The structure of an archaeal homodimeric ligase which has RNA circularization activity

Protein Science

Volumn 17, Issue 8, 2008, Pages 1336-1345

  Brooks, Mark Adrian ^a,b   Meslet Cladiére, Laurence ^a,b   Graille, Marc ^a   Kuhn, Joëlle ^a   Blondeau, Karine ^a   Myllykallio, Hannu ^a   Van Tilbeurgh, Herman ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

Gene expression; Ligase; Nucleotidyl transferase; Pyrococcus abyssi; RNA, crystallization; X ray crystallography

Indexed keywords

ADENOSINE TRIPHOSPHATE; NUCLEOTIDYLTRANSFERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RNA LIGASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; CRYSTAL STRUCTURE; DIMERIZATION; GENE EXPRESSION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PYROCOCCUS ABYSSI; RNA CONFORMATION; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; BACTERIOPHAGE T4; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA LIGASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PYROCOCCUS ABYSSI; RNA LIGASE (ATP); SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

ARCHAEA; PYROCOCCUS ABYSSI;

EID: 48249105842     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.035493.108     Document Type: Article

References (47)

1. Abrahams, J.P. and Leslie, A.G. 1996. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D Biol. Crystallogr. 52: 30-42.
2. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, Z.W.M., and Lipman, D.J. 1997. Gapped Blast and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
3. Barnham, K.J., McKinstry, W.J., Multhaup, G., Galatis, D., Morton, C.J., Curtain, C.C., Williamson, N.A., White, A.R., Hinds, M.G., Norton, R.S., et al. 2003. Structure of the Alzheimer's disease amyloid precursor protein copper binding domain. A regulator of neuronal copper homeostasis. J. Biol. Chem. 278: 17401-17407.
4. Brünger, A.T., Kuriyan, J., and Karplus, M. 1987. Crystallographic R factor refinement by molecular dynamics. Science 235: 458-460.
5. Burggraf, S., Larsen, N., Woese, C.R., and Stetter, K.O. 1993. An intron within the 16S ribosomal RNA gene of the archaeon Pyrobaculum aerophilum. Proc. Natl. Acad. Sci. 90: 2547-2550.
6. Cowtan, K. 1994. "dm": An automated procedure for phase improvement by density modification. Newsletter on Protein Crystallography 31: 34-38.
7. de La Fortelle, E. and Bricogne, G. 1997. Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD methods. Methods Enzymol. 276: 472-494.
8. Deng, J., Schnaufer, A., Salavati, R., Stuart, K.D., and Hol, W.G.J. 2004. High resolution crystal structure of a key editosome enzyme from Trypanosoma brucei: RNA editing ligase 1. J. Mol. Biol. 343: 601-613.
9. d'Orval, B.C., Bortolin, M.L., Gaspin, C., and Bachellerie, J.P. 2001. Box C/D RNA guides for the ribose methylation of archaeal tRNAs. The tRNATrp intron guides the formation of two ribose-methylated nucleosides in the mature tRNATrp. Nucleic Acids Res. 29: 4518-4529.
10. Doublié, S. 1997. Preparation of selenomethionyl proteins for phase determination. Methods Enzymol. 276: 523-530.
11. El Omari, K., Ren, J., Bird, L.E., Bona, M.K., Klarmann, G., LeGrice, S.F.J., and Stammers, D.K. 2006. Molecular architecture and ligand recognition determinants for T4 RNA ligase. J. Biol. Chem. 281: 1573-1579.
12. Esnouf, R.M. 1997. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model. 15: 132-134.
13. Ha°kansson, K., Doherty, A.J., Shuman, S., and Wigley, D.B. 1997. X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell 89: 545-553.
14. Ho, C.K. and Shuman, S. 2002. Bacteriophage T4 RNA ligase 2 (gp24.1) exemplifies a family of RNA ligases found in all phylogenetic domains. Proc. Natl. Acad. Sci. 99: 12709-12714.
15. Ho, C.K., Etten, J.L.V., and Shuman, S. 1997. Characterization of an ATP-dependent DNA ligase encoded by Chlorella virus PBCV-1. J. Virol. 71: 1931-1937.
16. Kjems, J. and Garrett, R.A. 1988. Novel splicing mechanism for the ribosomal RNA intron in the archaebacterium Desulfurococcus mobilis. Cell 54: 693-703.
17. Konarska, M., Filipowicz, W., Domdey, H., and Gross, H.J. 1981. Formation of a 2′-phosphomonoester, 3′,5′-phosphodiester linkage by a novel RNA ligase in wheat germ. Nature 293: 112-116.
18. Kong, G.K.W., Adams, J.J., Harris, H.H., Boas, J.F., Curtain, C.C., Galatis, D., Masters, C.L., Barnham, K.J., McKinstry, W.J., Cappai, R., et al. 2007. Structural studies of the Alzheimer's amyloid precursor protein copper-binding domain reveal how it binds copper ions. J. Mol. Biol. 367: 148-161.
