(9):1622–8. doi: 10.1021/bi00602a007 247991

58. Vogeli G. The nucleotide sequence of tRNA tyrosine from the fission yeast Schizosaccharomyces pombe. Nucleic Acids Res. 1979;7(4):1059–65. doi: 10.1093/nar/7.4.1059 116193

59. Chan PP, Lowe TM. GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes. Nucleic Acids Res. 2016;44(D1):D184–9. doi: 10.1093/nar/gkv1309 26673694

60. Matsumoto K, Toyooka T, Tomikawa C, Ochi A, Takano Y, Takayanagi N, et al. RNA recognition mechanism of eukaryote tRNA (m7G46) methyltransferase (Trm8-Trm82 complex). FEBS Lett. 2007;581(8):1599–604. doi: 10.1016/j.febslet.2007.03.023 17382321

61. Gustavsson M, Ronne H. Evidence that tRNA modifying enzymes are important in vivo targets for 5-fluorouracil in yeast. RNA. 2008;14(4):666–74. doi: 10.1261/rna.966208 18314501

62. Mojardin L, Botet J, Moreno S, Salas M. Chromosome segregation and organization are targets of 5'-Fluorouracil in eukaryotic cells. Cell Cycle. 2015;14(2):206–18. doi: 10.4161/15384101.2014.974425 25483073

63. Sugano S, Shobuike T, Takeda T, Sugino A, Ikeda H. Molecular analysis of the dhp1+ gene of Schizosaccharomyces pombe: an essential gene that has homology to the DST2 and RAT1 genes of Saccharomyces cerevisiae. Mol Gen Genet. 1994;243(1):1–8. doi: 10.1007/BF00283869 8190062

64. Shobuike T, Tatebayashi K, Tani T, Sugano S, Ikeda H. The dhp1(+) gene, encoding a putative nuclear 5'—>3' exoribonuclease, is required for proper chromosome segregation in fission yeast. Nucleic Acids Res. 2001;29(6):1326–33. doi: 10.1093/nar/29.6.1326 11238999

65. Xiang S, Cooper-Morgan A, Jiao X, Kiledjian M, Manley JL, Tong L. Structure and function of the 5'—>3' exoribonuclease Rat1 and its activating partner Rai1. Nature. 2009;458(7239):784–8. doi: 10.1038/nature07731 19194460

66. Dever TE, Feng L, Wek RC, Cigan AM, Donahue TF, Hinnebusch AG. Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell. 1992;68(3):585–96. doi: 10.1016/0092-8674(92)90193-g 1739968

67. Sattlegger E, Hinnebusch AG. Separate domains in GCN1 for binding protein kinase GCN2 and ribosomes are required for GCN2 activation in amino acid-starved cells. EMBO J. 2000;19(23):6622–33. doi: 10.1093/emboj/19.23.6622 11101534

68. Pavitt GD, Yang W, Hinnebusch AG. Homologous segments in three subunits of the guanine nucleotide exchange factor eIF2B mediate translational regulation by phosphorylation of eIF2. Mol Cell Biol. 1997;17(3):1298–313. doi: 10.1128/mcb.17.3.1298 9032257

69. Castilho BA, Shanmugam R, Silva RC, Ramesh R, Himme BM, Sattlegger E. Keeping the eIF2 alpha kinase Gcn2 in check. Biochim Biophys Acta. 2014;1843(9):1948–68. doi: 10.1016/j.bbamcr.2014.04.006 24732012

70. Marton MJ, Vazquez de Aldana CR, Qiu H, Chakraburtty K, Hinnebusch AG. Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2alpha kinase GCN2. Mol Cell Biol. 1997;17(8):4474–89. doi: 10.1128/mcb.17.8.4474 9234705

71. Sood R, Porter AC, Olsen DA, Cavener DR, Wek RC. A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2alpha. Genetics. 2000;154(2):787–801. 10655230

