A Single TRNA Base Pair Mediates Bacterial TRNA-dependent Biosynthesis of Asparagine

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2006 Nov 1

PMID 17074748

Citations 28

Authors

Marc Bailly

Stamatina Giannouli

Mickael Blaise

Constantinos Stathopoulos

Daniel Kern

Hubert Dominique Becker

Affiliations

Soon will be listed here.

Abstract

In many prokaryotes and in organelles asparagine and glutamine are formed by a tRNA-dependent amidotransferase (AdT) that catalyzes amidation of aspartate and glutamate, respectively, mischarged on tRNAAsn and tRNAGln. These pathways supply the deficiency of the organism in asparaginyl- and glutaminyl-tRNA synthtetases and provide the translational machinery with Asn-tRNAAsn and Gln-tRNAGln. So far, nothing is known about the structural elements that confer to tRNA the role of a specific cofactor in the formation of the cognate amino acid. We show herein, using aspartylated tRNAAsn and tRNAAsp variants, that amidation of Asp acylating tRNAAsn is promoted by the base pair U1-A72 whereas the G1-C72 pair and presence of the supernumerary nucleotide U20A in the D-loop of tRNAAsp prevent amidation. We predict, based on comparison of tRNAGln and tRNAGlu sequence alignments from bacteria using the AdT-dependent pathway to form Gln-tRNAGln, that the same combination of nucleotides also rules specific tRNA-dependent formation of Gln. In contrast, we show that the tRNA-dependent conversion of Asp into Asn by archaeal AdT is mainly mediated by nucleotides G46 and U47 of the variable region. In the light of these results we propose that bacterial and archaeal AdTs use kingdom-specific signals to catalyze the tRNA-dependent formations of Asn and Gln.

Citing Articles

The tRNA identity landscape for aminoacylation and beyond.

Giege R, Eriani G Nucleic Acids Res. 2023; 51(4):1528-1570.

PMID: 36744444 PMC: 9976931. DOI: 10.1093/nar/gkad007.

Clinically Relevant Mutations of Mycobacterial GatCAB Inform Regulation of Translational Fidelity.

Li Y, Cai R, Yang J, Hendrickson T, Xiang Y, Javid B mBio. 2021; 12(4):e0110021.

PMID: 34225495 PMC: 8406222. DOI: 10.1128/mBio.01100-21.

BpForms and BcForms: a toolkit for concretely describing non-canonical polymers and complexes to facilitate global biochemical networks.

Lang P, Chebaro Y, Zheng X, Sekar J, Shaikh B, Natale D Genome Biol. 2020; 21(1):117.

PMID: 32423472 PMC: 7236495. DOI: 10.1186/s13059-020-02025-z.

Development of Assay Systems for Amber Codon Decoding at the Steps of Initiation and Elongation in Mycobacteria.

Govindan A, Miryala S, Mondal S, Varshney U J Bacteriol. 2018; 200(22).

PMID: 30181124 PMC: 6199473. DOI: 10.1128/JB.00372-18.

Aminoacyl-tRNA Synthetases in the Bacterial World.

Giege R, Springer M EcoSal Plus. 2016; 7(1).

PMID: 27223819 PMC: 11575706. DOI: 10.1128/ecosalplus.ESP-0002-2016.

References

Becker H, Giege R, Kern D . Identity of prokaryotic and eukaryotic tRNA(Asp) for aminoacylation by aspartyl-tRNA synthetase from Thermus thermophilus. Biochemistry. 1996; 35(23):7447-58. DOI: 10.1021/bi9601058. View

Sherman J, Soll D . Aminoacyl-tRNA synthetases optimize both cognate tRNA recognition and discrimination against noncognate tRNAs. Biochemistry. 1996; 35(2):601-7. DOI: 10.1021/bi951602b. View

Sprinzl M, Horn C, Brown M, Ioudovitch A, Steinberg S . Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1998; 26(1):148-53. PMC: 147216. DOI: 10.1093/nar/26.1.148. View

Fechter P, Rudinger J, Giege R, Theobald-Dietrich A . Ribozyme processed tRNA transcripts with unfriendly internal promoter for T7 RNA polymerase: production and activity. FEBS Lett. 1998; 436(1):99-103. DOI: 10.1016/s0014-5793(98)01096-5. View

