The Cm56 tRNA modification in archaea is catalyzed either by a specific 2′-O-methylase, or a C/D sRNP

RNA

Volumn 11, Issue 7, 2005, Pages 1051-1063

  Renalier, Marie Hél̀ene ^a   Joseph, Nicole ^a   Gaspin, Christine ^b   Thebault, Patricia ^b   Mougin, Annie ^a  

^a CNRS   (France)

^b CEMAGREF   (France)

Author keywords

Archaea; Cm56; Ribose 2 O methylation; sRNP; tRNA

Indexed keywords

METHYLTRANSFERASE; NUCLEOSIDE; RNA METHYLTRANSFERASE; S ADENOSYLMETHIONINE; TRANSFER RNA;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; CONTROLLED STUDY; CRENARCHAEOTA; GENE EXPRESSION; GENE SEQUENCE; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PYROCOCCUS ABYSSI; RNA METHYLATION; RNA TRANSCRIPTION; YEAST;

AMINO ACID SEQUENCE; CATALYSIS; CLONING, MOLECULAR; CONSENSUS SEQUENCE; CYTOSINE; ESCHERICHIA COLI; GENOME, ARCHAEAL; GLUTATHIONE TRANSFERASE; KINETICS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; OPEN READING FRAMES; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; PYROBACULUM; PYROCOCCUS ABYSSI; RECOMBINANT PROTEINS; RNA, ARCHAEAL; RNA, SMALL NUCLEOLAR; RNA, TRANSFER; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TEMPERATURE; TRNA METHYLTRANSFERASES;

ARCHAEA; PYROBACULUM AEROPHILUM; PYROCOCCUS ABYSSI;

EID: 22244492008     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.2110805     Document Type: Article

References (82)

