Archaeal 3′-phosphate RNA splicing ligase characterization identifies the missing component in tRNA maturation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 4, 2011, Pages 1290-1295

  Englert, Markus ^a   Sheppard, Kelly ^a,c   Aslanian, Aaron ^b   Yates III, John R ^b   Söll, Dieter ^a  

^a YALE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c SKIDMORE COLLEGE   (United States)

Author keywords

Ligation; RNA processing; tRNA biosynthesis

Indexed keywords

BACTERIAL PROTEIN; LIGASE; PHOSPHATE; PROTEIN RTCB; TRANSFER RNA; UNCLASSIFIED DRUG; ZINC; ARCHAEAL PROTEIN; ARCHAEAL RNA; RNA LIGASE; RNA PRECURSOR; RTCB PROTEIN, METHANOPYRUS KANDLERI;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL MUTATION; CATALYSIS; CRYSTAL STRUCTURE; FUNGUS; METHANOPYRUS KANDLERI; NONHUMAN; PLANT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; PYROBACULUM AEROPHILUM; PYROCOCCUS HORIKOSHII; RNA SPLICING; STRUCTURAL GENOMICS; BINDING SITE; BIOCATALYSIS; CLASSIFICATION; ENZYMOLOGY; EURYARCHAEOTA; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE HOMOLOGY;

ANIMALIA; ARCHAEA; EUKARYOTA; FUNGI; METHANOPYRUS KANDLERI; PYROBACULUM AEROPHILUM; PYROCOCCUS HORIKOSHII;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; BASE SEQUENCE; BINDING SITES; BIOCATALYSIS; EURYARCHAEOTA; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHATES; PHYLOGENY; PYROCOCCUS HORIKOSHII; RNA LIGASE (ATP); RNA PRECURSORS; RNA SPLICING; RNA, ARCHAEAL; RNA, TRANSFER; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

EID: 79952142391     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1018307108     Document Type: Article

References (39)

