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The unique tRNASec and its role in selenocysteine biosynthesis

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Abstract

Selenium (Se) is an essential trace element for several organisms and is mostly present in proteins as l-selenocysteine (Sec or U). Sec is synthesized on its l-seryl–tRNASec to produce Sec–tRNASec molecules by a dedicated selenocysteine synthesis machinery and incorporated into selenoproteins at specified in-frame UGA codons. UGA–Sec insertion is signaled by an mRNA stem-loop structure called the SElenoCysteine Insertion Sequence (SECIS). tRNASec transcription regulation and folding have been described showing its importance to Sec biosynthesis. Here, we discuss structural aspects of Sec–tRNASec and its role in Sec biosynthesis as well as Sec incorporation into selenoproteins. Defects in the Sec biosynthesis or incorporation pathway have been correlated with pathological conditions.

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References

  • Aeby E, Palioura S, Pusnik M, Marazzi J, Lieberman A, Ullu E, Soll D, Schneider A (2009) The canonical pathway for selenocysteine insertion is dispensable in Trypanosomes. Proc Natl Acad Sci USA 106:5088–5092

    Article  PubMed  Google Scholar 

  • Aeby E, Ullu E, Yepiskoposyan H, Schimanski B, Roditi I, Muehlemann O, Schneider A (2010) tRNA(Sec) is transcribed by RNA polymerase II in Trypanosoma brucei but not in humans. Nucleic Acids Res 38:5833–5843

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Agirrezabala X, Frank J (2009) Elongation in translation as a dynamic interaction among the ribosome, tRNA, and elongation factors EF-G and EF-Tu. Q Rev Biophys 42:159–200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Agris PF (2004) Decoding the genome: a modified view. Nucleic Acids Res 32:223–238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Agris PF (2008) Bringing order to translation: the contributions of transfer RNA anticodon-domain modifications. EMBO Rep 9:629–635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ahmad Z (2014) Statin intolerance. Am J Cardiol 113:1765–1771

    Article  PubMed  CAS  Google Scholar 

  • Araiso Y, Palioura S, Ishitani R, Sherrer RL, O’Donoghue P, Yuan J, Oshikane H, Domae N, DeFranco J, Soll D et al (2008) Structural insights into RNA-dependent eukaryal and archaeal selenocysteine formation. Nucleic Acids Res 36:1187–1199

    Article  PubMed  CAS  Google Scholar 

  • Archambault J, Friesen JD (1993) Genetics of eukaryotic RNA polymerase-I, polymerase-II, and polymerase-III. Microbiol Rev 57:703–724

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ardell DH, Hou YM (2016) Initiator tRNA genes template the 3’ CCA end at high frequencies in bacteria. BMC Genom 17:1003

    Article  CAS  Google Scholar 

  • Arner ESJ (2009) Focus on mammalian thioredoxin reductases—important selenoproteins with versatile functions. Biochimica Et Biophysica Acta-General Subjects 1790:495–526

    Article  CAS  Google Scholar 

  • Arner ESJ (2010) Selenoproteins—what unique properties can arise with selenocysteine in place of cysteine? Exp Cell Res 316:1296–1303

    Article  PubMed  CAS  Google Scholar 

  • Baron C, Bock A (1991) The length of the aminoacyl-acceptor stem of the selenocysteine-specific transfer rnasec of Escherichia-coli is the determinant for binding to elongation-factors selb or tu. J Biol Chem 266:20375–20379

    PubMed  CAS  Google Scholar 

  • Baron C, Westhof E, Bock A, Giege R (1993) Solution structure of selenocysteine-inserting transfer RNA(SEC) from Escherichia-coli—comparison with canonical transfer RNA(SER). J Mol Biol 231:274–292

    Article  PubMed  CAS  Google Scholar 

  • Barroso M, Florindo C, Kalwa H, Silva Z, Turanov AA, Carlson BA, de Almeida IT, Blom HJ, Gladyshev VN, Hatfield DL et al (2014) Inhibition of cellular methyltransferases promotes endothelial cell activation by suppressing glutathione peroxidase 1 protein expression. J Biol Chem 289:15350–15362

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bellinger FP, Raman AV, Reeves MA, Berry MJ (2009) Regulation and function of selenoproteins in human disease. Biochem J 422:11–22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berry MJ (2005) Insights into the hierarchy of selenium incorporation. Nat Genet 37:1162–1163

    Article  PubMed  CAS  Google Scholar 

  • Berry MJ, Tujebajeva RM, Copeland PR, Xu XM, Carlson BA, Martin GW, Low SC, Mansell JB, Grundner-Culemann E, Harney JW et al (2001) Selenocysteine incorporation directed from the 3′UTR: characterization of eukaryotic EFsec and mechanistic implications. BioFactors 14:17–24

    Article  PubMed  CAS  Google Scholar 

  • Beuning PJ, Musier-Forsyth K (1999) Transfer RNA recognition by aminoacyl-tRNA synthetases. Biopolymers 52:1–28

    Article  PubMed  CAS  Google Scholar 

  • Bifano AL, Atassi T, Ferrara T, Driscoll DM (2013) Identification of nucleotides and amino acids that mediate the interaction between ribosomal protein L30 and the SECIS element. BMC Mol Biol 14:12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bock A, Forchhammer K, Heider J, Baron C (1991a) Selenoprotein synthesis—an expansion of the genetic-code. Trends Biochem Sci 16:463–467

    Article  PubMed  CAS  Google Scholar 

  • Bock A, Forchhammer K, Heider J, Leinfelder W, Sawers G, Veprek B, Zinoni F (1991b) Selenocysteine—the 21st amino-acid. Mol Microbiol 5:515–520

    Article  PubMed  CAS  Google Scholar 

  • Bonilla M, Krull E, Irigoin F, Salinas G, Comini MA (2016) Selenoproteins of African trypanosomes are dispensable for parasite survival in a mammalian host. Mol Biochem Parasitol 206:13–19

    Article  PubMed  CAS  Google Scholar 

  • Bosl MR, Takaku K, Oshima M, Nishimura S, Taketo MM (1997) Early embryonic lethality caused by targeted disruption of the mouse selenocysteine tRNA gene (Trsp). Proc Natl Acad Sci USA 94:5531–5534

    Article  PubMed  CAS  Google Scholar 

  • Brocker MJ, Ho JML, Church GM, Soll D, O’Donoghue P (2014) Recoding the genetic code with selenocysteine. Angewandte Chemie-Int Edn 53:319–323

    Article  CAS  Google Scholar 

  • Browning DF, Busby SJW (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:57–65

    Article  PubMed  CAS  Google Scholar 

  • Budiman ME, Bubenik JL, Miniard AC, Middleton LM, Gerber CA, Cash A, Driscoll DM (2009) Eukaryotic initiation factor 4a3 is a selenium-regulated RNA-binding protein that selectively inhibits selenocysteine incorporation. Mol Cell 35:479–489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Budiman ME, Bubenik JL, Driscoll DM (2011) Identification of a signature motif for the eIF4a3-SECIS interaction. Nucleic Acids Res 39:7730–7739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bult CJ, White O, Olsen GJ, Zhou LX, Fleischmann RD, Sutton GG, Blake JA, FitzGerald LM, Clayton RA, Gocayne JD et al (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–1073

