The last rRNA methyltransferase of E. coli revealed: The yhiR gene encodes adenine-N6 methyltransferase specific for modification of A2030 of 23S ribosomal RNA

RNA

Volumn 18, Issue 9, 2012, Pages 1725-1734

  Golovina, Anna Y ^a   Dzama, Margarita M ^a   Osterman, Ilya A ^a   Sergiev, Petr V ^a   Serebryakova, Marina V ^a   Bogdanov, Alexey A ^a   Dontsova, Olga A ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Methylation; Modification; N6 methyl adenosine; rRNA; yhiR

Indexed keywords

A2030; ADENINE N6 METHYLTRANSFERASE; BACTERIAL PROTEIN; METHYLTRANSFERASE; PROTEOME; RIBONUCLEOPROTEIN; RIBOSOME RNA; RIBOSOME RNA METHYLTRANSFERASE; RLMJ PROTEIN; RNA 23S; RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG; YHIR PROTEIN;

ANAEROBIC BACTERIUM; ANAEROBIC GROWTH; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; ENZYME MODIFICATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE IDENTIFICATION; GENE INACTIVATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; RNA METHYLATION;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE KNOCKOUT TECHNIQUES; METHYLATION; METHYLTRANSFERASES; PHENOTYPE; PROTEOMICS; RNA, RIBOSOMAL, 23S;

EID: 84865133343     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.034207.112     Document Type: Article

References (61)

