Structure of a TRNA-dependent Kinase Essential for Selenocysteine Decoding

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2009 Oct 7

PMID 19805283

Citations 10

Authors

Yuhei Araiso

R Lynn Sherrer

Ryuichiro Ishitani

Joanne M L Ho

Dieter Soll

Osamu Nureki

Affiliations

Soon will be listed here.

Abstract

Compared to bacteria, archaea and eukaryotes employ an additional enzyme for the biosynthesis of selenocysteine (Sec), the 21(st) natural amino acid (aa). An essential RNA-dependent kinase, O-phosphoseryl-tRNA(Sec) kinase (PSTK), converts seryl-tRNA(Sec) to O-phosphoseryl-tRNA(Sec), the immediate precursor of selenocysteinyl-tRNA(Sec). The sequence of Methanocaldococcus jannaschii PSTK (MjPSTK) suggests an N-terminal kinase domain (177 aa) followed by a presumed tRNA binding region (75 aa). The structures of MjPSTK complexed with ADP and AMPPNP revealed that this enzyme belongs to the P-loop kinase class, and that the kinase domain is closely related to gluconate kinase and adenylate kinase. ATP is bound by the P-loop domain (residues 11-18). Formed by antiparallel dimerization of two PSTK monomers, the enzyme structure shows a deep groove with positive electrostatic potential. Located in this groove is the enzyme's active site, which biochemical and genetic data suggest is composed of Asp-41, Arg-44, Glu-55, Tyr-82, Tyr-83, Met-86, and Met-132. Based on structural comparison with Escherichia coli adenylate kinase a docking model was generated that assigns these amino acids to the recognition of the terminal A76-Ser moieties of Ser-tRNA(Sec). The geometry and electrostatic environment of the groove in MjPSTK are perfectly complementary to the unusually long acceptor helix of tRNA(Sec).

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References

Yoshizawa S, Bock A . The many levels of control on bacterial selenoprotein synthesis. Biochim Biophys Acta. 2009; 1790(11):1404-14. DOI: 10.1016/j.bbagen.2009.03.010. View

MacRae I, Segel I, Fisher A . Crystal structure of adenosine 5'-phosphosulfate kinase from Penicillium chrysogenum. Biochemistry. 2000; 39(7):1613-21. DOI: 10.1021/bi9924157. View

Berry M, Meador B, Bilderback T, Liang P, Glaser M, Phillips Jr G . The closed conformation of a highly flexible protein: the structure of E. coli adenylate kinase with bound AMP and AMPPNP. Proteins. 1994; 19(3):183-98. DOI: 10.1002/prot.340190304. View

Sanner M, Olson A, Spehner J . Reduced surface: an efficient way to compute molecular surfaces. Biopolymers. 1996; 38(3):305-20. DOI: 10.1002/(SICI)1097-0282(199603)38:3%3C305::AID-BIP4%3E3.0.CO;2-Y. View

Su D, Hohn M, Palioura S, Sherrer R, Yuan J, Soll D . How an obscure archaeal gene inspired the discovery of selenocysteine biosynthesis in humans. IUBMB Life. 2008; 61(1):35-9. DOI: 10.1002/iub.136. View

Oshikane H, Sheppard K, Fukai S, Nakamura Y, Ishitani R, Numata T . Structural basis of RNA-dependent recruitment of glutamine to the genetic code. Science. 2006; 312(5782):1950-4. DOI: 10.1126/science.1128470. View

Carlson B, Xu X, Kryukov G, Rao M, Berry M, Gladyshev V . Identification and characterization of phosphoseryl-tRNA[Ser]Sec kinase. Proc Natl Acad Sci U S A. 2004; 101(35):12848-53. PMC: 516484. DOI: 10.1073/pnas.0402636101. View

Xu X, Carlson B, Mix H, Zhang Y, Saira K, Glass R . Biosynthesis of selenocysteine on its tRNA in eukaryotes. PLoS Biol. 2006; 5(1):e4. PMC: 1717018. DOI: 10.1371/journal.pbio.0050004. View

Shindyalov I, Bourne P . Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 1998; 11(9):739-47. DOI: 10.1093/protein/11.9.739. View

10.

Wu J, Bu W, Sheppard K, Kitabatake M, Kwon S, Soll D . Insights into tRNA-dependent amidotransferase evolution and catalysis from the structure of the Aquifex aeolicus enzyme. J Mol Biol. 2009; 391(4):703-16. PMC: 2830067. DOI: 10.1016/j.jmb.2009.06.014. View

11.

Kraft L, Sprenger G, Lindqvist Y . Conformational changes during the catalytic cycle of gluconate kinase as revealed by X-ray crystallography. J Mol Biol. 2002; 318(4):1057-69. DOI: 10.1016/S0022-2836(02)00215-2. View

12.

Sherrer R, ODonoghue P, Soll D . Characterization and evolutionary history of an archaeal kinase involved in selenocysteinyl-tRNA formation. Nucleic Acids Res. 2008; 36(4):1247-59. PMC: 2275090. DOI: 10.1093/nar/gkm1134. View

13.

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

14.

Sheppard K, Yuan J, Hohn M, Jester B, Devine K, Soll D . From one amino acid to another: tRNA-dependent amino acid biosynthesis. Nucleic Acids Res. 2008; 36(6):1813-25. PMC: 2330236. DOI: 10.1093/nar/gkn015. View

15.

Yuan J, Palioura S, Salazar J, Su D, ODonoghue P, Hohn M . RNA-dependent conversion of phosphoserine forms selenocysteine in eukaryotes and archaea. Proc Natl Acad Sci U S A. 2006; 103(50):18923-7. PMC: 1748153. DOI: 10.1073/pnas.0609703104. View

16.

Bilokapic S, Korencic D, Soll D, Weygand-Durasevic I . The unusual methanogenic seryl-tRNA synthetase recognizes tRNASer species from all three kingdoms of life. Eur J Biochem. 2004; 271(4):694-702. DOI: 10.1111/j.1432-1033.2003.03971.x. View

17.

Sherrer R, Ho J, Soll D . Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O-phosphoseryl-tRNASec kinase. Nucleic Acids Res. 2008; 36(6):1871-80. PMC: 2330242. DOI: 10.1093/nar/gkn036. View

18.

Nicholls A, Sharp K, Honig B . Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 1991; 11(4):281-96. DOI: 10.1002/prot.340110407. View

19.

Leipe D, Koonin E, Aravind L . Evolution and classification of P-loop kinases and related proteins. J Mol Biol. 2003; 333(4):781-815. DOI: 10.1016/j.jmb.2003.08.040. View

20.

Galburt E, Pelletier J, Wilson G, Stoddard B . Structure of a tRNA repair enzyme and molecular biology workhorse: T4 polynucleotide kinase. Structure. 2002; 10(9):1249-60. DOI: 10.1016/s0969-2126(02)00835-3. View