    Article  PubMed  CAS  Google Scholar 

  • Burkard U, Soll D (1988) The unusually long amino-acid acceptor stem of Escherichia-coli selenocystein transfer-RNA results from abnormal cleavage by RNase p. Nucleic Acids Res 16:11617–11624

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caban K, Copeland PR (2012) Selenocysteine insertion sequence (SECIS)-binding protein 2 alters conformational dynamics of residues involved in tRNA accommodation in 80 S ribosomes. J Biol Chem 287:10664–10673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caban K, Kinzy SA, Copeland PR (2007) The L7Ae RNA binding motif is a multifunctional domain required for the ribosome-dependent Sec incorporation activity of Sec insertion sequence binding protein 2. Mol Cell Biol 27:6350–6360

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carbon P, Krol A (1991) Transcription of the Xenopus-laevis selenocysteine transfer RNA(Ser)Sec gene—a system that combines an internal B box and upstream elements also found in U6 snRNA genes. EMBO J 10:599–606

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carlson BA, Xu XM, Gladyshev VN, Hatfield DL (2005) Um34 in selenocysteine tRNA is required for the expression of stress-related selenoproteins in mammals. Fine-Tuning of RNA Funct Modif Ed 12:431–438

    Article  CAS  Google Scholar 

  • Carlson BA, Yoo M-H, Tsuji PA, Gladyshev VN, Hatfield DL (2009) Mouse models targeting selenocysteine tRNA expression for elucidating the role of selenoproteins in health and development. Molecules 14:3509–3527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carlson BA, Tobe R, Yefremova E, Tsuji PA, Hoffmann VJ, Schweizer U, Gladyshev VN, Hatfield DL, Conrad M (2016) Glutathione peroxidase 4 and vitamin E cooperatively prevent hepatocellular degeneration. Redox Biol 9:22–31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carlson BA, Gupta N, Pinkerton MH, Hatfield DL, Copeland PR (2017) The utilization of selenocysteine-tRNA(Ser Sec) isoforms is regulated in part at the level of translation in vitro. Translation 5:e1314240

    Article  PubMed  PubMed Central  Google Scholar 

  • Chavatte L, Brown BA, Driscoll DM (2005) Ribosomal protein L30 is a component of the UGA-selenocysteine recoding machinery in eukaryotes. Nat Struct Mol Biol 12:408–416

    Article  PubMed  CAS  Google Scholar 

  • Chiba S, Itoh Y, Sekine S-I, Yokoyama S (2010) Structural basis for the major role of O-phosphoseryl-tRNA kinase in the UGA-specific encoding of selenocysteine. Mol Cell 39:410–420

    Article  PubMed  CAS  Google Scholar 

  • Choi IS, Diamond AM, Crain PF, Kolker JD, McCloskey JA, Hatfield DL (1994) Reconstitution of the biosynthetic-pathway of selenocysteine transfer-RNAS in xenopus-oocytes. Biochemistry 33:601–605

    Article  PubMed  CAS  Google Scholar 

  • Ciliberto G, Castagnoli L, Cortese R (1983) Transcription by RNA polymerase-III. Curr Top Dev Biol 18:59–88

    Article  PubMed  CAS  Google Scholar 

  • Collins R, Johansson A-L, Karlberg T, Markova N, van den Berg S, Olesen K, Hammarstrom M, Flores A, Schuler H, Schiavone LH et al. (2012) Biochemical discrimination between selenium and sulfur 1: a single residue provides selenium specificity to human selenocysteine lyase. PLoS One 7:e30581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Combs GF, Combs SB (1984) The nutritional biochemistry of selenium. Annu Rev Nutr 4:257–280

    Article  PubMed  CAS  Google Scholar 

  • Commans S, Bock A (1999) Selenocysteine inserting tRNAs: an overview. FEMS Microbiol Rev 23:335–351

    Article  PubMed  CAS  Google Scholar 

  • Copeland PR, Fletcher JE, Carlson BA, Hatfield DL, Driscoll DM (2000) A novel RNA binding protein, SBP2, is required for the translation of mammalian selenoprotein mRNAs (vol. 19, pg. 306, 2000). Embo J 19:6634–6634

  • Costa FC, Oliva MAV, de Jesus TCL, Schenkman S, Thiemann OH (2011) Oxidative stress protection of Trypanosomes requires selenophosphate synthase. Mol Biochem Parasitol 180:47–50

    Article  PubMed  CAS  Google Scholar 

  • Cravedi P, Mori G, Fischer F, Percudani R (2015) Evolution of the selenoproteome in Helicobacter pylori and epsilonproteobacteria. Genome Biol Evol 7:2692–2704

    PubMed  PubMed Central  CAS  Google Scholar 

  • Crick FHC (1966) Codon-anticodon pairing—wobble hypothesis. J Mol Biol 19:548

    Article  PubMed  CAS  Google Scholar 

  • Crick FHC (1968) Origin of genetic code. J Mol Biol 38:367

    Article  PubMed  CAS  Google Scholar 

  • da Silva MTA, Caldas VEA, Costa FC, Silvestre DAMM, Thiemann OH (2013) Selenocysteine biosynthesis and insertion machinery in Naegleria gruberi. Mol Biochem Parasitol 188:87–90

    Article  PubMed  CAS  Google Scholar 

  • da Silva MTA, Silva-Jardim I, Thiemann OH (2014) Biological implications of selenium and its role in trypanosomiasis treatment. Curr Med Chem 21:1772–1780

    Article  PubMed  CAS  Google Scholar 

  • Diamond A, Dudock B, Hatfield D (1981) Structure and properties of a bovine liver UGA suppressor serine tRNA with a tryptophan anticodon, vol 25. In: Dudock HDB (ed), pp 497–506

  • Diamond AM, Choi IS, Crain PF, Hashizume T, Pomerantz SC, Cruz R, Steer CJ, Hill KE, Burk RF, McCloskey JA et al (1993) Dietary selenium affects methylation of the wobble nucleoside in the anticodon of selenocysteine transfer RNA Ser Sec. J Biol Chem 268:14215–14223

    PubMed  CAS  Google Scholar 

  • Dobosz-Bartoszek M, Pinkerton MH, Otwinowski Z, Chakravarthy S, Soll D, Copeland PR, Simonovic M (2016) Crystal structures of the human elongation factor eEFSec suggest a non-canonical mechanism for selenocysteine incorporation. Nature Commun 7:12941

    Article  CAS  Google Scholar 

  • Ingold I, Berndt C, Schmitt S, Doll, S, Poschmann G, Buday K, Roveri A, Peng XX, Freitas FP, Seibt T et al (2018) Selenium utilization by GPX4 is required to prevent hydroperoxide-induced ferroptosis. Cell 172:409

  • Donovan J, Copeland PR (2009) Evolutionary history of selenocysteine incorporation from the perspective of SECIS binding proteins. BMC Evol Biol 9:229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Donovan J, Copeland PR (2010) Threading the needle: getting selenocysteine into proteins. Antioxid Redox Signal 12:881–892

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Donovan J, Caban K, Ranaweera R, Gonzalez-Flores JN, Copeland PR (2008) A novel protein domain induces high affinity selenocysteine insertion sequence binding and elongation factor recruitment. J Biol Chem 283:35129–35139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Driscoll DM, Copeland PR (2003) Mechanism and regulation of selenoprotein synthesis. Annu Rev Nutr 23:17–40