1. 5U1939 methyltransferase from Escherichia coli. J Biol Chem 277: 8835-8840.
2. 5C methyltransferase specific for 16 S rRNA nucleotide 1407. J Mol Biol 359: 777-786.
3. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2: 2006.0008. doi: 10.1038/msb4100050.
4. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289: 905-920. (Pubitemid 30659939)
5. Basturea GN, Rudd KE, Deutscher MP. 2006. Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA 12: 426-434. (Pubitemid 43290870)
6. Basturea GN, Dague DR, Deutscher MP, Rudd KE. 2012. YhiQ is RsmJ, the methyltransferase responsible for methylation of G1516 in 16S rRNA of E. coli. J Mol Biol 415: 16-21.
7. Branlant C, Krol A, Machatt MA, Pouyet J, Ebel JP, Edwards K, Kossel H. 1981. Primary and secondary structures of Escherichia coli MRE 600 23S ribosomal RNA. Comparison with models of secondary structure for maize chloroplast 23S rRNA and for large portions of mouse and human 16S mitochondrial rRNAs. Nucleic Acids Res 9: 4303-4324. (Pubitemid 12195771)
8. Bugl H, Fauman EB, Staker BL, Zheng F, Kushner SR, Saper MA, Bardwell JC, Jakob U. 2000. RNA methylation under heat shock control. Mol Cell 6: 349-360.
9. Caldas T, Binet E, Bouloc P, Costa A, Desgres J, Richarme G. 2000. The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23 S ribosomal RNA methyltransferase. J Biol Chem 275: 16414-16419. (Pubitemid 30398860)
10. Connolly K, Rife JP, Culver G. 2008. Mechanistic insight into the ribosome biogenesis functions of the ancient protein KsgA. Mol Microbiol 70: 1062-1075.
11. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci 97: 6640-6645. (Pubitemid 30412767)
12. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, Friedland GD, Huang KH, Keller K, Novichkov PS, et al. 2010. MicrobesOnline: An integrated portal for comparative and functional genomics. Nucleic Acids Res 38: D396-D400.
13. Ero R, Peil L, Liiv A, Remme J. 2008. Identification of pseudouridine methyltransferase in Escherichia coli. RNA 14: 2223-2233.
14. 5UAC). RNA 15: 1134-1141.
15. 5C967 methyltransferase from Escherichia coli. Biochemistry 38: 4053-4057.
16. 1G745-deficient mutant. J Bacteriol 180: 359-365.
17. Gutgsell NS, Deutscher MP, Ofengand J. 2005. The pseudouridine synthase RluD is required for normal ribosome assembly and function in Escherichia coli. RNA 11: 1141-1152. (Pubitemid 40994194)
18. Hager J, Staker BL, Bugl H, Jakob U. 2002. Active site in RrmJ, a heat shock-induced methyltransferase. J Biol Chem 277: 41978-41986. (Pubitemid 35257512)
19. Havelund JF, Giessing AM, Hansen T, Rasmussen A, Scott LG, Kirpekar F. 2011. Identification of 5-hydroxycytidine at position 2501 concludes characterization of modified nucleotides in E. coli 23S rRNA. J Mol Biol 411: 529-536.
20. Helser TL, Davies JE, Dahlberg JE. 1972. Mechanism of kasugamycin resistance in Escherichia coli. Nat New Biol 235: 6-9.
21. Huang L, Ku J, Pookanjanatavip M, Gu X, Wang D, Greene PJ, Santi DV. 1998. Identification of two Escherichia coli pseudouridine synthases that show multisite specificity for 23S RNA. Biochemistry 37: 15951-15957. (Pubitemid 28524767)
22. Keseler IM, Collado-Vides J, Santos-Zavaleta A, Peralta-Gil M, Gama-Castro S, Muniz-Rascado L, Bonavides-Martinez C, Paley S, Krummenacker M, Altman T, et al. 2011. EcoCyc: A comprehensive database of Escherichia coli biology. Nucleic Acids Res 39: D583-D590.
23. Kimura S, Suzuki T. 2010. Fine-tuning of the ribosomal decoding center by conserved methyl-modifications in the Escherichia coli rRNA. Nucleic Acids Res 38: 1341-1352.
24. Kimura S, Ikeuchi Y, Kitahara K, Sakaguchi Y, Suzuki T. 2011. Base methylations in the double-stranded RNA by a fused methyltransferase bearing unwinding activity. Nucleic Acids Res 40: 4071-4085.
25. Kirpekar F, Hansen LH, Rasmussen A, Poehlsgaard J, Vester B. 2005. The archaeon Haloarcula marismortui has few modifications in the central parts of its 23S ribosomal RNA. J Mol Biol 348: 563-573. (Pubitemid 40515669)
26. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (A complete Set of E. coli K-12 ORF Archive): Unique resources for biological research. DNA Res 12: 291-299.
27. Konan KV, Yanofsky C. 1997. Regulation of the Escherichia coli tna operon: Nascent leader peptide control at the tnaC stop codon. J Bacteriol 179: 1774-1779. (Pubitemid 27100469)
28. 2G methyltransferases: I. The ycbY gene encodes a methyltransferase specific for G2445 of the 23 S rRNA. J Mol Biol 364: 20-25.
29. Lesnyak DV, Osipiuk J, Skarina T, Sergiev PV, Bogdanov AA, Edwards A, Savchenko A, Joachimiak A, Dontsova OA. 2007. Methyltransferase that modifies guanine 966 of the 16 S rRNA: Functional identification and tertiary structure. J Biol Chem 282: 5880-5887. (Pubitemid 47093721)
30. Lovgren JM, Wikstrom PM. 2001. The rlmB gene is essential for formation of Gm2251 in 23S rRNA but not for ribosome maturation in Escherichia coli. J Bacteriol 183: 6957-6960. (Pubitemid 33064212)
31. 5U1939 in 23S rRNA using MALDI mass spectrometry. Nucleic Acids Res 31: 4738-4746.
