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The ATP-mediated formation of the YgjD-YeaZ-YjeE complex is required for the biosynthesis of tRNA t6A in Escherichia coli.

Zhang W, Collinet B, Perrochia L, Durand D, van Tilbeurgh H
Nucleic Acids Res 43 1804-17 (2015)
Related entries: 4wq5, 4ydu

Cited: 29 times
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Abstract

The essential and universal N(6)-threonylcarbamoyladenosine (t(6)A) modification at position 37 of ANN-decoding tRNAs plays a pivotal role in translational fidelity through enhancement of the cognate codon recognition and stabilization of the codon-anticodon interaction. In Escherichia coli, the YgjD (TsaD), YeaZ (TsaB), YjeE (TsaE) and YrdC (TsaC) proteins are necessary and sufficient for the in vitro biosynthesis of t(6)A, using tRNA, ATP, L-threonine and bicarbonate as substrates. YrdC synthesizes the short-lived L-threonylcarbamoyladenylate (TCA), and YgjD, YeaZ and YjeE cooperate to transfer the L-threonylcarbamoyl-moiety from TCA onto adenosine at position 37 of substrate tRNA. We determined the crystal structure of the heterodimer YgjD-YeaZ at 2.3 Å, revealing the presence of an unexpected molecule of ADP bound at an atypical site situated at the YgjD-YeaZ interface. We further showed that the ATPase activity of YjeE is strongly activated by the YgjD-YeaZ heterodimer. We established by binding experiments and SAXS data analysis that YgjD-YeaZ and YjeE form a compact ternary complex only in presence of ATP. The formation of the ternary YgjD-YeaZ-YjeE complex is required for the in vitro biosynthesis of t(6)A but not its ATPase activity.

Reviews - 4wq4 mentioned but not cited (1)

  1. The structural and functional workings of KEOPS. Beenstock J, Sicheri F. Nucleic Acids Res 49 10818-10834 (2021)

Articles - 4wq4 mentioned but not cited (2)

  1. The ATP-mediated formation of the YgjD-YeaZ-YjeE complex is required for the biosynthesis of tRNA t6A in Escherichia coli. Zhang W, Collinet B, Perrochia L, Durand D, van Tilbeurgh H. Nucleic Acids Res. 43 1804-1817 (2015)
  2. Predictive approaches to guide the expression of recombinant vaccine targets in Escherichia coli: a case study presentation utilising Absynth Biologics Ltd. proprietary Clostridium difficile vaccine antigens. Hussain H, McKenzie EA, Robinson AM, Gingles NA, Marston F, Warwicker J, Dickson AJ. Appl Microbiol Biotechnol 105 5657-5674 (2021)


Reviews citing this publication (3)

  1. Conservation and Diversification of tRNA t6A-Modifying Enzymes across the Three Domains of Life. Su C, Jin M, Zhang W. Int J Mol Sci 23 13600 (2022)
  2. Interaction between two essential, conserved bacterial proteins YeaZ and glycoprotease as a potential antibacterial target in multi-drug-resistant Staphylococcus aureus. Britton TA, Guo H, Ji Y. Sci Prog 103 36850419890521 (2020)
  3. Metal utilization in genome-reduced bacteria: Do human mycoplasmas rely on iron? Perálvarez-Marín A, Baranowski E, Bierge P, Pich OQ, Lebrette H. Comput Struct Biotechnol J 19 5752-5761 (2021)

Articles citing this publication (23)