    Article  PubMed  CAS  Google Scholar 

  • Dunkle JA, Cate JHD (2010) Ribosome structure and dynamics during translocation and termination. Ann Rev Biophys 39(39):227–244

    Article  CAS  Google Scholar 

  • Ehrenreich A, Forchhammer K, Tormay P, Veprek B, Bock A (1992) Selenoprotein synthesis in Escherichia-coli—purification and characterization of the enzyme catalyzing selenium activation. Eur J Biochem 206:767–773

    Article  PubMed  CAS  Google Scholar 

  • Engelbergkulka H (1981) UGA suppression by normal transfer rnatrp in Escherichia-coli—codon context effects. Nucleic Acids Res 9:983–991

    Article  CAS  Google Scholar 

  • Engelberg-Kulka H, Liu ZS, Li C, Reches M (2001) An extended Escherichia coli “selenocysteine insertion sequence” (SECIS) as a multifunctional RNA structure. BioFactors 14:61–68

    Article  PubMed  CAS  Google Scholar 

  • Engelhardt H, Forchhammer K, Muller S, Goldie KN, Bock A (1992) Structure of selenocysteine synthase from Escherichia-coli and location of transfer-rna in the seryl transfer RNASec-enzyme complex. Mol Microbiol 6:3461–3467

    Article  PubMed  CAS  Google Scholar 

  • Fairweather-Tait SJ, Bao YP, Broadley MR, Collings R, Ford D, Hesketh JE, Hurst R (2011) Selenium in human health and disease. Antioxid Redox Signal 14:1337–1383

    Article  PubMed  CAS  Google Scholar 

  • Fajardo D, Schlautman B, Steffan S, Polashock J, Vorsa N, Zalapa J (2014) The American cranberry mitochondrial genome reveals the presence of selenocysteine (tRNA-Sec and SECIS) insertion machinery in land plants. Gene 536:336–343

    Article  PubMed  CAS  Google Scholar 

  • Fedacko J, Pella D, Fedackova P, Hanninen O, Tuomainen P, Jarcuska P, Lopuchovsky T, Jedlickova L, Merkovska L, Littarru GP (2013) Coenzyme Q(10) and selenium in statin-associated myopathy treatment. Can J Physiol Pharmacol 91:165–170

    Article  PubMed  CAS  Google Scholar 

  • Fischer N, Neumann P, Bock LV, Maracci C, Wang Z, Paleskava A, Konevega AL, Schroder GF, Grubmuller H., Ficner R et al (2016) The pathway to GTPase activation of elongation factor SelB on the ribosome. Nature 540:80

  • Fletcher JE, Copeland PR, Driscoll DM, Krol A (2001) The selenocysteine incorporation machinery: interactions between the SECIS RNA and the SECIS-binding protein SBP2. Rna-a Publ Rna Soc 7:1442–1453

    CAS  Google Scholar 

  • Forchhammer K, Bock A (1991) Selenocysteine synthase from Escherichia-coli—analysis of the reaction sequence. J Biol Chem 266:6324–6328

    PubMed  CAS  Google Scholar 

  • Forchhammer K, Leinfelder W, Bock A (1989) Identification of a novel translation factor necessary for the incorporation of selenocysteine into protein. Nature 342:453–456

    Article  PubMed  CAS  Google Scholar 

  • Fradejas-Villar N, Seeher S, Anderson CB, Doengi M, Carlson BA, Hatfield DL, Schweizer U, Howard MT (2017) The RNA-binding protein Secisbp2 differentially modulates UGA codon reassignment and RNA decay. Nucleic Acids Res 45:4094–4107

    Article  PubMed  CAS  Google Scholar 

  • Franke KW, Moxon AL (1937) The toxicity of orally ingested arsenic, selenium, tellurium, vanadium and molybdenum. J Pharmacol Exp Ther 61:89–102

    CAS  Google Scholar 

  • French RL, Gupta N, Copeland PR, Simonovic M (2014) Structural asymmetry of the terminal catalytic complex in selenocysteine synthesis. J Biol Chem 289:28783–28794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Frenkel FE, Chaley MB, Korotkov EV, Skryabin KG (2004) Evolution of tRNA-like sequences and genome variability. Gene 335:57–71

    Article  PubMed  CAS  Google Scholar 

  • Fuhrmeister J, Tews M, Kromer A, Moosmann B (2012) Prooxidative toxicity and selenoprotein suppression by cerivastatin in muscle cells. Toxicol Lett 215:219–227

    Article  PubMed  CAS  Google Scholar 

  • Furberg CD, Pitt B (2001) Withdrawal of cerivastatin from the world market. Curr Control Trials Cardiovasc Med 2:205–207

    Article  PubMed  PubMed Central  Google Scholar 

  • Ganichkin OM, Xu XM, Carlson BA, Mix H, Hatfield DL, Gladyshev VN, Wahl MC (2008) Structure and catalytic mechanism of eukaryotic selenocysteine synthase. J Biol Chem 283:5849–5865

    Article  PubMed  CAS  Google Scholar 

  • Ganichkin OM, Anedchenko EA, Wahl MC (2011) Crystal structure analysis reveals functional flexibility in the selenocysteine-specific tRNA from mouse. PLoS One 6:e20032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gladyshev VN, Kryukov GV (2001) Evolution of selenocysteine-containing proteins: significance of identification and functional characterization of selenoproteins. BioFactors 14:87–92

    Article  PubMed  CAS  Google Scholar 

  • Gossinger M, Lechner M, Brillante N, Weber C, Rossmanith W, Hartmann RK (2017) Protein-only RNase P function in Escherichia coli: viability, processing defects and differences between PRORP isoenzymes. Nucleic Acids Res 45:7441–7454

    Article  CAS  Google Scholar 

  • Gribling-Burrer AS, Leichter M, Wurth L, Huttin A, Schlotter F, Troffer-Charlier N, Cura V, Barkats M, Cavarelli J, Massenet S et al (2017) SECIS-binding protein 2 interacts with the SMN complex and the methylosome for selenoprotein mRNP assembly and translation. Nucleic Acids Res 45:5399–5413

    PubMed  PubMed Central  CAS  Google Scholar 

  • Grundner-Culemann E, Martin GW, Harney JW, Berry MJ (1999) Two distinct SECIS structures capable of directing selenocysteine incorporation in eukaryotes. Rna-a Publ Rna Soc 5:625–635

    Article  CAS  Google Scholar 

  • Guimaraes MJ, Peterson D, Vicari A, Cocks BG, Copeland NG, Gilbert DJ, Jenkins NA, Ferrick DA, Kastelein RA, Bazan JF et al (1996) Identification of a novel selD homolog from eukaryotes, bacteria, and archaea: is there an autoregulatory mechanism in selenocysteine metabolism? Proc Natl Acad Sci USA 93:15086–15091

    Article  PubMed  CAS  Google Scholar 

  • Hanauer SB (2006) Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis 12:S3–S9

    Article  PubMed  Google Scholar 

  • Hartlein M, Cusack S (1995) Structure, function and evolution of seryl-transfer-rna synthetases—implications for the evolution of aminoacyl-transfer-rna synthetases and the genetic-code. J Mol Evol 40:519–530

    Article  PubMed  CAS  Google Scholar 

  • Haruna K, Alkazemi MH, Liu YC, Soll D, Englert M (2014) Engineering the elongation factor Tu for efficient selenoprotein synthesis. Nucleic Acids Res 42:9976–9983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hatfield D, Diamond A, Dudock B (1982) Opal suppressor serine transfer-rnas from bovine liver form phosphoseryl-transfer rna. Proc Natl Acad Sci US Am-Biol Sci 79:6215–6219