32. Mangat CS, Brown ED. 2008. Ribosome biogenesis; the KsgA protein throws a methyl-mediated switch in ribosome assembly. Mol Microbiol 70: 1051-1053.
33. Merzlyak EM, Goedhart J, Shcherbo D, Bulina ME, Shcheglov AS, Fradkov AF, Gaintzeva A, Lukyanov KA, Lukyanov S, Gadella TW, et al. 2007. Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods 4: 555-557. (Pubitemid 47214772)
34. Nakatogawa H, Ito K. 2002. The ribosomal exit tunnel functions as a discriminating gate. Cell 108: 629-636. (Pubitemid 34241424)
35. Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, Lee S, Kazmierczak KM, Lee KJ, Wong A, et al. 2011. Phenotypic landscape of a bacterial cell. Cell 144: 143-156.
36. Nierhaus K. 1990. Reconstitution of ribosomes. In Ribosomes and protein synthesis: A practical approach (ed. G Spedding), pp. 161-189. Oxford University Press, Oxford.
37. O'Connor M, Gregory ST. 2011. Inactivation of the RluD pseudouridine synthase has minimal effects on growth and ribosome function in wild-type Escherichia coli and Salmonella enterica. J Bacteriol 193: 154-162.
38. Okamoto S, Tamaru A, Nakajima C, Nishimura K, Tanaka Y, Tokuyama S, Suzuki Y, Ochi K. 2007. Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol Microbiol 63: 1096-1106. (Pubitemid 46188264)
39. Osterman IA, Prokhorova IV, Sysoev VO, Boykova YV, Efremenkova OV, Svetlov MS, Kolb VA, Bogdanov AA, Sergiev PV, Dontsova OA. 2012. Attenuation-based dual-fluorescent-protein reporter for screening translation inhibitors. Antimicrob Agents Chemother 56: 1774-1783.
40. Palchevskiy V, Finkel SE. 2006. Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient. J Bacteriol 188: 3902-3910. (Pubitemid 43825395)
41. 6-dimethyladenosines near the 3′end of 16 S ribosomal RNA of Escherichia coli. III. Purification and properties of the methylating enzyme and methylase-30 S interactions. J Biol Chem 254: 9094-9100.
42. 3Ψ methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA. RNA 14: 2234-2244.
43. 5C methyltransferase specific for 23S rRNA nucleotide 1962. J Mol Biol 383: 641-651.
44. Purta E, O'Connor M, Bujnicki JM, Douthwaite S. 2009. YgdE is the 2′-O-ribose methyltransferase RlmM specific for nucleotide C2498 in bacterial 23S rRNA. Mol Microbiol 72: 1147-1158.
45. Rizzo MA, Springer GH, Granada B, Piston DW. 2004. An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22: 445-449. (Pubitemid 38451376)
46. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 A resolution. Science 310: 827-834. (Pubitemid 41567336)
47. Sergiev PV, Bogdanov AA, Dontsova OA. 2005a. How can elongation factors EF-G and EF-Tu discriminate the functional state of the ribosome using the same binding site? FEBS Lett 579: 5439-5442. (Pubitemid 41455612)
48. Sergiev PV, Lesnyak DV, Burakovsky DE, Kiparisov SV, Leonov AA, Bogdanov AA, Brimacombe R, Dontsova OA. 2005b. Alteration in location of a conserved GTPase-associated center of the ribosome induced by mutagenesis influences the structure of peptidyltransferase center and activity of elongation factor G. J Biol Chem 280: 31882-31889. (Pubitemid 41291938)
49. 2G methyltransferases: II. The ygjO gene encodes a methyltransferase specific for G1835 of the 23 S rRNA. J Mol Biol 364: 26-31.
50. 6methyltransferase specific for modification of A1618 of 23 S ribosomal RNA, a methylated residue located close to the ribosomal exit tunnel. J Mol Biol 375: 291-300.
51. Sergiev PV, Golovina AY, Prokhorova IV, Sergeeva OV, Osterman IA, Nesterchuk MV, Burakovskii DE, Bogdanov AA, Dontsova OA. 2011. Modifications of ribosomal RNA: From enzymes to function. In Ribosomes: Structure, function, and dynamics (ed. MV Rodnina et al.), pp. 97-110. Springer, New York.
52. Sergiev PV, Golovina AY, Sergeeva OV, Osterman IA, Nesterchuk MV, Bogdanov AA, Dontsova OA. 2012. How much can we learn about the function of bacterial rRNA modification by mining large-scale experimental datasets? Nucleic Acids Res 40: 5694-5705.
53. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
54. Siibak T, Remme J. 2010. Subribosomal particle analysis reveals the stages of bacterial ribosome assembly at which rRNA nucleotides are modified. RNA 16: 2023-2032.
55. Stewart V, Yanofsky C. 1986. Role of leader peptide synthesis in tryptophanase operon expression in Escherichia coli K-12. J Bacteriol 167: 383-386. (Pubitemid 16067092)
56. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, et al. 2011. The STRING database in 2011: Functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561-D568.
57. Toh SM, Xiong L, Bae T, Mankin AS. 2008. The methyltransferase YfgB/RlmN is responsible for modification of adenosine 2503 in 23S rRNA. RNA 14: 98-106.
58. 5C967 methyltransferase from Escherichia coli. Biochemistry 38: 1884-1892.
59. 2G1207 methyltransferase from Escherichia coli. J Biol Chem 274: 924-929.
60. Vecerek B, Moll I, Blasi U. 2007. Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J 26: 965-975.
61. Xu Z, O'Farrell HC, Rife JP, Culver GM. 2008. A conserved rRNA methyltransferase regulates ribosome biogenesis. Nat Struct Mol Biol 15: 534-536. (Pubitemid 351653583)