1. Agris, P.F. 1996. The importance of being modified: Roles of modified nucleosides and Mg2+ in RNA structure and function. Prog. Nucleic Acid Res. Mol. Biol. 53: 79-129.
2. Agris, P.F., Koh, H., and Soll, D. 1973. The effect of growth temperatures on the in vivo ribose methylation of Bacillus stearothermophilus transfer RNA. Arch. Biochem. Biophys. 154: 277-282.
3. Ahn, H.J., Kim, H.W., Yoon, H.J., Lee, B.I., Suh, S.W., and Yang, J.K. 2003. Crystal structure of tRNA(m1G37)methyltransferase: Insights into tRNA recognition. EMBO J. 22: 2593-2603.
4. Aittaleb, M., Rashid, R., Chen, Q., Palmer, J.R., Daniels, C.J., and Li, H. 2003. Structure and function of archaeal box C/D sRNP core proteins. Nat. Struct. Biol. 10: 256-263.
5. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. 1997. Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
6. Anantharaman, V., Koonin, E.V., and Aravind, L. 2002. SPOUT: A class of methyltransferases that includes spoU and trmD RNA methylase superfamilies, and novel superfamilies of predicted prokaryotic RNA methylases. J. Mol. Microbiol. Biotechnol. 4: 71-75.
7. Armengaud, J., Urbonavicius, J., Fernandez, B., Chaussinand, G., Bujnicki, J.M., and Grosjean, H. 2004. N2-methylation of guanosine at position 10 in tRNA is catalyzed by a THUMP domain containing, AdoMet-dependent methyltransferase, conserved in archaea and eukaryota. J. Biol. Chem. 279: 37142-37152.
8. Arn, E.A. and Abelson, J.N. 1996. The 2′-5′ RNA ligase of Escherichia coli. Purification, cloning, and genomic disruption. J. Biol. Chem. 271: 31145-31153.
9. Auffinger, P. and Westhof, E. 1998. Location and distribution of modified nucleotides in tRNA. In Modification and editing of RNA (H. Grosjean and R. Benne, eds.), pp. 569-576. ASM Press, Washington, D.C.
10. Bai, Y., Fox, D.T., Lacy, J.A., Van Lanen, S.G., and Iwata-Reuyl, D. 2000. Hypermodification of tRNA in Thermophilic archaea. Cloning, overexpression, and characterization of tRNA-guanine transglycosylase from Methanococcus jannaschii. J. Biol. Chem. 275: 28731-28738.
11. Becker, H.F., Motorin, Y., Sissler, M., Florentz, C., and Grosjean, H. 1997. Major identity determinants for enzymatic formation of ribothymidine and pseudouridine in the T ψ-loop of yeast tRNAs. J. Mol. Biol. 274: 505-518.
12. Behm-Ansmant, I., Urban, A., Ma, X., Yu, Y.T., Motorin, Y., and Branlant, C. 2003. The Saccharomyces cerevisiae U2 snRNA: pseudouridine-synthase Pus7p is a novel multisite-multisubstrate RNA:Ψ-synthase also acting on tRNAs. RNA 9: 1371-1382.
13. Bjork, G.R. 1995. tRNA: Structure, biosynthesis, and function. ASM Press, Washington, DC.
14. Bjork, G.R., Jacobsson, K., Nilsson, K., Johansson, M.J., Bystrom, A.S., and Persson, O.P. 2001. A primordial tRNA modification required for the evolution of life? EMBO J. 20: 231-239.
15. Bortolin, M.L., Bachellerie, J.P., and Clouet-d'Orval, B. 2003. In vitro RNP assembly and methylation guide activity of an unusual box C/D RNA, cis-acting archaeal pre-tRNA(Trp). Nucleic Acids Res. 31: 6524-6535.
16. Cavaille, J. and Bachellerie, J.P. 1996. Processing of fibrillarin-associated snoRNAs from pre-mRNA introns: An exonucleolytic process exclusively directed by the common stem-box terminal structure. Biochimie 78: 443-456.
17. _. 1998. SnoRNA-guided ribose methylation of rRNA: Structural features of the guide RNA duplex influencing the extent of the reaction. Nucleic Acids Res. 26: 1576-1587.
18. Cavaille, J., Chetouani, F., and Bachellerie, J.P. 1999. The yeast Saccharomyces cerevisiae YDL112w ORF encodes the putative 2′-O-ribose methyltransferase catalyzing the formation of Gm18 intRNAs. RNA 5: 66-81.
19. Clouet d'Orval, B., 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 ribosemethylated nucleosides in the mature tRNATrp. Nucleic Acids Res. 29: 4518-4529.
