C-terminal Domain of Archaeal O-phosphoseryl-tRNA Kinase Displays Large-scale Motion to Bind the 7-bp D-stem of Archaeal TRNA(Sec)

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2010 Sep 28

PMID 20870747

Citations 12

Authors

R Lynn Sherrer

Yuhei Araiso

Caroline Aldag

Ryuichiro Ishitani

Joanne M L Ho

Dieter Soll

Osamu Nureki

Affiliations

Soon will be listed here.

Abstract

O-Phosphoseryl-tRNA kinase (PSTK) is the key enzyme in recruiting selenocysteine (Sec) to the genetic code of archaea and eukaryotes. The enzyme phosphorylates Ser-tRNA(Sec) to produce O-phosphoseryl-tRNA(Sec) (Sep-tRNA(Sec)) that is then converted to Sec-tRNA(Sec) by Sep-tRNA:Sec-tRNA synthase. Earlier we reported the structure of the Methanocaldococcus jannaschii PSTK (MjPSTK) complexed with AMPPNP. This study presents the crystal structure (at 2.4-Å resolution) of MjPSTK complexed with an anticodon-stem/loop truncated tRNA(Sec) (Mj*tRNA(Sec)), a good enzyme substrate. Mj*tRNA(Sec) is bound between the enzyme's C-terminal domain (CTD) and N-terminal kinase domain (NTD) that are connected by a flexible 11 amino acid linker. Upon Mj*tRNA(Sec) recognition the CTD undergoes a 62-Å movement to allow proper binding of the 7-bp D-stem. This large reorganization of the PSTK quaternary structure likely provides a means by which the unique tRNA(Sec) species can be accurately recognized with high affinity by the translation machinery. However, while the NTD recognizes the tRNA acceptor helix, shortened versions of MjPSTK (representing only 60% of the original size, in which the entire CTD, linker loop and an adjacent NTD helix are missing) are still active in vivo and in vitro, albeit with reduced activity compared to the full-length enzyme.

Citing Articles

PSTK exerts protective role in cisplatin-tubular cell injury via BAX/BCL2/Caspase3 pathway.

Wu Y, Xv Y, Zhao L, Zhou Z, Wang M, Xi J Physiol Rep. 2025; 13(1):e70162.

PMID: 39794890 PMC: 11723822. DOI: 10.14814/phy2.70162.

Unconventional genetic code systems in archaea.

Meng K, Chung C, Soll D, Krahn N Front Microbiol. 2022; 13:1007832.

PMID: 36160229 PMC: 9499178. DOI: 10.3389/fmicb.2022.1007832.

Naturally Occurring tRNAs With Non-canonical Structures.

Krahn N, Fischer J, Soll D Front Microbiol. 2020; 11:596914.

PMID: 33193279 PMC: 7609411. DOI: 10.3389/fmicb.2020.596914.

Trypanosomatid selenophosphate synthetase structure, function and interaction with selenocysteine lyase.

da Silva M, E Silva I, Faim L, Bellini N, Pereira M, Lima A PLoS Negl Trop Dis. 2020; 14(10):e0008091.

PMID: 33017394 PMC: 7595633. DOI: 10.1371/journal.pntd.0008091.

Kti12, a PSTK-like tRNA dependent ATPase essential for tRNA modification by Elongator.

Krutyholowa R, Hammermeister A, Zabel R, Abdel-Fattah W, Reinhardt-Tews A, Helm M Nucleic Acids Res. 2019; 47(9):4814-4830.

PMID: 30916349 PMC: 6511879. DOI: 10.1093/nar/gkz190.

References

Palioura S, Sherrer R, Steitz T, Soll D, Simonovic M . The human SepSecS-tRNASec complex reveals the mechanism of selenocysteine formation. Science. 2009; 325(5938):321-5. PMC: 2857584. DOI: 10.1126/science.1173755. View

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

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

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

Sturchler C, Westhof E, Carbon P, Krol A . Unique secondary and tertiary structural features of the eucaryotic selenocysteine tRNA(Sec). Nucleic Acids Res. 1993; 21(5):1073-9. PMC: 309265. DOI: 10.1093/nar/21.5.1073. View

Itoh Y, Chiba S, Sekine S, Yokoyama S . Crystal structure of human selenocysteine tRNA. Nucleic Acids Res. 2009; 37(18):6259-68. PMC: 2764427. DOI: 10.1093/nar/gkp648. View

Baker N, Sept D, Joseph S, Holst M, McCammon J . Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A. 2001; 98(18):10037-41. PMC: 56910. DOI: 10.1073/pnas.181342398. View

Emsley P, Cowtan K . Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004; 60(Pt 12 Pt 1):2126-32. DOI: 10.1107/S0907444904019158. View

Adams P, Grosse-Kunstleve R, Hung L, Ioerger T, McCoy A, Moriarty N . PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr. 2002; 58(Pt 11):1948-54. DOI: 10.1107/s0907444902016657. View

10.

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

11.

Palioura S, Herkel J, Simonovic M, Lohse A, Soll D . Human SepSecS or SLA/LP: selenocysteine formation and autoimmune hepatitis. Biol Chem. 2010; 391(7):771-6. PMC: 6644032. DOI: 10.1515/BC.2010.078. View

12.

Yuan J, ODonoghue P, Ambrogelly A, Gundllapalli S, Sherrer R, Palioura S . Distinct genetic code expansion strategies for selenocysteine and pyrrolysine are reflected in different aminoacyl-tRNA formation systems. FEBS Lett. 2009; 584(2):342-9. PMC: 2795046. DOI: 10.1016/j.febslet.2009.11.005. View

13.

Nakanishi K, Bonnefond L, Kimura S, Suzuki T, Ishitani R, Nureki O . Structural basis for translational fidelity ensured by transfer RNA lysidine synthetase. Nature. 2009; 461(7267):1144-8. DOI: 10.1038/nature08474. View

14.

. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature. 2009; 460(7253):345-51. PMC: 3747554. DOI: 10.1038/nature08140. View

15.

Murshudov G, Vagin A, Dodson E . Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997; 53(Pt 3):240-55. DOI: 10.1107/S0907444996012255. View

16.

Cook A, Fukuhara N, Jinek M, Conti E . Structures of the tRNA export factor in the nuclear and cytosolic states. Nature. 2009; 461(7260):60-5. DOI: 10.1038/nature08394. View

17.

Otwinowski Z, Minor W . Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997; 276:307-26. DOI: 10.1016/S0076-6879(97)76066-X. View

18.

Chiba S, Itoh Y, Sekine S, Yokoyama S . Structural basis for the major role of O-phosphoseryl-tRNA kinase in the UGA-specific encoding of selenocysteine. Mol Cell. 2010; 39(3):410-20. DOI: 10.1016/j.molcel.2010.07.018. View

19.

Miroux B, Walker J . Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol. 1996; 260(3):289-98. DOI: 10.1006/jmbi.1996.0399. View

20.

Shoemaker B, Portman J, Wolynes P . Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc Natl Acad Sci U S A. 2000; 97(16):8868-73. PMC: 16787. DOI: 10.1073/pnas.160259697. View