    Article  CAS  Google Scholar 

  • Hatfield DL, Dudock BS, Eden FC (1983) Characterization and nucleotide-sequence of a chicken gene encoding an opal suppressor transfer-rna and its flanking dna segments. Proc Natl Acad Sci US Am-Biol Sci 80:4940–4944

    Article  CAS  Google Scholar 

  • Hatfield D, Choi IS, Mischke S, Owens LD (1992) Selenocysteyl-transfer rnas recognize uga in beta-vulgaris, a higher-plant, and in gliocladium-virens, a filamentous fungus. Biochem Biophys Res Commun 184:254–259

    Article  PubMed  CAS  Google Scholar 

  • Heider J, Bock A (1993) Selenium metabolism in microorganisms. Adv Microb Physiol 35(35):71–109

    Article  PubMed  CAS  Google Scholar 

  • Henkin TM (2002) Transcription termination control in bacteria. Signals, Switch, Regulons Cascades: Control Bact Gene Expr 61:169–181

    Google Scholar 

  • Hilgenfeld R, Bock A, Wilting R (1996) Structural model for the selenocysteine-specific elongation factor SelB. Biochimie 78:971–978

    Article  PubMed  CAS  Google Scholar 

  • Hiramoto K, Satoh H, Suzuki T, Moriguchi T, Pi J, Shimosegawa T, Yamamoto M (2014) Myeloid lineage-specific deletion of antioxidant system enhances tumor metastasis. Cancer Prev Res 7:835–844

    Article  CAS  Google Scholar 

  • Holman KM, Puppala AK, Lee JW, Lee H, Simonovic M (2017) Insights into substrate promiscuity of human seryl-tRNA synthetase. RNA 23:1685–1699

    Article  PubMed  CAS  Google Scholar 

  • Holtkamp W, Wintermeyer W, Rodnina MV (2014) Synchronous tRNA movements during translocation on the ribosome are orchestrated by elongation factor G and GTP hydrolysis. BioEssays 36:908–918

    Article  PubMed  CAS  Google Scholar 

  • Howard MT, Moyle MW, Aggarwal G, Carlson BA, Anderson CB (2007) A recoding element that stimulates decoding of UGA codons by Sec tRNA(Ser Sec). Rna-a Publ Rna Soc 13:912–920

    Article  CAS  Google Scholar 

  • Howard MT, Carlson BA, Anderson CB, Hatfield DL (2013) Translational redefinition of UGA codons is regulated by selenium availability. J Biol Chem 288:19401–19413

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang Z, Rose AH, Hoffmann PR (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16:705–743

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hubert N, Sturchler C, Westhof E, Carbon P, Krol A (1998) The 9/4 secondary structure of eukaryotic selenocysteine tRNA: more pieces of evidence. Rna-a Publ Rna Soc 4:1029–1033

    Article  CAS  Google Scholar 

  • Hudson TS, Carlson BA, Hoeneroff MJ, Young HA, Sordillo L, Muller WJ, Hatfield DL, Green JE (2012) Selenoproteins reduce susceptibility to DMBA-induced mammary carcinogenesis. Carcinogenesis 33:1225–1230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ilgen C, Kirk LL, Carbon J (1976) Isolation and characterization of large transfer ribonucleic-acid precursors from Escherichia-coli. J Biol Chem 251:922–929

    PubMed  CAS  Google Scholar 

  • Ishii TM, Kotlova N, Tapsoba F, Steinberg SV (2013) The long D-stem of the selenocysteine tRNA provides resilience at the expense of maximal function. J Biol Chem 288:13337–13344

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itoh Y, Chiba S, Sekine S-I, Yokoyama S (2009a) Crystal structure of human selenocysteine tRNA. Nucleic Acids Res 37:6259–6268

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itoh Y, Sekine SI, Matsumoto E, Akasaka R, Takemoto C, Shirouzu M, Yokoyama S (2009b) Structure of selenophosphate synthetase essential for selenium incorporation into proteins and RNAs. J Mol Biol 385:1456–1469

    Article  PubMed  CAS  Google Scholar 

  • Itoh Y, Broecker MJ, Sekine S-I, Hammond G, Suetsugu S, Soell D, Yokoyama S (2013a) Decameric SelA.tRNA(Sec) ring structure reveals mechanism of bacterial selenocysteine formation. Science 340:75–78

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itoh Y, Sekine S-I, Suetsugu S, Yokoyama S (2013b) Tertiary structure of bacterial selenocysteine tRNA. Nucleic Acids Res 41:6729–6738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itoh Y, Brocker MJ, Sekine S, Soll D, Yokoyama S (2014) Dimer-dimer interaction of the bacterial selenocysteine synthase SelA promotes functional active-site formation and catalytic specificity. J Mol Biol 426:1723–1735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itoh Y, Sekine S, Yokoyama S (2015) Crystal structure of the full-length bacterial selenocysteine-specific elongation factor SelB. Nucleic Acids Res 43:9028–9038

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Janas T, Janas T, Yarus M (2012) Human tRNA(Sec) associates with HeLa membranes, cell lipid liposomes, and synthetic lipid bilayers. Rna-a Publ Rna Soc 18:2260–2268

    Article  CAS  Google Scholar 

  • Jinksrobertson S, Gourse RL, Nomura M (1983) Expression of Ribosomal-RNA and transfer-RNA genes in Escherichia-coli—evidence for feedback-regulation by products of ribosomal-RNA operons. Cell 33:865–876

    Article  CAS  Google Scholar 

  • Kaiser JT, Gromadski K, Rother M, Engelhardt H, Rodnina MV, Wahl MC (2005) Structural and functional investigation of a putative archaeal selenocysteine synthase. Biochemistry 44:13315–13327

    Article  PubMed  CAS  Google Scholar 

  • Kasaikina MV, Turanov AA, Avanesov A, Schweizer U, Seeher S, Bronson RT, Novoselov SN, Carlson BA, Hatfield DL, Gladyshev VN (2013) Contrasting roles of dietary selenium and selenoproteins in chemically induced hepatocarcinogenesis. Carcinogenesis 34:1089–1095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kato N, Hoshino H, Harada F (1983) Minor serine transfer-rna containing anticodon NCA(C4-RNA) from human and mouse cells. Biochem Int 7:635–645

    PubMed  CAS  Google Scholar 

  • Kaushal N, Kudva AK, Patterson AD, Chiaro C, Kennett MJ, Desai D, Amin S, Carlson BA, Cantorna MT, Prabhu KS (2014) Crucial role of macrophage selenoproteins in experimental colitis. J Immunol 193:3683–3692

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kawatani Y, Suzuki T, Shimizu R, Kelly VP, Yamamoto M (2011) Nrf2 and selenoproteins are essential for maintaining oxidative homeostasis in erythrocytes and protecting against hemolytic anemia. Blood 117:986–996

    Article  PubMed  CAS  Google Scholar 

  • Kazantsev AV, Pace NR (2006) Bacterial RNase P: a new view of an ancient enzyme. Nat Rev Microbiol 4:729–740