20. Clouet d'Orval, B., Gaspin, C., and Mougin, A. 2005. Two different mechanisms for tRNA ribose methylation in Archaea: A short survey. Biochimie (in press).
21. Constantinesco, F., Motorin, Y., and Grosjean, H. 1999a. Characterisation and enzymatic properties of tRNA(guanine 26, N (2), N (2))-dimethyltransferase (Trm1p) from Pyrococcus furiosus. J. Mol. Biol. 291: 375-392.
22. _. 1999b. Transfer RNA modification enzymes from Pyrococcus furiosus: Detection of the enzymatic activities in vitro. Nucleic Acids Res. 27: 1308-1315.
23. Cuff, J.A., Clamp, M.E., Siddiqui, A.S., Finlay, M., and Barton, G.J. 1998. JPred: A consensus secondary structure prediction server.Bioinformatics 14: 892-893.
24. Davis, D.R. 1998. Biophysical and conformational properties of modified nucleosides in RNA (nuclear magnetic resonance studies). In Modification and editing of RNA (H. Grosjea and R. Benne, eds.), pp. 85-102. ASM Press, Washington, DC.
25. Decatur, W.A. and Fournier, M.J. 2003. RNA-guided nucleotide modification of ribosomal and other RNAs. J. Biol. Chem. 278: 695-698.
26. Dennis, P.P., Omer, A., and Lowe, T. 2001. A guided tour: Small RNA function in Archaea. Mol. Microbiol. 40: 509-519.
27. Droogmans, L., Haumont, E., de Henau, S., and Grosjean, H. 1986. Enzymatic 2′-O-methylation of the wobble nucleoside of eukaryotic tRNAPhe: Specificity depends on structural elements outside the anticodon loop. EMBO J. 5: 1105-1109.
28. Elkins, P.A., Watts, J.M., Zalacain, M., van Thiel, A., Vitazka, P.R., Redlak, M., Andraos-Selim, C., Rastinejad, F., and Holmes, W.M. 2003. Insights into catalysis by a knotted TrmD tRNA methyltransferase. J. Mol. Biol. 333: 931-949.
29. Grosjean, H. and Benne, R. 1998. Modification and editing of RNA.ASM Press, Washington, DC.
30. Grosjean, H., Sprinzl, M., and Steinberg, S. 1995. Posttranscriptionally modified nucleosides in transfer RNA: Their locations and frequencies. Biochimie 77: 139-141.
31. Grosjean, H., Keith, G., and Droogmans, L. 2004. Detection and quantification of modified nucleotides in RNA using thin-layer chromatography. Humana Press, Inc., Totowa, NJ.
32. Gu, X., Yu, M., Ivanetich, K.M., and Santi, D.V. 1998. Molecular recognition of tRNA by tRNA pseudouridine 55 synthase. Biochemistry 37: 339-343.
33. Gustafsson, C., Reid, R., Greene, P.J., and Santi, D.V. 1996. Identification of new RNA modifying enzymes by iterative genome search using known modifying enzymes as probes. Nucleic Acids Res. 24: 3756-3762.
34. Hoang, C. and Ferre-D'Amare, A.R. 2001. Cocrystal structure of a tRNA Psi55 pseudouridine synthase: Nucleotide flipping by an RNA-modifying enzyme. Cell 107: 929-939.
35. Hori, H., Yamazaki, N., Matsumoto, T., Watanabe, Y., Ueda, T., Nishikawa, K., Kumagai, I., and Watanabe, K. 1998. Substrate recognition of tRNA (Guanosine-2′-)-methyltransferase from Thermus thermophilus HB27. J. Biol. Chem. 273: 25721-25727.
36. Ishitani, R., Nureki, O., Nameki, N., Okada, N., Nishimura, S., and Yokoyama, S. 2003. Alternative tertiary structure of tRNA for recognition by a posttranscriptional modification enzyme. Cell 113: 383-394.
37. Jiang, H.Q., Motorin, Y., Jin, Y.X., and Grosjean, H. 1997. Pleiotropic effects of intron removal on base modification pattern of yeast tRNAPhe: An in vitro study. Nucleic Acids Res. 25: 2694-2701.
38. Kiss T. 2001. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J. 20: 3617-3622.
39. Kiss-Laszlo, Z., Henry, Y., Bachellerie, J.P., Caizergues-Ferrer, M., and Kiss, T. 1996. Site-specific ribose methylation of preribosomal RNA: A novel function for small nucleolar RNAs. Cell 85: 1077- 1088.
40. Koonin, E.V. and Rudd, K.E. 1993. SpoU protein of Escherichia coli belongs to a new family of putative rRNA methylases. Nucleic Acids Res. 21: 5519.
41. Kowalak, J.A., Dalluge, J.J., McCloskey, J.A., and Stetter, K.O. 1994. The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry 33: 7869- 7876.