72. Zhan K, Vattem KM, Bauer BN, Dever TE, Chen JJ, Wek RC. Phosphorylation of eukaryotic initiation factor 2 by heme-regulated inhibitor kinase-related protein kinases in Schizosaccharomyces pombe is important for fesistance to environmental stresses. Mol Cell Biol. 2002;22(20):7134–46. doi: 10.1128/mcb.22.20.7134-7146.2002 12242291

73. Elsby R, Heiber JF, Reid P, Kimball SR, Pavitt GD, Barber GN. The alpha subunit of eukaryotic initiation factor 2B (eIF2B) is required for eIF2-mediated translational suppression of vesicular stomatitis virus. J Virol. 2011;85(19):9716–25. doi: 10.1128/JVI.05146-11 21795329

74. Anda S, Zach R, Grallert B. Activation of Gcn2 in response to different stresses. PloS One. 2017;12(8):e0182143. doi: 10.1371/journal.pone.0182143 28771613

75. Hinnebusch AG. Evidence for translational regulation of the activator of general amino acid control in yeast. Proc Natl Acad Sci U S A. 1984;81(20):6442–46. doi: 10.1073/pnas.81.20.6442 6387704

76. Dong J, Qiu H, Garcia-Barrio M, Anderson J, Hinnebusch AG. Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol Cell. 2000;6(2):269–79. doi: 10.1016/s1097-2765(00)00028-9 10983975

77. Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, et al. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol. 2001;21(13):4347–68. doi: 10.1128/MCB.21.13.4347-4368.2001 11390663

78. Hinnebusch AG, Natarajan K. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot Cell. 2002;1(1):22–32. doi: 10.1128/ec.01.1.22-32.2002 12455968

79. Udagawa T, Nemoto N, Wilkinson CR, Narashimhan J, Jiang L, Watt S, et al. Int6/eIF3e promotes general translation and Atf1 abundance to modulate Sty1 MAPK-dependent stress response in fission yeast. J Biol Chem. 2008;283(32):22063–75. doi: 10.1074/jbc.M710017200 18502752

80. Hinnebusch AG. Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol. 2005;59:407–50. doi: 10.1146/annurev.micro.59.031805.133833 16153175

81. Moehle CM, Hinnebusch AG. Association of RAP1 binding sites with stringent control of ribosomal protein gene transcription in Saccharomyces cerevisiae. Mol Cell Biol. 1991;11(5):2723–35. doi: 10.1128/mcb.11.5.2723 2017175

82. Duncan CDS, Rodriguez-Lopez M, Ruis P, Bahler J, Mata J. General amino acid control in fission yeast is regulated by a nonconserved transcription factor, with functions analogous to Gcn4/Atf4. Proc Natl Acad Sci U S A. 2018;115(8):E1829–E38. doi: 10.1073/pnas.1713991115 29432178

83. Han L, Guy MP, Kon Y, Phizicky EM. Lack of 2'-O-methylation in the tRNA anticodon loop of two phylogenetically distant yeast species activates the general amino acid control pathway. PLoS Genetics. 2018;14(3):e1007288. doi: 10.1371/journal.pgen.1007288 29596413

84. Dunand-Sauthier I, Walker CA, Narasimhan J, Pearce AK, Wek RC, Humphrey TC. Stress-activated protein kinase pathway functions to support protein synthesis and translational adaptation in response to environmental stress in fission yeast. Eukaryot Cell. 2005;4(11):1785–93. doi: 10.1128/EC.4.11.1785-1793.2005 16278445

85. Martin R, Berlanga JJ, de Haro C. New roles of the fission yeast eIF2alpha kinases Hri1 and Gcn2 in response to nutritional stress. J Cell Sci. 2013;126(Pt 14):3010–20. doi: 10.1242/jcs.118067 23687372

86. Ishimura R, Nagy G, Dotu I, Chuang JH, Ackerman SL. Activation of GCN2 kinase by ribosome stalling links translation elongation with translation initiation. Elife. 2016;5.

