RNA-dependent Conversion of Phosphoserine Forms Selenocysteine in Eukaryotes and Archaea

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2006 Dec 5

PMID 17142313

Citations 98

Authors

Jing Yuan

Sotiria Palioura

Juan Carlos Salazar

Dan Su

Patrick ODonoghue

Michael J Hohn

Alexander Machado Cardoso

William B Whitman

Dieter Soll

Affiliations

Soon will be listed here.

Abstract

The trace element selenium is found in proteins as selenocysteine (Sec), the 21st amino acid to participate in ribosome-mediated translation. The substrate for ribosomal protein synthesis is selenocysteinyl-tRNA(Sec). Its biosynthesis from seryl-tRNA(Sec) has been established for bacteria, but the mechanism of conversion from Ser-tRNA(Sec) remained unresolved for archaea and eukarya. Here, we provide evidence for a different route present in these domains of life that requires the tRNA(Sec)-dependent conversion of O-phosphoserine (Sep) to Sec. In this two-step pathway, O-phosphoseryl-tRNA(Sec) kinase (PSTK) converts Ser-tRNA(Sec) to Sep-tRNA(Sec). This misacylated tRNA is the obligatory precursor for a Sep-tRNA:Sec-tRNA synthase (SepSecS); this protein was previously annotated as SLA/LP. The human and archaeal SepSecS genes complement in vivo an Escherichia coli Sec synthase (SelA) deletion strain. Furthermore, purified recombinant SepSecS converts Sep-tRNA(Sec) into Sec-tRNA(Sec) in vitro in the presence of sodium selenite and purified recombinant E. coli selenophosphate synthetase (SelD). Phylogenetic arguments suggest that Sec decoding was present in the last universal common ancestor. SepSecS and PSTK coevolved with the archaeal and eukaryotic lineages, but the history of PSTK is marked by several horizontal gene transfer events, including transfer to non-Sec-decoding Cyanobacteria and fungi.

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References

Ibba M, Soll D . Quality control mechanisms during translation. Science. 1999; 286(5446):1893-7. DOI: 10.1126/science.286.5446.1893. View

Wies I, Brunner S, Henninger J, Herkel J, Kanzler S, Meyer zum Buschenfelde K . Identification of target antigen for SLA/LP autoantibodies in autoimmune hepatitis. Lancet. 2000; 355(9214):1510-5. DOI: 10.1016/s0140-6736(00)02166-8. View

Datsenko K, Wanner B . One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000; 97(12):6640-5. PMC: 18686. DOI: 10.1073/pnas.120163297. View

Rother M, Wilting R, Commans S, Bock A . Identification and characterisation of the selenocysteine-specific translation factor SelB from the archaeon Methanococcus jannaschii. J Mol Biol. 2000; 299(2):351-8. DOI: 10.1006/jmbi.2000.3756. View

Costa M, Rodriguez-Sanchez J, Czaja A, Gelpi C . Isolation and characterization of cDNA encoding the antigenic protein of the human tRNP(Ser)Sec complex recognized by autoantibodies from patients withtype-1 autoimmune hepatitis. Clin Exp Immunol. 2000; 121(2):364-74. PMC: 1905695. DOI: 10.1046/j.1365-2249.2000.01280.x. View

Ibba M, Soll D . Aminoacyl-tRNA synthesis. Annu Rev Biochem. 2000; 69:617-50. DOI: 10.1146/annurev.biochem.69.1.617. View

Wiemann S, Weil B, Wellenreuther R, Gassenhuber J, Glassl S, Ansorge W . Toward a catalog of human genes and proteins: sequencing and analysis of 500 novel complete protein coding human cDNAs. Genome Res. 2001; 11(3):422-35. PMC: 311072. DOI: 10.1101/gr.gr1547r. View

Kernebeck T, Lohse A, Grotzinger J . A bioinformatical approach suggests the function of the autoimmune hepatitis target antigen soluble liver antigen/liver pancreas. Hepatology. 2001; 34(2):230-3. DOI: 10.1053/jhep.2001.26632. View

Lacourciere G, Levine R, Stadtman T . Direct detection of potential selenium delivery proteins by using an Escherichia coli strain unable to incorporate selenium from selenite into proteins. Proc Natl Acad Sci U S A. 2002; 99(14):9150-3. PMC: 123109. DOI: 10.1073/pnas.142291199. View

10.

Kryukov G, Castellano S, Novoselov S, Lobanov A, Zehtab O, Guigo R . Characterization of mammalian selenoproteomes. Science. 2003; 300(5624):1439-43. DOI: 10.1126/science.1083516. View

11.

Guindon S, Gascuel O . A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003; 52(5):696-704. DOI: 10.1080/10635150390235520. View

12.

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

13.

Ibba M, Soll D . Aminoacyl-tRNAs: setting the limits of the genetic code. Genes Dev. 2004; 18(7):731-8. DOI: 10.1101/gad.1187404. View

14.

Kryukov G, Gladyshev V . The prokaryotic selenoproteome. EMBO Rep. 2004; 5(5):538-43. PMC: 1299047. DOI: 10.1038/sj.embor.7400126. View

15.

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

16.

MATTHAEI J, Voigt H, Heller G, NETH R, Schoch G, Kubler H . Specific interactions of ribosomes in decoding. Cold Spring Harb Symp Quant Biol. 1966; 31:25-38. DOI: 10.1101/sqb.1966.031.01.009. View

17.

Maenpaa P, BERNFIELD M . A specific hepatic transfer RNA for phosphoserine. Proc Natl Acad Sci U S A. 1970; 67(2):688-95. PMC: 283260. DOI: 10.1073/pnas.67.2.688. View

18.

Sharp S, Stewart T . The characterization of phosphoseryl tRNA from lactating bovine mammary gland. Nucleic Acids Res. 1977; 4(7):2123-36. PMC: 342552. DOI: 10.1093/nar/4.7.2123. View

19.

Leinfelder W, Zehelein E, Mandrand-Berthelot M, Bock A . Gene for a novel tRNA species that accepts L-serine and cotranslationally inserts selenocysteine. Nature. 1988; 331(6158):723-5. DOI: 10.1038/331723a0. View

20.

Schon A, Bock A, Ott G, Sprinzl M, Soll D . The selenocysteine-inserting opal suppressor serine tRNA from E. coli is highly unusual in structure and modification. Nucleic Acids Res. 1989; 17(18):7159-65. PMC: 334795. DOI: 10.1093/nar/17.18.7159. View