42. Kuhn, J.F., Tran, E.J., and Maxwell, E.S. 2002. Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/ Snu13p snoRNP core protein. Nucleic Acids Res. 30: 931-941.
43. Lapeyre, B. and Purushothaman, S.K. 2004. Spb1p-directed formation of Gm2922 in the ribosome catalytic center occurs at a late processing stage. Mol. Cell 16: 663-669.
44. Li, H., Trotta, C.R., and Abelson, J. 1998. Crystal structure and evolution of a transfer RNA splicing enzyme. Science 280: 279-284.
45. Lim, K., Zhang, H., Tempczyk, A., Krajewski, W., Bonander, N., Toedt, J., Howard, A., Eisenstein, E., and Herzberg, O. 2003. Structure of the YibK methyltransferase from Haemophilus influenzae (HI0766): A cofactor bound at a site formed by a knot. Proteins 51: 56-67.
46. Limbach, P.A., Crain, P.F., and McCloskey, J.A. 1994. Summary: The modified nucleosides of RNA. Nucleic Acids Res. 22: 2183-2196.
47. Lo Conte, L., Ailey, B., Hubbard, T.J., Brenner, S.E., Murzin, A.G., and Chothia, C. 2000. SCOP: A structural classification of proteins database. Nucleic Acids Res. 28: 257-259.
48. Marck, C. and Grosjean, H. 2002. tRNomics: Analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8: 1189-1232.
49. _. 2003. Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: Evolutionary implications. RNA 9: 1516-1531.
50. McCloskey, J.A. and Crain, P.F. 1998. The RNA modification database-1998. Nucleic Acids Res. 26: 196-197.
51. McCloskey, J.A., Graham, D.E., Zhou, S., Crain, P.F., Ibba, M., Konisky, J., Soll, D., and Olsen, G.J. 2001. Post-transcriptional modification in archaeal tRNAs: Identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res. 29: 4699-4706.
52. Michel, G., Sauve, V., Larocque, R., Li, Y., Matte, A., and Cygler, M. 2002. The structure of the RlmB 23S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot. Structure (Camb) 10: 1303-1315.
53. Motorin, Y. and Grosjean, H. 1998. Chemical structures and classification of postranscriptionally modified nucleosides in RNA. In Modification and editing of RNA (H. Grosjean and R. Benne, eds.), pp. 543-549. ASM Press, Washington, DC.
54. _. 1999. Multisite-specific tRNA:m5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: Identification of the gene and substrate specificity of the enzyme. RNA 5: 1105-1118.
55. Noon, K.R., Guymon, R., Crain, P.F., McCloskey, J.A., Thomm, M., Lim, J., and Cavicchioli, R. 2003. Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii (optimum growth temperature [Topt], 23°C) and Stetteria hydrogenophila (Topt, 95°C). J. Bacteriol. 185: 5483-5490.
56. Nureki, O., Shirouzu, M., Hashimoto, K., Ishitani, R., Terada, T., Tamakoshi, M., Oshima, T., Chijimatsu,M., Takio, K.,Vassylyev,D.G., et al. 2002. An enzyme with a deep trefoil knot for the active-site architecture. Acta Crystallogr. D Biol. Crystallogr. 58: 1129-1137.
57. Nureki, O., Watanabe, K., Fukai, S., Ishii, R., Endo, Y., Hori, H., and Yokoyama, S. 2004. Deep knot structure for construction of active site and cofactor binding site of tRNA modification enzyme. Structure (Camb) 12: 593-602.
58. Omer, A.D., Lowe, T.M., Russell, A.G., Ebhardt, H., Eddy, S.R., and Dennis, P.P. 2000. Homologs of small nucleolar RNAs in Archaea. Science 288: 517-522.
59. Omer, A.D., Ziesche, S., Ebhardt, H., and Dennis, P.P. 2002. In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex. Proc. Natl. Acad. Sci. 99: 5289-5294.
60. Omer, A.D., Ziesche, S., Decatur, W.A., Fournier, M.J., and Dennis, P.P. 2003. RNA-modifying machines in archaea. Mol. Microbiol. 48: 617-629.
61. Pierrel, F., Hernandez, H.L., Johnson,M.K., Fontecave, M., and Atta,M. 2003. MiaB protein from Thermotoga maritima. Characterization of an extremely thermophilic tRNA-methylthiotransferase. J. Biol. Chem. 278: 29515-29524.
