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PMID: 21285948 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A role for the universal Kae1/Qri7/YgjD (COG0533) family in tRNA modification.

The EMBO journal ·Vol. 30 ·No. 5 ·2011-03-02 ·Pages 882-93

El Yacoubi B, Hatin I, Deutsch C, Kahveci T, Rousset JP, Iwata-Reuyl D, Murzin AG, de Crécy-Lagard V

Abstract

The YgjD/Kae1 family (COG0533) has been on the top-10 list of universally conserved proteins of unknown function for over 5 years. It has been linked to DNA maintenance in bacteria and mitochondria and transcription regulation and telomere homeostasis in eukaryotes, but its actual function has never been found. Based on a comparative genomic and structural analysis, we predicted this family was involved in the biosynthesis of N(6)-threonylcarbamoyl adenosine, a universal modification found at position 37 of tRNAs decoding ANN codons. This was confirmed as a yeast mutant lacking Kae1 is devoid of t(6)A. t(6)A(-) strains were also used to reveal that t(6)A has a critical role in initiation codon restriction to AUG and in restricting frameshifting at tandem ANN codons. We also showed that YaeZ, a YgjD paralog, is required for YgjD function in vivo in bacteria. This work lays the foundation for understanding the pleiotropic role of this universal protein family.

MeSH Terms
Adenosine/analogs & derivatives,metabolism Genetic Complementation Test Metalloendopeptidases/genetics,metabolism Mitochondrial Proteins/genetics,metabolism Multiprotein Complexes RNA, Transfer/chemistry,genetics,metabolism Saccharomyces cerevisiae/genetics,growth & development,metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism
Chemicals
Mitochondrial Proteins Multiprotein Complexes Qri7 protein, S cerevisiae Saccharomyces cerevisiae Proteins N(6)-(N-threonylcarbonyl)adenosine RNA, Transfer Kae1 protein, S cerevisiae Metalloendopeptidases Adenosine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
El Yacoubi Basma
Department of Microbiology and Cell Science, University of Florida, Gainesville, FL, USA. basma@ufl.edu.edu
Hatin Isabelle
Deutsch Christopher
Kahveci Tamer
Rousset Jean-Pierre
Iwata-Reuyl Dirk
Murzin Alexey G
de Crécy-Lagard Valérie
References (88)
88 references, click to expand
  1. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast.
    Genetics. 2000 May;155(1):475-9 PMID: 10790418
  2. Temperature sensitivity caused by mutant release factor 1 is suppressed by mutations that affect 16S rRNA maturation.
    J Bacteriol. 2004 May;186(10):3046-55 PMID: 15126466
  3. X-ray crystal structure of a hypothetical Sua5 protein from Sulfolobus tokodaii strain 7.
    Proteins. 2008 Feb 15;70(3):1108-11 PMID: 18004774
  4. Kinetic and thermodynamic analysis of the role of start codon/anticodon base pairing during eukaryotic translation initiation.
    RNA. 2009 Jan;15(1):138-52 PMID: 19029312
  5. The 1.5-A resolution crystal structure of bacterial luciferase in low salt conditions.
    J Biol Chem. 1996 Sep 6;271(36):21956-68 PMID: 8703001
  6. The Escherichia coli K-12 ORFeome: a resource for comparative molecular microbiology.
    BMC Genomics. 2010 Aug 11;11:470 PMID: 20701780
  7. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation.
    Genes Dev. 1992 May;6(5):801-14 PMID: 1577274
  8. The yeast VAS1 gene encodes both mitochondrial and cytoplasmic valyl-tRNA synthetases.
    J Biol Chem. 1988 Jan 5;263(1):52-7 PMID: 3275649
  9. The small-subunit processome is a ribosome assembly intermediate.
    Eukaryot Cell. 2004 Dec;3(6):1619-26 PMID: 15590835
  10. The naturally occurring N6-threonyl adenine in anticodon loop of Schizosaccharomyces pombe tRNAi causes formation of a unique U-turn motif.
    Nucleic Acids Res. 2006 May 31;34(10):2878-86 PMID: 16738127
  11. The universal YrdC/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA.
    Nucleic Acids Res. 2009 May;37(9):2894-909 PMID: 19287007
  12. Global analysis of protein localization in budding yeast.
    Nature. 2003 Oct 16;425(6959):686-91 PMID: 14562095
  13. Characterization of two bifunctional Arabdopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs.
    Eur J Biochem. 1999 Dec;266(3):848-54 PMID: 10583378
  14. Qri7/OSGEPL, the mitochondrial version of the universal Kae1/YgjD protein, is essential for mitochondrial genome maintenance.