    Article  PubMed  CAS  Google Scholar 

  • Kelly VP, Suzuki T, Nakajima O, Arai T, Tamai Y, Takahashi S, Nishimura S, Yamamoto M (2005) The distal sequence element of the selenocysteine tRNA gene is a tissue-dependent enhancer essential for mouse embryogenesis. Mol Cell Biol 25:3658–3669

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koehler A, Hurt E (2007) Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 8:761–773

    Article  CAS  Google Scholar 

  • Kossinova O, Malygin A, Krol A, Karpova G (2013) A novel insight into the mechanism of mammalian selenoprotein synthesis. Rna-a Publ Rna Soc 19:1147–1158

    Article  CAS  Google Scholar 

  • Kossinova O, Malygin A, Krol A, Karpova G (2014) The SBP2 protein central to selenoprotein synthesis contacts the human ribosome at expansion segment 7L of the 28S rRNA. RNA 20:1046–1056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kryukov GV, Gladyshev VN (2004) The prokaryotic selenoproteome. Embo Rep 5:538–543

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigo R, Gladyshev VN (2003) Characterization of mammalian selenoproteomes. Science 300:1439–1443

    Article  PubMed  CAS  Google Scholar 

  • Laalami S, Grentzmann G, Bremaud L, Cenatiempo Y (1996) Messenger RNA translation in prokaryotes: GTPase centers associated with translational factors. Biochimie 78:577–589

    Article  PubMed  CAS  Google Scholar 

  • Lacourciere GM, Stadtman TC (2001) Utilization of selenocysteine as a source of selenium for selenophosphate biosynthesis. BioFactors 14:69–74

    Article  PubMed  CAS  Google Scholar 

  • Lamichhane TN, Mattijssen S, Maraia RJ (2013) Human cells have a limited set of tRNA anticodon loop substrates of the tRNA isopentenyltransferase TRIT1 tumor suppressor. Mol Cell Biol 33:4900–4908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee BJ, Delapena P, Tobian JA, Zasloff M, Hatfield D (1987) Unique pathway of expression of an opal suppressor phosphoserine transfer-RNA. Proc Natl Acad Sci USA 84:6384–6388

    Article  PubMed  CAS  Google Scholar 

  • Lee BJ, Kang SG, Hatfield D (1989) Transcription of xenopus selenocysteine transfer rnaser (formerly designated opal suppressor phosphoserine transfer-RNA) gene is directed by multiple 5′-extragenic regulatory elements. J Biol Chem 264:9696–9702

    PubMed  CAS  Google Scholar 

  • Lee BJ, Rajagopalan M, Kim YS, You KH, Jacobson KB, Hatfield D (1990) Selenocysteine transfer RNA Ser Sec gene is ubiquitous within the animal kingdom. Mol Cell Biol 10:1940–1949

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leibundgut M, Frick C, Thanbichler M, Bock A, Ban N (2005) Selenocysteine tRNA-specific elongation factor SelB is a structural chimaera of elongation and initiation factors. EMBO J 24:11–22

    Article  PubMed  CAS  Google Scholar 

  • Leinfelder W, Forchhammer K, Zinoni F, Sawers G, Mandrandberthelot MA, Bock A (1988a) Escherichia-coli genes whose products are involved in selenium metabolism. J Bacteriol 170:540–546

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leinfelder W, Zehelein E, Mandrandberthelot MA, Bock A (1988b) Gene for a novel transfer-RNA species that accepts l-serine and cotranslationally inserts selenocysteine. Nature 331:723–725

    Article  PubMed  CAS  Google Scholar 

  • Lin HC, Ho SC, Chen YY, Khoo KH, Hsu PH, Yen HCS (2015) CRL2 aids elimination of truncated selenoproteins produced by failed UGA/Sec decoding. Science 349:91–95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu YC, Nakamura A, Nakazawa Y, Asano N, Ford KA, Hohn MJ, Tanaka I, Yao M, Soll D (2014) Ancient translation factor is essential for tRNA-dependent cysteine biosynthesis in methanogenic archaea. Proc Natl Acad Sci USA 111:10520–10525

    Article  PubMed  CAS  Google Scholar 

  • Lobanov AV, Delgado C, Rahlfs S, Novoselov SV, Kryukov GV, Gromer S, Hatfield DL, Becker K, Gladyshev VN (2006) The plasmodium selenoproteome. Nucleic Acids Res 34:496–505

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lobanov AV, Hatfield DL, Gladyshev VN (2008) Selenoproteinless animals: selenophosphate synthetase SPS1 functions in a pathway unrelated to selenocysteine biosynthesis. Protein Sci 17:176–182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Low SC, Grundner-Culemann E, Harney JW, Berry MJ (2000) SECIS-SBP2 interactions dictate selenocysteine incorporation efficiency and selenoprotein hierarchy. EMBO J 19:6882–6890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu J, Holmgren A (2009) Selenoproteins. J Biol Chem 284:723–727

    Article  PubMed  CAS  Google Scholar 

  • Maciel-Dominguez A, Swan D, Ford D, Hesketh J (2013) Selenium alters miRNA profile in an intestinal cell line: evidence that miR-185 regulates expression of GPX2 and SEPSH2. Mol Nutr Food Res 57:2195–2205

    Article  PubMed  CAS  Google Scholar 

  • Macino G, Coruzzi G, Nobrega FG, Li M, Tzagoloff A (1979) Use of the uga terminator as a tryptophan codon in yeast mitochondria. Proc Natl Acad Sci USA 76:3784–3785

    Article  PubMed  CAS  Google Scholar 

  • Mahdi Y, Xu XM, Carlson BA, Fradejas N, Gunter P, Braun D, Southon E, Tessarollo L, Hatfield DL, Schweizer U (2015) Expression of selenoproteins is maintained in mice carrying mutations in SECp43, the tRNA selenocysteine 1 associated protein (Trnau1ap). PLoS One 10:e0127349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mangiapane E, Pessione A, Pessione E (2014) Selenium and selenoproteins: an overview on different biological systems. Curr Protein Pept Sci 15:598–607

    Article  PubMed  CAS  Google Scholar 

  • Mansell JB, Guevremont D, Poole ES, Tate WP (2001) A dynamic competition between release factor 2 and the tRNA(Sec) decoding UGA at the recoding site of Escherichia coli formate dehydrogenase H. EMBO J 20:7284–7293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manzine LR, Serrao VHB, Lima L, de Souza MM, Bettini J, Portugal RV, van Heel M, Thiemann OH (2013) Assembly stoichiometry of bacterial selenocysteine synthase and SelC (tRNA(sec)). FEBS Lett 587:906–911

    Article  PubMed  CAS  Google Scholar 

  • Maraia RJ, Iben JR (2014) Different types of secondary information in the genetic code. Rna-a Publ Rna Soc 20:977–984

    Article  CAS  Google Scholar 

  • Mariotti M, Lobanov AV, Manta B, Santesmasses D, Bofill A, Guigo R, Gabaldon T, Gladyshev VN (2016) Lokiarchaeota marks the transition between the archaeal and eukaryotic selenocysteine encoding systems. Mol Biol Evol 33:2441–2453

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mehta A, Rebsch CM, Kinzy SA, Fletcher JE, Copeland PR (2004) Efficiency of mammalian selenocysteine incorporation. J Biol Chem 279:37852–37859

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meyer F, Schmidt HJ, Plumper E, Hasilik A, Mersmann G, Meyer HE, Engstrom A, Heckmann K (1991) UGA is translated as cysteine in pheromone-3 of euplotes-octocarinatus. Proc Natl Acad Sci USA 88:3758–3761