Becker H, Kern D . Thermus thermophilus: a link in evolution of the tRNA-dependent amino acid amidation pathways. Proc Natl Acad Sci U S A. 1998; 95(22):12832-7. PMC: 23616. DOI: 10.1073/pnas.95.22.12832. View

Curnow A, Tumbula D, Pelaschier J, Min B, Soll D . Glutamyl-tRNA(Gln) amidotransferase in Deinococcus radiodurans may be confined to asparagine biosynthesis. Proc Natl Acad Sci U S A. 1998; 95(22):12838-43. PMC: 23620. DOI: 10.1073/pnas.95.22.12838. View

Feng L, Sheppard K, Tumbula-Hansen D, Soll D . Gln-tRNAGln formation from Glu-tRNAGln requires cooperation of an asparaginase and a Glu-tRNAGln kinase. J Biol Chem. 2004; 280(9):8150-5. DOI: 10.1074/jbc.M411098200. View

Sauerwald A, Zhu W, Major T, Roy H, Palioura S, Jahn D . RNA-dependent cysteine biosynthesis in archaea. Science. 2005; 307(5717):1969-72. DOI: 10.1126/science.1108329. View

Schmitt E, Panvert M, Blanquet S, Mechulam Y . Structural basis for tRNA-dependent amidotransferase function. Structure. 2005; 13(10):1421-33. DOI: 10.1016/j.str.2005.06.016. View

10.

Freyhult E, Moulton V, Ardell D . Visualizing bacterial tRNA identity determinants and antideterminants using function logos and inverse function logos. Nucleic Acids Res. 2006; 34(3):905-16. PMC: 1363773. DOI: 10.1093/nar/gkj478. View

11.

Nakamura A, Yao M, Chimnaronk S, Sakai N, Tanaka I . Ammonia channel couples glutaminase with transamidase reactions in GatCAB. Science. 2006; 312(5782):1954-8. DOI: 10.1126/science.1127156. View

12.

Tettelin H, Saunders N, Heidelberg J, Jeffries A, Nelson K, Eisen J . Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science. 2000; 287(5459):1809-15. DOI: 10.1126/science.287.5459.1809. View

13.

Ibba M, Becker H, Stathopoulos C, Tumbula D, Soll D . The adaptor hypothesis revisited. Trends Biochem Sci. 2000; 25(7):311-6. DOI: 10.1016/s0968-0004(00)01600-5. View

14.

Becker H, Min B, Jacobi C, Raczniak G, Pelaschier J, Roy H . The heterotrimeric Thermus thermophilus Asp-tRNA(Asn) amidotransferase can also generate Gln-tRNA(Gln). FEBS Lett. 2000; 476(3):140-4. DOI: 10.1016/s0014-5793(00)01697-5. View

15.

Tumbula D, Becker H, Chang W, Soll D . Domain-specific recruitment of amide amino acids for protein synthesis. Nature. 2000; 407(6800):106-10. DOI: 10.1038/35024120. View

16.

LaRiviere F, Wolfson A, Uhlenbeck O . Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science. 2001; 294(5540):165-8. DOI: 10.1126/science.1064242. View

17.

Raczniak G, Becker H, Min B, Soll D . A single amidotransferase forms asparaginyl-tRNA and glutaminyl-tRNA in Chlamydia trachomatis. J Biol Chem. 2001; 276(49):45862-7. DOI: 10.1074/jbc.M109494200. View

18.

Asahara H, Uhlenbeck O . The tRNA specificity of Thermus thermophilus EF-Tu. Proc Natl Acad Sci U S A. 2002; 99(6):3499-504. PMC: 122552. DOI: 10.1073/pnas.052028599. View

19.

Roy H, Becker H, Reinbolt J, Kern D . When contemporary aminoacyl-tRNA synthetases invent their cognate amino acid metabolism. Proc Natl Acad Sci U S A. 2003; 100(17):9837-42. PMC: 187858. DOI: 10.1073/pnas.1632156100. View

20.

Kern D, Lapointe J . Glutamyl transfer ribonucleic acid synthetase of Escherichia coli. Effect of alteration of the 5-(methylaminomethyl)-2-thiouridine in the anticodon of glutamic acid transfer ribonucleic acid on the catalytic mechanism. Biochemistry. 1979; 18(26):5819-26. DOI: 10.1021/bi00593a011. View