1. Abelson J, Trotta CR, Li H (1998) tRNA splicing. J Biol Chem 273:12685-12688.
2. Peebles CL, Gegenheimer P, Abelson J (1983) Precise excision of intervening sequences from precursor tRNAs by a membrane-associated yeast endonuclease. Cell 32:525-536.
3. Mori T, et al. (2010) Dual functions of yeast tRNA ligase in the unfolded protein response: Unconventional cytoplasmic splicing of HAC1 pre-mRNA is not sufficient to release translational attenuation. Mol Biol Cell 21:3722-3734.
4. Schwer B, Sawaya R, Ho CK, Shuman S (2004) Portability and fidelity of RNA-repair systems. Proc Natl Acad Sci USA 101:2788-2793.
5. Englert M, Beier H (2005) Plant tRNA ligases are multifunctional enzymes that have diverged in sequence and substrate specificity from RNA ligases of other phylogenetic origins. Nucleic Acids Res 33:388-399.
6. Wang LK, Schwer B, Englert M, Beier H, Shuman S (2006) Structure-function analysis of the kinase-CPD domain of yeast tRNA ligase (Trl1) and requirements for complementation of tRNA splicing by a plant Trl1 homolog. Nucleic Acids Res 34:517-527.
7. Filipowicz W, Shatkin AJ (1983) Origin of splice junction phosphate in tRNAs processed by HeLa cell extract. Cell 32:547-557.
8. Perkins KK, Furneaux H, Hurwitz J (1985) Isolation and characterization of an RNA ligase from HeLa cells. Proc Natl Acad Sci USA 82:684-688.
9. Gomes I, Gupta R (1997) RNA splicing ligase activity in the archaeon Haloferax volcanii. Biochem Biophys Res Commun 237:588-594.
10. Kjems J, Garrett RA (1988) Novel splicing mechanism for the ribosomal RNA intron in the archaebacterium Desulfurococcus mobilis. Cell 54:693-703.
11. Zofallova L, Guo Y, Gupta R (2000) Junction phosphate is derived from the precursor in the tRNA spliced by the archaeon Haloferax volcanii cell extract. RNA 6:1019-1030.
12. Goyal K, Mande SC (2008) Exploiting 3D structural templates for detection of metalbinding sites in protein structures. Proteins 70:1206-1218.
13. Sauerwald A, et al. (2005) RNA-dependent cysteine biosynthesis in archaea. Science 307:1969-1972.
14. Okada C, Maegawa Y, Yao M, Tanaka I (2006) Crystal structure of an RtcB homolog protein (PH1602-extein protein) from Pyrococcus horikoshii reveals a novel fold. Proteins 63:1119-1122.
15. Kanai A, et al. (2009) Characterization of a heat-stable enzyme possessing GTP-dependent RNA ligase activity from a hyperthermophilic archaeon, Pyrococcus furiosus. RNA 15:420-431.
16. Torchia C, Takagi Y, Ho CK (2008) Archaeal RNA ligase is a homodimeric protein that catalyzes intramolecular ligation of single-stranded RNA and DNA. Nucleic Acids Res 36:6218-6227.
17. Genschik P, Drabikowski K, Filipowicz W (1998) Characterization of the Escherichia coli RNA 3′-terminal phosphate cyclase and its sigma54-regulated operon. J Biol Chem 273:25516-25526.
18. Reinhold-Hurek B, Shub DA (1992) Self-splicing introns in tRNA genes of widely divergent bacteria. Nature 357:173-176.
19. Genschik P, Billy E, Swianiewicz M, Filipowicz W (1997) The human RNA 3′-terminal phosphate cyclase is a member of a new family of proteins conserved in Eucarya, Bacteria and Archaea. EMBO J 16:2955-2967.
20. Tanaka N, Shuman S (2009) Structure-activity relationships in human RNA 3′-phosphate cyclase. RNA 15:1865-1874.
21. Tanaka N, Smith P, Shuman S (2010) Structure of the RNA 3′-phosphate cyclaseadenylate intermediate illuminates nucleotide specificity and covalent nucleotidyl transfer. Structure 18:449-457.
22. Blattner FR, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462.
23. Phizicky EM, Consaul SA, Nehrke KW, Abelson J (1992) Yeast tRNA ligase mutants are nonviable and accumulate tRNA splicing intermediates. J Biol Chem 267:4577-4582.
24. Wang LK, Schwer B, Shuman S (2006) Structure-guided mutational analysis of T4 RNA ligase 1. RNA 12:2126-2134.
25. Zillmann M, Gorovsky MA, Phizicky EM (1991) Conserved mechanism of tRNA splicing in eukaryotes. Mol Cell Biol 11:5410-5416.
26. Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin transports RNA: Isolation and characterization of an RNA-transporting granule. Neuron 43:513-525.
27. Trowitzsch S (2008) Functional and structural investigation of spliceosomal snRNPs. PhD thesis (Georg-August-Universität, Göttingen, Germany).
28. Choudhary C, et al. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834-840.
29. Molina H, Horn DM, Tang N, Mathivanan S, Pandey A (2007) Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc Natl Acad Sci USA 104:2199-2204.
30. Kouzuma Y, et al. (2003) Reconstitution of archaeal ribonuclease P from RNA and four protein components. Biochem Biophys Res Commun 306:666-673.
31. Kjems J, Jensen J, Olesen T, Garrett RA (1989) Comparison of transfer RNA and ribosomal RNA intron splicing in the extreme thermophile and archaebacterium Desulfurococcus mobilis. Can J Microbiol 35:210-214.
32. Kjems J, Garrett RA (1991) Ribosomal RNA introns in archaea and evidence for RNA conformational changes associated with splicing. Proc Natl Acad Sci USA 88:439-443.
33. Watanabe Y, et al. (2002) Introns in protein-coding genes in Archaea. FEBS Lett 510:27-30.
34. Yokobori S, et al. (2009) Gain and loss of an intron in a protein-coding gene in Archaea: The case of an archaeal RNA pseudouridine synthase gene. BMC Evol Biol 9:198.
35. Laska S, Kletzin A (2000) Improved purification of the membrane-bound hydrogenasesulfur- reductase complex from thermophilic archaea using epsilon-aminocaproic acid-containing chromatography buffers. J Chromatogr B 737:151-160.
36. Gln formation. Nucleic Acids Res 38:7286-7297.
37. Heinemann IU, et al. (2009) The appearance of pyrrolysine in tRNAHis guanylyltransferase by neutral evolution. Proc Natl Acad Sci USA 106:21103-21108.
38. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704.
39. Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45:667-671.