    Article  PubMed  CAS  Google Scholar 

  • Mihara H, Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60:12–23

    Article  PubMed  CAS  Google Scholar 

  • Mihara H, Kurihara T, Yoshimura T, Soda K, Esaki N (1997) Cysteine sulfinate desulfinase, a NIFS-like protein of Escherichia coli with selenocysteine lyase and cysteine desulfurase activities—gene cloning, purification, and characterization of a novel pyridoxal enzyme. J Biol Chem 272:22417–22424

    Article  PubMed  CAS  Google Scholar 

  • Mihara H, Maeda M, Fujii T, Kurihara T, Hata Y, Esaki N (1999) A nifS-like gene, csdB, encodes an Escherichia coli counterpart of mammalian selenocysteine lyase—gene cloning, purification, characterization and preliminary X-ray crystallographic studies. J Biol Chem 274:14768–14772

    Article  PubMed  CAS  Google Scholar 

  • Miniard AC, Middleton LM, Budiman ME, Gerber CA, Driscoll DM (2010) Nucleolin binds to a subset of selenoprotein mRNAs and regulates their expression. Nucleic Acids Res 38:4807–4820

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell A, Bale AE, Lee BJ, Hatfield D, Harley H, Rundle SA, Fan YS, Fukushima Y, Shows TB, McBride OW (1992) Regional localization of the selenocysteine transfer-RNA gene (TRSP) on human chromosome-19. Cytogenet Cell Genet 61:117–120

    Article  PubMed  CAS  Google Scholar 

  • Mitra K, Frank J (2006) Ribosome dynamics: insights from atomic structure modeling into cryo-electron microscopy maps. Annu Rev Biophys Biomol Struct 35:299–317

    Article  PubMed  CAS  Google Scholar 

  • Moosmann B, Behl C (2004a) Selenoprotein synthesis and side-effects of statins. Lancet 363:892–894

    Article  PubMed  CAS  Google Scholar 

  • Moosmann B, Behl C (2004b) Selenoproteins, cholesterol-lowering drugs, and the consequences—revisiting of the mevalonate pathway. Trends Cardiovasc Med 14:273–281

    Article  PubMed  CAS  Google Scholar 

  • Mosshammer D, Schaeffeler E, Schwab M, Moerike K (2014) Mechanisms and assessment of statin-related muscular adverse effects. Br J Clin Pharmacol 78:454–466

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moustafa ME, Carlson BA, Anver MR, Bobe G, Zhong N, Ward JM, Perella CM, Hoffmann VJ, Rogers K, Combs GF Jr et al. (2013) Selenium and selenoprotein deficiencies induce widespread pyogranuloma formation in mice, while high levels of dietary selenium decrease liver tumor size driven by TGF alpha. PLoS One 8:e57389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moxon AL, Anderson HD, Painter EP (1938) The toxicity of some organic selenium compounds. J Pharmacol Exp Ther 63:357–368

    CAS  Google Scholar 

  • Mukai T, Englert M, Tripp HJ, Miller C, Ivanova NN, Rubin EM, Kyrpides NC, Soll D (2016) Facile recoding of selenocysteine in nature. Angewandte Chemie-Int Edn 55:5337–5341

    Article  CAS  Google Scholar 

  • Myslinski E, Krol A, Carbon P (1992) Optimal transfer RNA(Ser)Sec gene activity requires an upstream SPH motif. Nucleic Acids Res 20:203–209

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Narayan V, Ravindra KC, Liao C, Kaushal N, Carlson BA, Prabhu KS (2015) Epigenetic regulation of inflammatory gene expression in macrophages by selenium. J Nutr Biochem 26:138–145

    Article  PubMed  CAS  Google Scholar 

  • Nelson SM, Shay AE, James JL, Carlson BA, Urban JF, Prabhu KS (2016) Selenoprotein expression in macrophages is critical for optimal clearance of parasitic helminth nippostrongylus brasiliensis. J Biol Chem 291:2787–2798

    Article  PubMed  CAS  Google Scholar 

  • Noinaj N, Wattanasak R, Lee D-Y, Wally JL, Piszczek G, Chock PB, Stadtman TC, Buchanan SK (2012) Structural insights into the catalytic mechanism of escherichia coli selenophosphate synthetase. J Bacteriol 194:499–508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Novoselov SV, Rao M, Onoshko NV, Zhi HJ, Kryukov GV, Xiang YB, Weeks DP, Hatfield DL, Gladyshev VN (2002) Selenoproteins and selenocysteine insertion system in the model plant cell system, Chlamydomonas reinhardtii. EMBO J 21:3681–3693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ogasawara Y, Lacourciere GM, Ishii K, Stadtman TC (2005) Characterization of potential selenium-binding proteins in the selenophosphate synthetase system. Proc Natl Acad Sci USA 102:1012–1016

    Article  PubMed  CAS  Google Scholar 

  • Ohama T, Choi IS, Hatfield DL, Johnson KR (1994) Mouse selenocysteine TRNA(Ser Sec) gene (TRSP) and its localization on chromosome-7. Genomics 19:595–596

    Article  PubMed  CAS  Google Scholar 

  • Ose T, Soler N, Rasubala L, Kuroki K, Kohda D, Fourmy D, Yoshizawa S, Maenaka K (2007) Structural basis for dynamic interdomain movement and RNA recognition of the selenocysteine-specific elongation factor SelB. Structure 15:577–586

    Article  PubMed  CAS  Google Scholar 

  • Oudouhou F, Casu B, Puemi ASD, Sygusch J, Baron C (2017) Analysis of novel interactions between components of the selenocysteine biosynthesis pathway, SEPHS1, SEPHS2, SEPSECS, and SECp43. Biochemistry 56:2261–2270

    Article  PubMed  CAS  Google Scholar 

  • Padilla-Mejia NE, Florencio-Martinez LE, Moreno-Campos R, Vizuet-de-Rueda JC, Cevallos AM, Hernandez-Rivas R, Manning-Cela R, Martinez-Calvilloa S (2015) The selenocysteine tRNA gene in leishmania major is transcribed by both RNA polymerase II and RNA polymerase III. Eukaryot Cell 14:216–227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paleskava A, Konevega AL, Rodnina MV (2010) Thermodynamic and kinetic framework of selenocysteyl-tRNA(Sec) recognition by elongation factor SelB. J Biol Chem 285

  • Palioura S, Sherrer RL, Steitz TA, Soell D, Simonovic M (2009) The human SepSecS-tRNA(Sec) complex reveals the mechanism of selenocysteine formation. Science 325:321–325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paule MR, White RJ (2000) Transcription by RNA polymerases I and III. Nucleic Acids Res 28:1283–1298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pei J, Fu W, Yang L, Zhang Z, Liu Y (2013) Oxidative stress is involved in the pathogenesis of keshan disease (an endemic dilated cardiomyopathy) in China. Oxidative Medicine and Cellular Longevity. 2013:474203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao M, Carlson BA, Novoselov SV, Weeks DP, Gladyshev VN, Hatfield DL (2003) Chlamydomonas reinhardtii selenocysteine tRNA (Ser Sec). Rna-a Publ Rna Soc 9:923–930

    Article  CAS  Google Scholar 

  • Reilly C (1996) Selenium in food and health. Blackie Academic & Professional, New York