    Nucleic Acids Res. 2009 Sep;37(16):5343-52 PMID: 19578062
  15. Protein structure prediction on the Web: a case study using the Phyre server.
    Nat Protoc. 2009;4(3):363-71 PMID: 19247286
  16. Sua5p a single-stranded telomeric DNA-binding protein facilitates telomere replication.
    EMBO J. 2009 May 20;28(10):1466-78 PMID: 19369944
  17. Distribution of glycoprotease activity and the glycoprotease gene among serotypes of Pasteurella haemolytica.
    Biochem Soc Trans. 1990 Oct;18(5):901-3 PMID: 2083719
  18. Comparative RNomics and modomics in Mollicutes: prediction of gene function and evolutionary implications.
    IUBMB Life. 2007 Oct;59(10):634-58 PMID: 17852564
  19. The construction of systematic in-frame, single-gene knockout mutant collection in Escherichia coli K-12.
    Methods Mol Biol. 2008;416:171-81 PMID: 18392967
  20. Functional anticodon architecture of human tRNALys3 includes disruption of intraloop hydrogen bonding by the naturally occurring amino acid modification, t6A.
    Biochemistry. 2000 Nov 7;39(44):13396-404 PMID: 11063577
  21. Atomic structure of the KEOPS complex: an ancient protein kinase-containing molecular machine.
    Mol Cell. 2008 Oct 24;32(2):259-75 PMID: 18951093
  22. Programmed translational frameshifting in a gene required for yeast telomere replication.
    Curr Biol. 1997 Dec 1;7(12):969-76 PMID: 9382847
  23. Structural characterization of Salmonella typhimurium YeaZ, an M22 O-sialoglycoprotein endopeptidase homolog.
    Proteins. 2006 Jul 1;64(1):111-23 PMID: 16617437
  24. Information content of binding sites on nucleotide sequences.
    J Mol Biol. 1986 Apr 5;188(3):415-31 PMID: 3525846
  25. Switching and signaling at the telomere.
    Cell. 2001 Sep 21;106(6):661-73 PMID: 11572773
  26. Yeast homolog of a cancer-testis antigen defines a new transcription complex.
    EMBO J. 2006 Aug 9;25(15):3576-85 PMID: 16874308
  27. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence.
    Genome Res. 1998 May;8(5):464-78 PMID: 9582191
  28. The Escherichia coli tRNA-guanine transglycosylase can recognize and modify DNA.
    J Biol Chem. 2002 Mar 1;277(9):7178-82 PMID: 11751936
  29. Structure of the beta 2 homodimer of bacterial luciferase from Vibrio harveyi: X-ray analysis of a kinetic protein folding trap.
    Protein Sci. 1997 Jan;6(1):13-23 PMID: 9007973
  30. Crystal structure and anion binding in the prokaryotic hydrogenase maturation factor HypF acylphosphatase-like domain.
    J Mol Biol. 2002 Aug 30;321(5):785-96 PMID: 12206761
  31. The enzymatic synthesis of N-(purin-6-ylcarbamoyl)threonine, an anticodon-adjacent base in transfer ribonucleic acid.
    Biochemistry. 1974 Oct 22;13(22):4622-8 PMID: 4609459
  32. Effect of threonylcarbamoyl modification (t6A) in yeast tRNA Arg III on codon-anticodon and anticodon-anticodon interactions. A thermodynamic and kinetic evaluation.
    Eur J Biochem. 1981 May;116(1):207-13 PMID: 6788546
  33. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast.
    EMBO J. 1996 Oct 15;15(20):5701-14 PMID: 8896463
  34. Mitochondria-specific RNA-modifying enzymes responsible for the biosynthesis of the wobble base in mitochondrial tRNAs. Implications for the molecular pathogenesis of human mitochondrial diseases.
    J Biol Chem. 2005 Jan 14;280(2):1613-24 PMID: 15509579
  35. Biosynthesis of N-(purin-6-ylcarbamoyl)-L-threonine riboside. Incorporation of L-threonine in vivo into modified nucleoside of transfer ribonucleic acid.