87. Hussain S, Tuorto F, Menon S, Blanco S, Cox C, Flores JV, et al. The mouse cytosine-5 RNA methyltransferase NSun2 is a component of the chromatoid body and required for testis differentiation. Mol Cell Biol. 2013;33(8):1561–70. doi: 10.1128/MCB.01523-12 23401851

88. Braun DA, Shril S, Sinha A, Schneider R, Tan W, Ashraf S, et al. Mutations in WDR4 as a new cause of Galloway-Mowat syndrome. Am J Med Genet A. 2018;176(11):2460–5. doi: 10.1002/ajmg.a.40489 30079490

89. Lamichhane TN, Arimbasseri AG, Rijal K, Iben JR, Wei FY, Tomizawa K, et al. Lack of tRNA-i6A modification causes mitochondrial-like metabolic deficiency in S. pombe by limiting activity of cytosolic tRNATyr, not mito-tRNA. RNA. 2016;22(4):583–96. doi: 10.1261/rna.054064.115 26857223

90. Johansson MJ, Esberg A, Huang B, Bjork GR, Bystrom AS. Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol Cell Biol. 2008;28(10):3301–12. doi: 10.1128/MCB.01542-07 18332122

91. Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics. 2010;11:129. doi: 10.1186/1471-2105-11-129 20230624

92. Jinek M, Coyle SM, Doudna JA. Coupled 5' nucleotide recognition and processivity in Xrn1-mediated mRNA decay. Mol Cell. 2011;41(5):600–8. doi: 10.1016/j.molcel.2011.02.004 21362555

93. Robertus JD, Ladner JE, Finch JT, Rhodes D, Brown RS, Clark BF, et al. Structure of yeast phenylalanine tRNA at 3 A resolution. Nature. 1974;250(467):546–51. doi: 10.1038/250546a0 4602655

94. Kim SH, Suddath FL, Quigley GJ, McPherson A, Sussman JL, Wang AH, et al. Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science. 1974;185(4149):435–40. doi: 10.1126/science.185.4149.435 4601792

95. Westhof E, Dumas P, Moras D. Crystallographic refinement of yeast aspartic acid transfer RNA. J Mol Biol. 1985;184(1):119–45. doi: 10.1016/0022-2836(85)90048-8 3897553

96. Johnson AW. Rat1p and Xrn1p are functionally interchangeable exoribonucleases that are restricted to and required in the nucleus and cytoplasm, respectively. Mol Cell Biol. 1997;17(10):6122–30. doi: 10.1128/mcb.17.10.6122 9315672

97. Shaheen HH, Hopper AK. Retrograde movement of tRNAs from the cytoplasm to the nucleus in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2005;102(32):11290–5. doi: 10.1073/pnas.0503836102 16040803

98. Shaheen HH, Horetsky RL, Kimball SR, Murthi A, Jefferson LS, Hopper AK. Retrograde nuclear accumulation of cytoplasmic tRNA in rat hepatoma cells in response to amino acid deprivation. Proc Natl Acad Sci U S A. 2007;104(21):8845–50. doi: 10.1073/pnas.0700765104 17502605

99. Takano A, Endo T, Yoshihisa T. tRNA Actively Shuttles Between the Nucleus and Cytosol in Yeast. Science. 2005;309:140–2. doi: 10.1126/science.1113346 15905365

100. Kramer EB, Hopper AK. Retrograde transfer RNA nuclear import provides a new level of tRNA quality control in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2013;110(52):21042–7. doi: 10.1073/pnas.1316579110 24297920

101. Chalamcharla VR, Folco HD, Dhakshnamoorthy J, Grewal SI. Conserved factor Dhp1/Rat1/Xrn2 triggers premature transcription termination and nucleates heterochromatin to promote gene silencing. Proc Natl Acad Sci U S A. 2015;112(51):15548–55. doi: 10.1073/pnas.1522127112 26631744