    Book  Google Scholar 

  • Reiner Z (2014) Resistance and intolerance to statins. Nutr Metab Cardiovasc Dis 24:1057–1066

    Article  PubMed  CAS  Google Scholar 

  • Rother M, Wilting R, Commans S, Bock A (2000) Identification and characterisation of the selenocysteine-specific translation factor SelB from the archaeon Methanococcus jannaschii. J Mol Biol 299:351–358

    Article  PubMed  CAS  Google Scholar 

  • Rother M, Resch A, Wilting R, Bock A (2001) Selenoprotein synthesis in archaea. BioFactors 14:75–83

    Article  PubMed  CAS  Google Scholar 

  • Santesmasses D, Mariotti M, Guigo R (2017) Computational identification of the selenocysteine tRNA (tRNA(Sec)) in genomes. PLoS Comput Biol 13:e1005383

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sawers G, Heider J, Zehelein E, Bock A (1991) Expression and operon structure of the Sel genes of Escherichia-coli and identification of a 3rd selenium-containing formate dehydrogenase isoenzyme. J Bacteriol 173:4983–4993

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schimmel PR, Soll D (1979) Aminoacyl transfer RNA-synthetases—general features and recognition of transfer-RNAS. Annu Rev Biochem 48:601–648

    Article  PubMed  CAS  Google Scholar 

  • Schmeing TM, Voorhees RM, Kelley AC, Ramakrishnan V (2011) How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nat Struct Mol Biol 18:432–461

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schurer H, Schiffer S, Marchfelder A, Morl M (2001) This is the end: processing, editing and repair at the tRNA 3′-terminus. Biol Chem 382:1147–1156

    PubMed  CAS  Google Scholar 

  • Schuster C, Myslinski E, Krol A, Carbon P (1995) Staf, a novel zinc-finger protein that activates the rna-polymerase-III promoter of the selenocysteine transfer-RNA gene. EMBO J 14:3777–3787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sherrer RL, Ho JML, Soll D (2008) Divergence of selenocysteine tRNA recognition by archaeal and eukaryotic O-phosphoseryl-tRNA(Sec) kinase. Nucleic Acids Res 36:1871–1880

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sherrer RL, Araiso Y, Aldag C, Ishitani R, Ho JML, Soell D, Nureki O (2011) C-terminal domain of archaeal O-phosphoseryl-tRNA kinase displays large-scale motion to bind the 7-bp D-stem of archaeal tRNA(Sec). Nucleic Acids Res 39:1034–1041

    Article  PubMed  CAS  Google Scholar 

  • Shrimali RK, Lobanov AV, Xu XM, Rao M, Carlson BA, Mahadeo DC, Parent CA, Gladyshev VN, Hatfield DL (2005) Selenocysteine tRNA identification in the model organisms Dictyostelium discoideum and Tetrahymena thermophila. Biochem Biophys Res Commun 329:147–151

    Article  PubMed  CAS  Google Scholar 

  • Siebenlist U, Simpson RB, Gilbert W (1980) Escherichia-coli RNA-polymerase interacts homologously with 2 different promoters. Cell 20:269–281

    Article  PubMed  CAS  Google Scholar 

  • Silva AL, Romao L (2009) The mammalian nonsense-mediated mRNA decay pathway: to decay or not to decay! Which players make the decision? FEBS Lett 583:499–505

    Article  PubMed  CAS  Google Scholar 

  • Silva IR, Serrao VHB, Manzine LR, Faim LM, da Silva MTA, Makki R, Saidemberg DM, Cornelio ML, Palma MS, Thiemann OH (2015) Formation of a ternary complex for selenocysteine biosynthesis in bacteria. J Biol Chem 290:29178–29188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soler N, Fourmy D, Yoshizawa S (2007) Structural insight into a molecular switch in tandem winged-helix motifs from elongation factor SelB. J Mol Biol 370:728–741

    Article  PubMed  CAS  Google Scholar 

  • Soll D, RajBhandary UL (2006) The genetic code—thawing the ‘frozen accident’. J Biosci 31:459–463

    Article  PubMed  CAS  Google Scholar 

  • Squires JE, Berry MJ (2008) Eukaryotic selenoprotein synthesis: mechanistic insight incorporating new factors and new functions for old factors. IUBMB Life 60:232–235

    Article  PubMed  CAS  Google Scholar 

  • Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65:83–100

    Article  PubMed  CAS  Google Scholar 

  • Stock T, Rother M (2009) Selenoproteins in archaea and gram-positive bacteria. Biochimica Et Biophysica Acta-Gen Subj 1790:1520–1532

    Article  CAS  Google Scholar 

  • Stock T, Selzer M, Connery S, Seyhan D, Resch A, Rother M (2011) Disruption and complementation of the selenocysteine biosynthesis pathway reveals a hierarchy of selenoprotein gene expression in the archaeon Methanococcus maripaludis. Mol Microbiol 82:734–747

    Article  PubMed  CAS  Google Scholar 

  • Sturchler C, Westhof E, Carbon P, Krol A (1993) Unique secondary and tertiary structural features of the eukaryotic selenocysteine transfer RNA(Sec). Nucleic Acids Res 21:1073–1079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sturchler C, Lescure A, Keith G, Carbon P, Krol A (1994) Base modification pattern at the wobble position of xenopus selenocysteine TRNA(Sec). Nucleic Acids Res 22:1354–1358

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su D, Li YH, Gladyshev VN (2005) Selenocysteine insertion directed by the 3′-UTR SECIS element in Escherichia coli. Nucleic Acids Res 33:2486–2492

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takeuchi A, Schmitt D, Chapple C, Babaylova E, Karpova G, Guigo R, Krol A, Allmang C (2009) A short motif in drosophila SECIS binding protein 2 provides differential binding affinity to SECIS RNA hairpins. Nucleic Acids Res 37:2126–2141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tamura T, Yamamoto S, Takahata M, Sakaguchi H, Tanaka H, Stadtman TC, Inagaki K (2004) Selenophosphate synthetase genes from lung adenocarcinoma cells: sps1 for recycling l-selenocysteine and Sps2 for selenite assimilation. Proc Natl Acad Sci USA 101:16162–16167

    Article  PubMed  CAS  Google Scholar 

  • Taskov K, Chapple C, Kryukov GV, Castellano S, Lobanov AV, Korotkov KV, Guigo R, Gladyshev VN (2005) Nematode selenoproteome: the use of the selenocysteine insertion system to decode one codon in an animal genome? Nucleic Acids Res 33:2227–2238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thanbichler M, Bock A (2002) The function of SECIS RNA in translational control of gene expression in Escherichia coli. EMBO J 21:6925–6934

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tormay P, Sawers A, Bock A (1996) Role of stoichiometry between mRNA, translation factor SeIB and selenocysteyl-tRNA in selenoprotein synthesis. Mol Microbiol 21:1253–1259

    Article  PubMed  CAS  Google Scholar 

  • Vinceti M, Dennert G, Crespi CM, Zwahlen M, Brinkman M, Zeegers MPA, Horneber M, D’Amico R, Del Giovane C (2014) Selenium for preventing cancer. Cochrane Database Syst Rev 3:CD005195

    PubMed Central  Google Scholar 

  • Wang KT, Wang J, Li LF, Su XD (2009) Crystal structures of catalytic intermediates of human selenophosphate synthetase 1. J Mol Biol 390:747–759