    Biochem J. 1972 Apr;127(3):515-9 PMID: 4561775
  36. Versatile vectors to study recoding: conservation of rules between yeast and mammalian cells.
    Nucleic Acids Res. 1995 May 11;23(9):1557-60 PMID: 7784210
  37. AUG is the only recognisable signal sequence in the 5' non-coding regions of eukaryotic mRNA.
    Nature. 1978 Jul 6;274(5666):84-7 PMID: 662001
  38. tRNAdb 2009: compilation of tRNA sequences and tRNA genes.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D159-62 PMID: 18957446
  39. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19392-7 PMID: 18048332
  40. ESPript: analysis of multiple sequence alignments in PostScript.
    Bioinformatics. 1999 Apr;15(4):305-8 PMID: 10320398
  41. Multiple sequence alignment with the Clustal series of programs.
    Nucleic Acids Res. 2003 Jul 1;31(13):3497-500 PMID: 12824352
  42. A genome-based approach for the identification of essential bacterial genes.
    Nat Biotechnol. 1998 Sep;16(9):851-6 PMID: 9743119
  43. Cloning, nucleotide sequence, and expression of the Pasteurella haemolytica A1 glycoprotease gene.
    J Bacteriol. 1991 Sep;173(18):5597-603 PMID: 1885539
  44. From complete genome sequence to 'complete' understanding?
    Trends Biotechnol. 2010 Aug;28(8):398-406 PMID: 20647113
  45. Convergent evolution of metabolic roles in bacterial co-symbionts of insects.
    Proc Natl Acad Sci U S A. 2009 Sep 8;106(36):15394-9 PMID: 19706397
  46. Myosin-like proteins 1 and 2 are not required for silencing or telomere anchoring, but act in the Tel1 pathway of telomere length control.
    J Struct Biol. 2002 Oct-Dec;140(1-3):79-91 PMID: 12490156
  47. The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine tRNA synthetases of S. cerevisiae.
    Cell. 1986 Jul 18;46(2):235-43 PMID: 3521891
  48. The YrdC protein--a putative ribosome maturation factor.
    Biochim Biophys Acta. 2005 Feb 14;1727(2):87-96 PMID: 15716138
  49. Y'-Help1, a DNA helicase encoded by the yeast subtelomeric Y' element, is induced in survivors defective for telomerase.
    J Biol Chem. 1998 Dec 11;273(50):33360-6 PMID: 9837911
  50. Nonsense-mediated decay mutants do not affect programmed -1 frameshifting.
    RNA. 2000 Jul;6(7):952-61 PMID: 10917592
  51. Analysis of the interaction between piD261/Bud32, an evolutionarily conserved protein kinase of Saccharomyces cerevisiae, and the Grx4 glutaredoxin.
    Biochem J. 2004 Jan 15;377(Pt 2):395-405 PMID: 14519092
  52. A dual-specificity pseudouridine synthase: an Escherichia coli synthase purified and cloned on the basis of its specificity for psi 746 in 23S RNA is also specific for psi 32 in tRNA(phe).
    RNA. 1995 Jun;1(4):437-48 PMID: 7493321
  53. An adenosine triphosphate-dependent carbamoylphosphate--3-hydroxymethylcephem O-carbamoyltransferase from Streptomyces clavuligerus.
    Biochem J. 1980 Mar 1;185(3):555-64 PMID: 6248024
  54. Proteome survey reveals modularity of the yeast cell machinery.
    Nature. 2006 Mar 30;440(7084):631-6 PMID: 16429126
  55. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis.
    Nature. 2002 Jun 27;417(6892):967-70 PMID: 12068309
  56. Dissociation of eIF1 from the 40S ribosomal subunit is a key step in start codon selection in vivo.
    Genes Dev. 2007 May 15;21(10):1217-30 PMID: 17504939
  57. Structure of an essential bacterial protein YeaZ (TM0874) from Thermotoga maritima at 2.5 Å resolution.
    Acta Crystallogr Sect F Struct Biol Cryst Commun. 2010 Oct 1;66(Pt 10):1230-6 PMID: 20944216
  58. Reciprocal association of the budding yeast ATM-related proteins Tel1 and Mec1 with telomeres in vivo.
    Mol Cell. 2004 May 21;14(4):515-22 PMID: 15149600
  59. Npa1p is an essential trans-acting factor required for an early step in the assembly of 60S ribosomal subunits in Saccharomyces cerevisiae.
    RNA. 2004 Jul;10(7):1073-83 PMID: 15208443
  60. Structural basis for sulfur relay to RNA mediated by heterohexameric TusBCD complex.
    Structure. 2006 Feb;14(2):357-66 PMID: 16472754
  61. Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast.
    Genetics. 2005 Apr;169(4):1915-25 PMID: 15716499
  62. Nucleotide sequence of N-formyl-methionyl-transfer RNA.
    Nature. 1968 Apr 20;218(5138):232-3 PMID: 4869713
  63. Cell size regulation during telomere-directed senescence in Saccharomyces cerevisiae.
    Biosci Biotechnol Biochem. 2010;74(1):195-8 PMID: 20057141
  64. Nucleotide modifications in three functionally important regions of the Saccharomyces cerevisiae ribosome affect translation accuracy.