62. Pintard, L., Lecointe, F., Bujnicki, J.M., Bonnerot, C., Grosjean, H., and Lapeyre, B. 2002. Trm7p catalyses the formation of two 2′- Omethylriboses in yeast tRNA anticodon loop. EMBO J. 21: 1811-1820.
63. Reyes, V.M. and Abelson, J. 1987. A synthetic substrate for tRNA splicing. Anal. Biochem. 166: 90-106.
64. Romby, P., Carbon, P., Westhof, E., Ehresmann, C., Ebel, J.P., Ehresmann, B., and Giege, R. 1987. Importance of conserved residues for the conformation of the T-loop in tRNAs. J. Biomol. Struct. Dyn. 5: 669-687.
65. Roovers, M., Wouters, J., Bujnicki, J.M., Tricot, C., Stalon, V., Grosjean, H., and Droogmans, L. 2004. A primordial RNA modification enzyme: The case of tRNA (m1A) methyltransferase. Nucleic Acids Res. 32: 465-476.
66. Rozenski, J., Crain, P.F., and McCloskey, J.A. 1999. The RNA modification database: 1999 update. Nucleic Acids Res. 27: 196-197.
67. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
68. Sampson, J.R. and Uhlenbeck, O.C. 1988. Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro. Proc. Natl. Acad. Sci. 85: 1033-1037.
69. Sampson, J.R., DiRenzo, A.B., Behlen, L.S., and Uhlenbeck, O.C. 1990. Role of the tertiary nucleotides in the interaction of yeast phenylalanine tRNA with its cognate synthetase. Biochemistry 29: 2523-2532.
70. Schubert, H.L., Blumenthal, R.M., and Cheng, X. 2003. Many paths to methyltransfer: A chronicle of convergence. Trends Biochem Sci. 28: 329-335.
71. Singh, S.K., Gurha, P., Tran, E.J., Maxwell, E.S., and Gupta, R. 2004. Sequential 2′-O-methylation of archaeal pre-tRNATrp nucleotides is guided by the intron-encoded but trans-acting box C/D ribonucleoprotein of pre-tRNA. J. Biol. Chem. 279: 47661-47671.
72. Sprinzl, M., Horn, C., Brown, M., Ioudovitch, A., and Steinberg, S. 1998. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 26: 148-153.
73. Szewczak, L.B., DeGregorio, S.J., Strobel, S.A., and Steitz, J.A. 2002. Exclusive interaction of the 15.5 kD protein with the terminal box C/D motif of a methylation guide snoRNP. Chem. Biol. 9: 1095-1107.
74. Tang, T.H., Bachellerie, J.P., Rozhdestvensky, T., Bortolin, M.L., Huber, H., Drungowski, M., Elge, T., Brosius, J., and Huttenhofer, A. 2002. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc. Natl. Acad. Sci. 99: 7536-7541.
75. Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Mazumder, R., Mekhedov, S.L., Nikolskaya, A.N., et al. 2003. The COG database: An updated version includes eukaryotes. BMC Bioinformatics 4: 41.
76. Tran, E.J., Zhang, X., and Maxwell, E.S. 2003. Efficient RNA 2′-Omethylation requires juxtaposed and symmetrically assembled archaeal box C/D and C'/D' RNPs. EMBO J. 22: 3930-3940.
77. Tran, E., Brown, J., and Maxwell, E.S. 2004. Evolutionary origins of the RNA-guided nucleotide-modification complexes: From the primitive translation apparatus? Trends Biochem. Sci. 29: 343-350.
78. Trotta, C.R., Miao, F., Arn, E.A., Stevens, S.W., Ho, C.K., Rauhut, R., and Abelson, J.N. 1997. The yeast tRNA splicing endonuclease: A tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases. Cell 89: 849-858.
79. Watanabe, K., Nureki, O., Fukai, S., Ishii, R., Okamoto, H., Yokoyama, S., Endo, Y., and Hori, H. 2005. Roles of conserved amino acid sequence motifs in the SpoU (TrmH) RNA methyltransferase family. J. Biol. Chem. 280: 10368-10377.
80. Watkins, N.J., Dickmanns, A., and Luhrmann, R. 2002. Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5 K protein, for the hierarchical assembly of the box C/D snoRNP. Mol. Cell. Biol. 22: 8342-8352.
81. Zarembinski, T.I., Kim, Y., Peterson, K., Christendat, D., Dharamsi, A., Arrowsmith, C.H., Edwards, A.M., and Joachimiak, A. 2003. Deep trefoil knot implicated in RNA binding found in an archaebacterial protein. Proteins 50: 177-183.
82. Ziesche, S.M., Omer, A.D., and Dennis, P.P. 2004. RNA-guided nucleotide modification of ribosomal and non-ribosomal RNAs in Archaea. Mol. Microbiol. 54: 980-993.