    Article  PubMed  CAS  Google Scholar 

  • Wang CY, Guo Y, Tian QN, Jia Q, Gao YZ, Zhang QF, Zhou C, Xie W (2015) SerRS-tRNA(Sec) complex structures reveal mechanism of the first step in selenocysteine biosynthesis. Nucleic Acids Res 43:10534–10545

    PubMed  PubMed Central  CAS  Google Scholar 

  • Warner GJ, Berry MJ, Moustafa ME, Carlson BA, Hatfield DL, Faust JR (2000) Inhibition of selenoprotein synthesis by selenocysteine tRNA(Ser Sec) lacking isopentenyladenosine. J Biol Chem 275:28110–28119

    PubMed  CAS  Google Scholar 

  • Weingarten-Gabbay S, Segal E (2014) The grammar of transcriptional regulation. Hum Genet 133:701–711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wende S, Bonin S, Gotze O, Betat H, Morl M (2015) The identity of the discriminator base has an impact on CCA addition. Nucleic Acids Res 43:5617–5629

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Werner F (2013) Molecular mechanisms of transcription elongation in archaea. Chem Rev 113:8331–8349

    Article  PubMed  CAS  Google Scholar 

  • Wirth EK, Bharathi BS, Hatfield D, Conrad M, Brielmeier M, Schweizer U (2014) Cerebellar hypoplasia in mice lacking selenoprotein biosynthesis in neurons. Biol Trace Elem Res 158:203–210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Witting R, Schorling S, Persson BC, Bock A (1997) Selenoprotein synthesis in archaea: identification of an mRNA element of Methanococcus jannaschii probably directing selenocystein insertion. J Mol Biol 266:637–641

    Article  Google Scholar 

  • Wittwer AJ, Tsai L, Ching WM, Stadtman TC (1984) Identification and synthesis of a naturally-occurring selenonucleoside in bacterial transfer-RNAS-5-(methylamino)methyl-2-selenouridine. Biochemistry 23:4650–4655

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Olsen GJ, Ibba M, Soll D (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev 64:202

  • Wohlgemuth I, Pohl C, Mittelstaet J, Konevega AL, Rodnina MV (2011) Evolutionary optimization of speed and accuracy of decoding on the ribosome. Philos Trans R Soc B-Biol Sci 366:2979–2986

    Article  CAS  Google Scholar 

  • Wu R, Shen QC, Newburger PE (2000) Recognition and binding of the human selenocysteine insertion sequence by nucleolin. J Cell Biochem 77:507–516

    Article  PubMed  CAS  Google Scholar 

  • Xu XM, Mix H, Carlson BA, Grabowski PJ, Gladyshev VN, Berry MJ, Hatfield DL (2005) Evidence for direct roles of two additional factors, SECp43 and soluble liver antigen, in the selenoprotein synthesis machinery. J Biol Chem 280:41568–41575

    Article  PubMed  CAS  Google Scholar 

  • Xu X-M, Carlson BA, Mix H, Zhang Y, Saira K, Glass RS, Berry MJ, Gladyshev VN, Hatfield DL (2007a) Biosynthesis of selenocysteine on its tRNA in eukaryotes. PLoS Biol 5:96–105

    Article  CAS  Google Scholar 

  • Xu XM, Carlson BA, Irons R, Mix H, Zhong NX, Gladyshev VN, Hatfield DL (2007b) Selenophosphate synthetase 2 is essential for selenoprotein biosynthesis. Biochem J 404:115–120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu JQ, Croitoru V, Rutishauser D, Cheng Q, Arner ESJ (2013) Wobble decoding by the Escherichia coli selenocysteine insertion machinery. Nucleic Acids Res 41:9800–9811

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu F, Jerlstrom-Hultqvist J, Einarsson E, Ástvaldsson A, Svard SG, Andersson JO (2014) The genome of spironucleus salmonicida highlights a fish pathogen adapted to fluctuating environments. PLoS Genet 10(2):e1004053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yagishita Y, Uruno A, Fukutomi T, Saito R, Saigusa D, Pi JB, Fukamizu A, Sugiyama F, Takahashi S, Yamamoto M (2017) Nrf2 improves leptin and insulin resistance provoked by hypothalamic oxidative stress. Cell Rep 18:2030–2044

    Article  PubMed  CAS  Google Scholar 

  • Yarham JW, Lamichhane TN, Pyle A, Mattijssen S, Baruffini E, Bruni F, Donnini C, Vassilev A, He LP, Blakely EL et al (2014) Defective i(6)A37 Modification of mitochondrial and cytosolic tRNAs results from pathogenic mutations in TRIT1 and its substrate tRNA. PLoS Genetics 10

  • Yoshizawa S, Boeck A (2009) The many levels of control on bacterial selenoprotein synthesis. Biochimica Et Biophysica Acta-General Subjects 1790:1404–1414

    Article  CAS  Google Scholar 

  • Yuan J, Palioura S, Salazar JC, Su D, O’Donoghue P, Hohn MJ, Cardoso AM, Whitman WB, Soll D (2006) RNA-dependent conversion of phosphoserine forms selenocysteine in eukaryotes and archaea. Proc Natl Acad Sci USA 103:18923–18927

    Article  PubMed  CAS  Google Scholar 

  • Yuan J, O’Donoghue P, Ambrogelly A, Gundllapalli S, Sherrer RL, Palioura S, Simonovic M, Soll D (2010) Distinct genetic code expansion strategies for selenocysteine and pyrrolysine are reflected in different aminoacyl-tRNA formation systems. FEBS Lett 584:342–349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang G, Lukoszek R, Mueller-Roeber B, Ignatova Z (2011) Different sequence signatures in the upstream regions of plant and animal tRNA genes shape distinct modes of regulation. Nucleic Acids Res 39:3331–3339

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Zhang J, Xiao J (2014) Selenoproteins and selenium status in bone physiology and pathology. Biochimica Et Biophysica Acta-General Subjects 1840:3246–3256

    Article  CAS  Google Scholar 

  • Zhou X, Park SI, Moustafa ME, Carlson BA, Crain PF, Diamond AM, Hatfield DL, Lee BJ (1999) Selenium metabolism in drosophila—characterization of the selenocysteine tRNA population. J Biol Chem 274:18729–18734

    Article  PubMed  CAS  Google Scholar 

  • Zupanic A, Meplan C, Huguenin GVB, Hesketh JE, Shanley DP (2016) Modeling and gene knockdown to assess the contribution of nonsense-mediated decay, premature termination, and selenocysteine insertion to the selenoprotein hierarchy. RNA 22:1076–1084

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This work was supported by the research grants from FAPESP 2013/17791-0 and CNPq 420226/2016-8 to OHT. Research fellowships from FAPESP to MTAS—2011/24017-4; IRS—2010/04429-3; VHBS—2012/23730-1; JFS—2016/20977-7; CNPq AFF—134013/2015-8; VHBS—232251/2014-2 and CAPES. Louis Perry Jones Postdoctoral Fellow (HMS, USA) also supported VHBS.

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Correspondence to Otavio Henrique Thiemann.

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Serrão, V.H.B., Silva, I.R., da Silva, M.T.A. et al. The unique tRNASec and its role in selenocysteine biosynthesis. Amino Acids 50, 1145–1167 (2018). https://doi.org/10.1007/s00726-018-2595-6

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