102. Wan Y, Hopper AK. From powerhouse to processing plant: conserved roles of mitochondrial outer membrane proteins in tRNA splicing. Genes Dev. 2018;32(19–20):1309–14. doi: 10.1101/gad.316257.118 30228203

103. Payea MJ, Hauke AC, De Zoysa T, Phizicky EM. Mutations in the anticodon stem of tRNA cause accumulation and Met22-dependent decay of pre-tRNA in yeast. RNA. 2020;26(1):29–43. doi: 10.1261/rna.073155.119 31619505

104. Zinshteyn B, Gilbert WV. Loss of a conserved tRNA anticodon modification perturbs cellular signaling. PLoS Genetics. 2013;9(8):e1003675. doi: 10.1371/journal.pgen.1003675 23935536

105. Chou HJ, Donnard E, Gustafsson HT, Garber M, Rando OJ. Transcriptome-wide Analysis of Roles for tRNA Modifications in Translational Regulation. Mol Cell. 2017;68(5):978–92 e4.

106. Pintard L, Lecointe F, Bujnicki JM, Bonnerot C, Grosjean H, Lapeyre B. Trm7p catalyses the formation of two 2'-O-methylriboses in yeast tRNA anticodon loop. EMBO J. 2002;21(7):1811–20. doi: 10.1093/emboj/21.7.1811 11927565

107. Han L, Kon Y, Phizicky EM. Functional importance of Psi38 and Psi39 in distinct tRNAs, amplified for tRNAGln(UUG) by unexpected temperature sensitivity of the s2U modification in yeast. RNA. 2015;21(2):188–201. doi: 10.1261/rna.048173.114 25505024

108. Xu F, Bystrom AS, Johansson MJO. SSD1 suppresses phenotypes induced by the lack of Elongator-dependent tRNA modifications. PLoS Genetics. 2019;15(8):e1008117. doi: 10.1371/journal.pgen.1008117 31465447

109. Wek RC. Role of eIF2alpha Kinases in Translational Control and Adaptation to Cellular Stress. Cold Spring Harb Perspect Biol. 2018;10(7).

110. Rashidi A, Miska J, Lee-Chang C, Kanojia D, Panek WK, Lopez-Rosas A, et al. GCN2 is essential for CD8(+) T cell survival and function in murine models of malignant glioma. Cancer Immunol Immunother. 2020;69(1):81–94. doi: 10.1007/s00262-019-02441-6 31844909

111. Manaud G, Nossent EJ, Lambert M, Ghigna MR, Boet A, Vinhas MC, et al. Comparison of Human and Experimental Pulmonary Veno-Occlusive Disease. Am J Respir Cell Mol Biol. 2020.

112. Turowski TW, Karkusiewicz I, Kowal J, Boguta M. Maf1-mediated repression of RNA polymerase III transcription inhibits tRNA degradation via RTD pathway. RNA. 2012;18(10):1823–32. doi: 10.1261/rna.033597.112 22919049

113. Yang R, Wek SA, Wek RC. Glucose limitation induces GCN4 translation by activation of Gcn2 protein kinase. Mol Cell Biol. 2000;20(8):2706–17. doi: 10.1128/mcb.20.8.2706-2717.2000 10733573

114. Narasimhan J, Staschke KA, Wek RC. Dimerization is required for activation of eIF2 kinase Gcn2 in response to diverse environmental stress conditions. J Biol Chem. 2004;279(22):22820–32. doi: 10.1074/jbc.M402228200 15010461

115. Zhan K, Narasimhan J, Wek RC. Differential activation of eIF2 kinases in response to cellular stresses in Schizosaccharomyces pombe. Genetics. 2004;168(4):1867–75. doi: 10.1534/genetics.104.031443 15611163

116. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, et al. Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell. 2003;14(1):214–29. doi: 10.1091/mbc.e02-08-0499 12529438

117. Cartlidge RA, Knebel A, Peggie M, Alexandrov A, Phizicky EM, Cohen P. The tRNA methylase METTL1 is phosphorylated and inactivated by PKB and RSK in vitro and in cells. EMBO J. 2005;24(9):1696–705. doi: 10.1038/sj.emboj.7600648 15861136

118. Huber SM, Leonardi A, Dedon PC, Begley TJ. The Versatile Roles of the tRNA Epitranscriptome during Cellular Responses to Toxic Exposures and Environmental Stress. Toxics. 2019;7(1).