    Nucleic Acids Res. 2009 Dec;37(22):7665-77 PMID: 19820108
  65. One bacterial cell, one complete genome.
    PLoS One. 2010 Apr 23;5(4):e10314 PMID: 20428247
  66. Structure of the archaeal Kae1/Bud32 fusion protein MJ1130: a model for the eukaryotic EKC/KEOPS subcomplex.
    EMBO J. 2008 Sep 3;27(17):2340-51 PMID: 19172740
  67. Systematic screen for human disease genes in yeast.
    Nat Genet. 2002 Aug;31(4):400-4 PMID: 12134146
  68. The Sua5 protein is essential for normal translational regulation in yeast.
    Mol Cell Biol. 2010 Jan;30(1):354-63 PMID: 19884342
  69. HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturation.
    J Biol Chem. 2002 Dec 20;277(51):49945-51 PMID: 12377778
  70. The role of modifications in codon discrimination by tRNA(Lys)UUU.
    Nat Struct Mol Biol. 2004 Dec;11(12):1186-91 PMID: 15558052
  71. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world.
    Nucleic Acids Res. 2008 Dec;36(21):6688-719 PMID: 18948295
  72. 'Conserved hypothetical' proteins: prioritization of targets for experimental study.
    Nucleic Acids Res. 2004 Oct 12;32(18):5452-63 PMID: 15479782
  73. Yeast mitochondrial initiator tRNA is methylated at guanosine 37 by the Trm5-encoded tRNA (guanine-N1-)-methyltransferase.
    J Biol Chem. 2007 Sep 21;282(38):27744-53 PMID: 17652090
  74. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  75. Conserved network of proteins essential for bacterial viability.
    J Bacteriol. 2009 Aug;191(15):4732-49 PMID: 19376873
  76. Characterization of the cmcH genes of Nocardia lactamdurans and Streptomyces clavuligerus encoding a functional 3'-hydroxymethylcephem O-carbamoyltransferase for cephamycin biosynthesis.
    Gene. 1995 Aug 30;162(1):21-7 PMID: 7557411
  77. Modified nucleoside dependent Watson-Crick and wobble codon binding by tRNALysUUU species.
    Biochemistry. 2000 Nov 7;39(44):13390-5 PMID: 11063576
  78. Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification.
    Mol Cell Biol. 2004 Jul;24(14):6324-37 PMID: 15226434
  79. Tight modulation of Escherichia coli bacterial biofilm formation through controlled expression of adhesion factors.
    Appl Environ Microbiol. 2007 May;73(10):3391-403 PMID: 17384304
  80. Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands.
    Science. 2003 Feb 14;299(5609):1067-70 PMID: 12586941
  81. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii.
    BMC Evol Biol. 2007 Oct 01;7:181 PMID: 17908294
  82. The presence of N-(purin-6-ylcarbamoyl)threonine in transfer ribonucleic acid species whose codons begin with adenine.
    J Biol Chem. 1972 Oct 25;247(20):6394-401 PMID: 4561935
  83. N-(purin-6-ylcarbamoyl)threonine: biosynthesis in vitro in transfer RNA by an enzyme purified from Escherichia coli.
    FEBS Lett. 1974 Mar 1;39(3):301-6 PMID: 4604806
  84. The 160-kilobase genome of the bacterial endosymbiont Carsonella.
    Science. 2006 Oct 13;314(5797):267 PMID: 17038615
  85. An archaeal orthologue of the universal protein Kae1 is an iron metalloprotein which exhibits atypical DNA-binding properties and apurinic-endonuclease activity in vitro.
    Nucleic Acids Res. 2007;35(18):6042-51 PMID: 17766251
  86. Characterization of NovP and NovN: completion of novobiocin biosynthesis by sequential tailoring of the noviosyl ring.
    Angew Chem Int Ed Engl. 2004 Jan;43(1):67-70 PMID: 14694473
  87. Premature stop codons involved in muscular dystrophies show a broad spectrum of readthrough efficiencies in response to gentamicin treatment.
    Gene Ther. 2004 Apr;11(7):619-27 PMID: 14973546
  88. A genome-wide screen identifies the evolutionarily conserved KEOPS complex as a telomere regulator.
    Cell. 2006 Mar 24;124(6):1155-68 PMID: 16564010
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
1460-2075
DOI
10.1038/emboj.2010.363
Email
basma@ufl.edu.edu
Published
2011-03-02
Epub
2011-00-01
Pages
882-93
Language
English
Region
England
NLM ID
8208664
PMCID
PMC3049207
Subset
IM
Grants
Medical Research Council · MC_U105192716 · United Kingdom
NIGMS NIH HHS · R01 GM070641 · United States
NIGMS NIH HHS · R01 GM70641-01 · United States
External Links
PubMed source DOI: 10.1038/emboj.2010.363 PMC Full Text View journal details
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