Crystal structure of the avilamycin resistance-conferring methyltransferase AviRa from Streptomyces viridochromogenes

Journal of Molecular Biology

Volumn 329, Issue 1, 2003, Pages 147-157

  Mosbacher, Tanja G ^a   Bechthold, Andreas ^a   Schulz, Georg E ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Antibiotic resistance; rRNA methyltransferase; S adenosyl L methionine; Selenomethionine MAD, ribosome docking

Indexed keywords

AVILAMYCIN; DOCKING PROTEIN; EVERNIMICIN; GUANINE; METHYL GROUP; METHYLTRANSFERASE; PEPTIDYLTRANSFERASE; PROTEIN AVIRA; RIBOSOME PROTEIN; RIBOSOME RNA; S ADENOSYLMETHIONINE; SELENOMETHIONINE; UNCLASSIFIED DRUG;

ALPHA HELIX; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; METHYLATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; RIBOSOME; RNA SEQUENCE; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; STREPTOMYCES; X RAY DIFFRACTION;

BACTERIA (MICROORGANISMS); STREPTOMYCES; STREPTOMYCES VIRIDOCHROMOGENES;

EID: 0038708223     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00407-8     Document Type: Article

References (48)

1. Buzzetti F., Eisenberg F., Grant H.N., Keller-Schierlein W., Voser W., Zähner H. Avilamycin. Experientia. 24:1968;320-323.
2. McNicholas P.M., Najarian D.J., Mann P.A., Hesk D., Hare R.S., Shaw K.J., Black T.A. Evernimicin binds exclusively to the 50 S ribosomal subunit and inhibits translation in cell-free systems derived from both gram-positive and gram-negative bacteria. Antimicrob. Agents Chemother. 44:2000;1121-1126.
3. Kofoed C.B., Vester B. Interaction of avilamycin with ribosomes and resistance caused by mutations in 23 S rRNA. Antimicrob. Agents Chemother. 46:2002;3339-3342.
4. Aarestrup F.M. Association between decreased susceptibility to a new antibiotic for treatment of human diseases, everninomicin (SCH 27899), and resistance to an antibiotic used for growth promotion in animals, avilamycin. Microb. Drug Resist. 4:1998;137-141.
5. Adrian P.V., Zhao W., Black T.A., Shaw K.J., Hare R.S., Klugman K.P. Mutations in ribosomal protein L16 conferring reduced susceptibility to evernimicin (SCH27899): implications for mechanism of action. Antimicrob. Agents Chemother. 44:2000;732-738.
6. Adrian P.V., Mendrick C., Loebenberg D., Shaw K.J., Klugman K.P., Hare R.S., Black T.A. Evernimicin (SCH27899) inhibits a novel ribosome target site: analysis of 23 S ribosomal DNA mutants. Antimicrob. Agents Chemother. 44:1999;3101-3106.
7. Weitnauer G., Gaisser S., Trefzer A., Stockert S., Westrich L., Quiros L.M., et al. An ATP-binding cassette transporter and two rRNA methyltransferases are involved in resistance to avilamycin in the producer organism Streptomyces viridochromogenes Tü57. Antimicrob. Agents Chemother. 45:2001;690-695.
8. Treede I., Jacobsen L., Kirpekar F., Vester B., Weitnauer G., Bechthold A., Douthwaite S. The avilamycin resistance determinants AviRa and AviRb methylate 23 S rRNA at the guanosine 2535 base and the uridine 2479 ribose. Mol. Microbiol. 2003;. In press.
9. Belova L., Tenson T., Xiong L., McNicholas P.M., Mankin A.S. A novel site of antibiotic action in the ribosome: interaction of evernimicin with the large ribosomal subunit. Proc. Natl Acad. Sci. USA. 98:2001;3726-3731.
10. Yu L., Petros A.M., Schnuchel A., Zhong P., Severin J.M., Walter K., et al. Solution structure of an rRNA methyltransferase (ErmAM) that confers macrolide-lincosamide-streptogramin antibiotic resistance. Nature Struct. Biol. 4:1997;483-489.
11. Schluckebier G., Zhong P., Stewart K.D., Kavanaugh T.J., Abad-Zapatero C. The 2.2 Å structure of the rRNA methyltransferase ErmC′ and its complexes with cofactor and cofactor analogs: implications for the reaction mechanism. J. Mol. Biol. 289:1999;277-291.
12. Cheng X., Blumenthal R.M. Editors of S-Adenosylmethionine-dependent Methyltransferases: Structures and Functions. 1999;World Scientific Publ. Singapore.
13. Schluckebier G., O'Gara M., Saenger W., Cheng X. Universal catalytic domain structure of AdoMet-dependent methyltransferases. J. Mol. Biol. 247:1995;16-20.
14. Cheng X., Roberts R.J. AdoMet-dependent methylation, DNA methyltransferases and base flipping. Nucl. Acids Res. 29:2001;3784-3795.
15. Martin J.L., McMillan F.M. SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol. 12:2002;783-793.
16. Malone T., Blumenthal R.M., Cheng X. Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J. Mol. Biol. 253:1995;618-632.