119. Gu C, Begley TJ, Dedon PC. tRNA modifications regulate translation during cellular stress. FEBS Lett. 2014;588(23):4287–96. doi: 10.1016/j.febslet.2014.09.038 25304425

120. Torres AG, Reina O, Stephan-Otto Attolini C, Ribas de Pouplana L. Differential expression of human tRNA genes drives the abundance of tRNA-derived fragments. Proc Natl Acad Sci U S A. 2019;116(17):8451–6. doi: 10.1073/pnas.1821120116 30962382

121. Dittmar KA, Goodenbour JM, Pan T. Tissue-specific differences in human transfer RNA expression. PLoS Genetics. 2006;2(12):e221. doi: 10.1371/journal.pgen.0020221 17194224

122. Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, Pan T. tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res. 2009;37(21):7268–80. doi: 10.1093/nar/gkp787 19783824

123. Gingold H, Tehler D, Christoffersen NR, Nielsen MM, Asmar F, Kooistra SM, et al. A dual program for translation regulation in cellular proliferation and differentiation. Cell. 2014;158(6):1281–92. doi: 10.1016/j.cell.2014.08.011 25215487

124. Pavon-Eternod M, Gomes S, Rosner MR, Pan T. Overexpression of initiator methionine tRNA leads to global reprogramming of tRNA expression and increased proliferation in human epithelial cells. RNA. 2013;19(4):461–6. doi: 10.1261/rna.037507.112 23431330

125. Ishimura R, Nagy G, Dotu I, Zhou H, Yang XL, Schimmel P, et al. RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science. 2014;345(6195):455–9. doi: 10.1126/science.1249749 25061210

126. Kim DU, Hayles J, Kim D, Wood V, Park HO, Won M, et al. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nature Biotechnol. 2010;28(6):617–23.

127. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A 3rd, Steever AB, et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast. 1998;14(10):943–51. doi: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y 9717240

128. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature. 2002;418(6896):387–91. doi: 10.1038/nature00935 12140549

129. Sherman F. Getting started with yeast. Methods Enzymol. 1991;194:3–21. doi: 10.1016/0076-6879(91)94004-v 2005794

130. Elder RT, Loh EY, Davis RW. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983;80(9):2432–6. doi: 10.1073/pnas.80.9.2432 6189122

131. Preston MA, D'Silva S, Kon Y, Phizicky EM. tRNAHis 5-methylcytidine levels increase in response to several growth arrest conditions in Saccharomyces cerevisiae. RNA. 2013;19(2):243–56. doi: 10.1261/rna.035808.112 23249748

132. Jackman JE, Montange RK, Malik HS, Phizicky EM. Identification of the yeast gene encoding the tRNA m1G methyltransferase responsible for modification at position 9. RNA. 2003;9(5):574–85. doi: 10.1261/rna.5070303 12702816

133. Guy MP, Podyma BM, Preston MA, Shaheen HH, Krivos KL, Limbach PA, et al. Yeast Trm7 interacts with distinct proteins for critical modifications of the tRNAPhe anticodon loop. RNA. 2012;18(10):1921–33. doi: 10.1261/rna.035287.112 22912484

134. Lee SJ, Ramesh R, de Boor V, Gebler JM, Silva RC, Sattlegger E. Cost-effective and rapid lysis of Saccharomyces cerevisiae cells for quantitative western blot analysis of proteins, including phosphorylated eIF2alpha. Yeast. 2017;34(9):371–82. doi: 10.1002/yea.3239 28568773

135. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucl Acids Res. 1988;16:10881–90. doi: 10.1093/nar/16.22.10881 2849754


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