19. Krissinel, E. and Henrick, K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60: 2256-2268.
20. Krissinel, E. and Henrick, K. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372: 774-797.
21. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
22. +-dependent DNA ligase: Modular architecture and functional implications. EMBO J. 19: 1119-1129.
23. Liu, Y. and Eisenberg, D. 2002. 3D domain swapping: As domains continue to swap. Protein Sci. 11: 1285-1299.
24. Marck, C. and Grosjean, H. 2003. Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: Evolutionary implications. RNA 9: 1516-1531.
25. Martins, A. and Shuman, S. 2004. An RNA ligase from Deinococcus radiodurans. J. Biol. Chem. 279: 50654-50661.
26. Meslet-Cladiére, L., Norais, C., Kuhn, J., Briffotaux, J., Sloostra, J.W., Ferrari, E., Hübscher, U., Flament, D., and Myllykallio, H. 2007. A novel proteomic approach identifies new interaction partners for proliferating cell nuclear antigen. J. Mol. Biol. 372: 1137-1148.
27. Murshudov, G.N., Vagin, A.A., Lebedev, A., Wilson, K.S., and Dodson, E.J. 1999. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55: 247-255.
28. Nakatani, M., Ezaki, S., Atomi, H., and Imanaka, T. 2000. A DNA ligase from a hyperthermophilic archaeon with unique cofactor specificity. J. Bacteriol. 182: 6424-6433.
29. Nandakumar, J., Shuman, S., and Lima, C.D. 2006. RNA ligase structures reveal the basis for RNA specificity and conformational changes that drive ligation forward. Cell 127: 71-84.
30. Nandakumar, J., Nair, P.A., and Shuman, S. 2007. Last stop on the road to repair: Structure of E. coli DNA ligase bound to nicked DNA-adenylate. Mol. Cell 26: 257-271.
31. Pascal, J.M. 2008. DNA and RNA ligases: Structural variations and shared mechanisms. Curr. Opin. Struct. Biol. 18: 96-105.
32. Pascal, J.M., O'Brien, P.J., Tomkinson, A.E., and Ellenberger, T. 2004. Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 432: 473-478.
33. Sabatini, R. and Hajduk, S.L. 1995. RNA ligase and its involvement in guide RNA/mRNA chimera formation. Evidence for a cleavage-ligation mechanism of Trypanosoma brucei mRNA editing. J. Biol. Chem. 270: 7233-7240.
34. Salgia, S.R., Singh, S.K., Gurha, P., and Gupta, R. 2003. Two reactions of Haloferax volcanii RNA splicing enzymes: Joining of exons and circularization of introns. RNA 9: 319-330.
35. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: A laboratory manual, 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Schneider, T.R. and Sheldrick, G.M. 2002. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58: 1772-1779.
37. Shuman, S. and Schwer, B. 1995. RNA capping enzyme and DNA ligase: A superfamily of covalent nucleotidyl transferases. Mol. Microbiol. 17: 405-410.
38. Silber, R., Malathi, V.G., and Hurwitz, J. 1972. Purification and properties of bacteriophage T4-induced RNA ligase. Proc. Natl. Acad. Sci. 69: 3009-3013.
39. +- dependent DNA ligase encoded by a eukaryotic virus. J. Biol. Chem. 276: 36100-36109.
40. Starostina, N.G., Marshburn, S., Johnson, L.S., Eddy, S.R., Terns, R.M., and Terns, M.P. 2004. Circular box C/D RNAs in Pyrococcus furiosus. Proc. Natl. Acad. Sci. 101: 14097-14101.
41. Tatusov, R.L., Koonin, E.V., and Lipman, D.J. 1997. A genomic perspective on protein families. Science 278: 631-637.
42. Tomkinson, A.E., Vijayakumar, S., Pascal, J.M., and Ellenberger, T. 2006. DNA ligases: Structure, reaction mechanism, and function. Chem. Rev. 106: 687-699.
43. Wang, L.K., Ho, C.K., Pei, Y., and Shuman, S. 2003. Mutational analysis of bacteriophage T4 RNA ligase 1. Different functional groups are required for the nucleotidyl transfer and phosphodiester bond formation steps of the ligation reaction. J. Biol. Chem. 278: 29454-29462.
44. Wang, L.K., Nandakumar, J., Schwer, B., and Shuman, S. 2007. The C-terminal domain of T4 RNA ligase 1 confers specificity for tRNA repair. RNA 13: 1235-1244.
45. Westaway, S.K., Phizicky, E.M., and Abelson, J. 1988. Structure and function of the yeast tRNA ligase gene. J. Biol. Chem. 263: 3171-3176.
46. Xue, S., Calvin, K., and Li, H. 2006. RNA recognition and cleavage by a splicing endonuclease. Science 312: 906-910.
47. Yin, S., Ho, C.K., Miller, E.S., and Shuman, S. 2004. Characterization of bacteriophage KVP40 and T4 RNA ligase 2. Virology 319: 141-151.