  1. Crystal structures of the Gon7/Pcc1 and Bud32/Cgi121 complexes provide a model for the complete yeast KEOPS complex. Zhang W, Collinet B, Graille M, Daugeron MC, Lazar N, Libri D, Durand D, van Tilbeurgh H. Nucleic Acids Res. 43 3358-3372 (2015)
  2. Proteomic analysis of the human KEOPS complex identifies C14ORF142 as a core subunit homologous to yeast Gon7. Wan LC, Maisonneuve P, Szilard RK, Lambert JP, Ng TF, Manczyk N, Huang H, Laister R, Caudy AA, Gingras AC, Durocher D, Sicheri F. Nucleic Acids Res. 45 805-817 (2017)
  3. The i6A37 tRNA modification is essential for proper decoding of UUX-Leucine codons during rpoS and iraP translation. Aubee JI, Olu M, Thompson KM. RNA 22 729-742 (2016)
  4. CO2-sensitive tRNA modification associated with human mitochondrial disease. Lin H, Miyauchi K, Harada T, Okita R, Takeshita E, Komaki H, Fujioka K, Yagasaki H, Goto YI, Yanaka K, Nakagawa S, Sakaguchi Y, Suzuki T. Nat Commun 9 1875 (2018)
  5. Biochemical evidence for relaxed substrate specificity of Nα-acetyltransferase (Rv3420c/rimI) of Mycobacterium tuberculosis. Pathak D, Bhat AH, Sapehia V, Rai J, Rao A. Sci Rep 6 28892 (2016)
  6. An extensive allelic series of Drosophila kae1 mutants reveals diverse and tissue-specific requirements for t6A biogenesis. Lin CJ, Smibert P, Zhao X, Hu JF, Ramroop J, Kellner SM, Benton MA, Govind S, Dedon PC, Sternglanz R, Lai EC. RNA 21 2103-2118 (2015)
  7. Crystal structure of YeaZ from Pseudomonas aeruginosa. Vecchietti D, Ferrara S, Rusmini R, Macchi R, Milani M, Bertoni G. Biochem. Biophys. Res. Commun. 470 460-465 (2016)
  8. Structure and mechanism of a bacterial t6A biosynthesis system. Luthra A, Swinehart W, Bayooz S, Phan P, Stec B, Iwata-Reuyl D, Swairjo MA. Nucleic Acids Res. 46 1395-1411 (2018)
  9. Structure of a reaction intermediate mimic in t6A biosynthesis bound in the active site of the TsaBD heterodimer from Escherichia coli. Kopina BJ, Missoury S, Collinet B, Fulton MG, Cirio C, van Tilbeurgh H, Lauhon CT. Nucleic Acids Res 49 2141-2160 (2021)
  10. Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages. Bennett GM, Mao M. Environ. Microbiol. 20 4461-4472 (2018)
  11. Bacillus subtilis Nucleoid-Associated Protein YlxR Is Involved in Bimodal Expression of the Fructoselysine Utilization Operon (frlBONMD-yurJ) Promoter. Ogura M, Shindo K, Kanesaki Y. Front Microbiol 11 2024 (2020)
  12. Commonality and diversity in tRNA substrate recognition in t6A biogenesis by eukaryotic KEOPSs. Wang JT, Zhou JB, Mao XL, Zhou L, Chen M, Zhang W, Wang ED, Zhou XL. Nucleic Acids Res 50 2223-2239 (2022)
  13. Molecular basis for t6A modification in human mitochondria. Zhou JB, Wang Y, Zeng QY, Meng SX, Wang ED, Zhou XL. Nucleic Acids Res 48 3181-3194 (2020)
  14. Protein target highlights in CASP15: Analysis of models by structure providers. Alexander LT, Durairaj J, Kryshtafovych A, Abriata LA, Bayo Y, Bhabha G, Breyton C, Caulton SG, Chen J, Degroux S, Ekiert DC, Erlandsen BS, Freddolino PL, Gilzer D, Greening C, Grimes JM, Grinter R, Gurusaran M, Hartmann MD, Hitchman CJ, Keown JR, Kropp A, Kursula P, Lovering AL, Lemaitre B, Lia A, Liu S, Logotheti M, Lu S, Markússon S, Miller MD, Minasov G, Niemann HH, Opazo F, Phillips GN, Davies OR, Rommelaere S, Rosas-Lemus M, Roversi P, Satchell K, Smith N, Wilson MA, Wu KL, Xia X, Xiao H, Zhang W, Zhou ZH, Fidelis K, Topf M, Moult J, Schwede T. Proteins 91 1571-1599 (2023)
  15. Structure-function analysis of Sua5 protein reveals novel functional motifs required for the biosynthesis of the universal t6A tRNA modification. Pichard-Kostuch A, Zhang W, Liger D, Daugeron MC, Létoquart J, Li de la Sierra-Gallay I, Forterre P, Collinet B, van Tilbeurgh H, Basta T. RNA 24 926-938 (2018)
  16. The structure of the TsaB/TsaD/TsaE complex reveals an unexpected mechanism for the bacterial t6A tRNA-modification. Missoury S, Plancqueel S, Li de la Sierra-Gallay I, Zhang W, Liger D, Durand D, Dammak R, Collinet B, van Tilbeurgh H. Nucleic Acids Res. 46 5850-5860 (2018)
  17. Conformational communication mediates the reset step in t6A biosynthesis. Luthra A, Paranagama N, Swinehart W, Bayooz S, Phan P, Quach V, Schiffer JM, Stec B, Iwata-Reuyl D, Swairjo MA. Nucleic Acids Res. 47 6551-6567 (2019)
  18. CycA-Dependent Glycine Assimilation Is Connected to Novobiocin Susceptibility in Escherichia coli. Shi H, Zhang L, Gu J, Li J, Liu Z, Deng JY. Microbiol Spectr 10 e0250122 (2022)
  19. Expression and protease characterization of a conserved protein YgjD in Vibrio harveyi. Zhang Y, Chen J, Wang Y, Li Y, Rui W, Zhang J, Luo D. PeerJ 8 e9061 (2020)
  20. Glucose-Mediated Protein Arginine Phosphorylation/Dephosphorylation Regulates ylxR Encoding Nucleoid-Associated Protein and Cell Growth in Bacillus subtilis. Ogura M. Front Microbiol 11 590828 (2020)
  21. Reductions in bacterial viability stimulate the production of Extra-intestinal Pathogenic Escherichia coli (ExPEC) cytoplasm-carrying Extracellular Vesicles (EVs). Jiang M, Wang Z, Xia F, Wen Z, Chen R, Zhu D, Wang M, Zhuge X, Dai J. PLoS Pathog 18 e1010908 (2022)
  22. Specificity in the biosynthesis of the universal tRNA nucleoside N 6-threonylcarbamoyl adenosine (t6A)-TsaD is the gatekeeper. Swinehart W, Deutsch C, Sarachan KL, Luthra A, Bacusmo JM, de Crécy-Lagard V, Swairjo MA, Agris PF, Iwata-Reuyl D. RNA 26 1094-1103 (2020)
  23. Structure-function analysis of an ancient TsaD-TsaC-SUA5-TcdA modular enzyme reveals a prototype of tRNA t6A and ct6A synthetases. Jin M, Zhang Z, Yu Z, Chen W, Wang X, Lei D, Zhang W. Nucleic Acids Res 51 8711-8729 (2023)


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