17. Bügl H., Fauman E.B., Staker B.L., Zheng F., Kushner S.R., Saper M.A., et al. RNA methylation under heat shock control. Mol. Cell. 6:2000;349-360.
18. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:1992;275-282.
19. Hall D.R., Bond C.S., Leonard G.A., Watt C.I., Berry A., Hunter W.N. Structure of tagatose-1,6-bisphosphate aldolase. Insight into chiral discrimination, mechanism, and specificity of class II. J. Biol. Chem. 277:2002;22018-22024.
20. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK - a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
21. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
22. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138.
23. Gupta A., Kumar P.H., Dineshkumar T.K., Varshney U., Subramanya H.S. Crystal structure of Rv2118c: an AdoMet-dependent methyltransferase from Mycobacterium tuberculosis H37Rv. J. Mol. Biol. 312:2001;381-391.
24. Bujnicki J.M., Rychlewski L. RNA:(guanine-N2) methyltransferases RsmC/RsmD and their homologs revisited - bioinformatic analysis and prediction of the active site based on the uncharacterized Mj0882 protein structure. BMC Bioinformatics. 3:2002;10-21.
25. Wang H., Boisvert D., Kim K.K., Kim R., Kim S.-H. Crystal structure of a fribrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 1.6 Å resolution. EMBO J. 19:2000;317-323.
26. Schulz G.E. Binding of nucleotides by proteins. Curr. Opin. Struct. Biol. 2:1992;61-67.
27. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., et al. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 107:2001;679-688.
28. Carter A.P., Clemons W.M. Jr, Brodersen D.E., Morgan-Warren R.J., Hartsch T., Wimberly B.T., Ramakrishnan V. Crystal structure of an initiation factor bound to the 30 S ribosomal subunit. Science. 291:2001;498-501.
29. Hendrickson W.A., Horton J.R., LeMaster D.M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9:1990;1665-1672.
30. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
31. Perrakis A., Sixma T.K., Wilson K.S., Lamzin V.S. wARP: improvement and extension of crystallographic phases by weighted averaging of multiple refined dummy atomic models. Acta Crystallog. sect. D. 53:1997;448-455.
32. Jones T., Zou J., Cowan S., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
33. Hooft R.W.H., Sander C., Vriend G., Abola E.E. Errors in protein structures. Nature. 381:1996;272.
34. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
35. Kleywegt G.J., Jones T.A. A super position. Joint ESF/CCP4 Newsletter. 31:1994;9-14.
36. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
37. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
38. Merritt E., Bacon D. Raster 3D. Photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
39. Schubert H.L., Wilson K.S., Raux E., Woodcock S.C., Warren M.J. The X-ray structure of a cobalamin biosynthetic enzyme, cobalt-precorrin-4 methyltransferase. Nature Struct. Biol. 5:1998;585-592.
40. Michel G., Sauvé V., Larocque R., Li Y., Matte A., Cygler M. The structure of RlmB 23 S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot. Structure. 10:2002;1303-1315.
41. Nureki O., Shirouzu M., Hashimoto K., Ishitani R., Tereda T., Tamokoshi M., et al. An enzyme with a deep trefoil knot for the active-site architecture. Acta Crystallog. sect. D. 58:2002;1129-1137.
42. Trievel R.C., Beach B.M., Dirk L.M., Houtz R.L., Hurley J.H. Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell. 111:2002;91-103.
43. Jacobs S.A., Harp J.M., Devarakonda S., Kim Y., Rastinejad F., Khorasanizadeh S. The active site of the SET domain is constructed on a knot. Nature Struct. Biol. 9:2002;833-838.
44. Min J., Zhang X., Cheng X., Grewal S.I., Xu R.M. Structure of the SET domain histone lysine methyltransferase Clr4. Nature Struct. Biol. 9:2002;828-832.
45. Wilson J.R., Jing C., Walker P.A., Martini S.R., Howell S.A., Blackburn G.M., et al. Crystal structure and functional analysis of the histone methyltransferase. Cell. 111:2002;105-115.
46. Zhang X., Tamaru H., Khan S.I., Horton J.R., Keefe L.J., Selker E.U., Cheng X. Structure of the neurospora SET domain protein DIM-5, a histone H3 lysine methyltransferase. Cell. 111:2002;117-127.
47. Roguey A., Schaft D., Shevchenko A., Pijnappel W.W.M.P., Wilm M., Assland R., Stewart A.F. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 20:2001;7137-7148.
48. Manzur K.L., Farooq A., Zeng L., Plotnikova O., Koch A.W., Sachchidanand, Zhou M.M. A dimeric viral SET domain methyltransferase specific to Lys27 of histone H3. Nature Struct. Biol. 10:2003;187-196.