Negamycin Interferes with Decoding and Translocation by Simultaneous Interaction with rRNA and tRNA

Molecular Cell

Volumn 56, Issue 4, 2014, Pages 541-550

  Polikanov, Yury S ^a   Szal, Teresa ^b   Jiang, Fuyan ^b,c   Gupta, Pulkit ^b   Matsuda, Ryoichi ^d   Shiozuka, Masataka ^d   Steitz, Thomas A ^a   Vázquez Laslop, Nora ^b   Mankin, Alexander S ^b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c Adlai E Stevenson High School   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; NEGAMYCIN; RIBOSOME RNA; RNA 16S; RNA 18S; TETRACYCLINE; TRANSFER RNA; ANTIINFECTIVE AGENT; DIAMINO ACID; PROTEIN SYNTHESIS INHIBITOR;

ANTIBACTERIAL ACTIVITY; ANTICODON; ARTICLE; BACTERIAL MUTATION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG STRUCTURE; GENE INTERACTION; LARGE RIBOSOMAL SUBUNIT; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; RNA STRUCTURE; RNA TRANSPORT; THERMUS THERMOPHILUS; X RAY DIFFRACTION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; PROTEIN SYNTHESIS; RNA STABILITY; SMALL RIBOSOMAL SUBUNIT; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; AMINO ACIDS, DIAMINO; ANTI-BACTERIAL AGENTS; BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA STABILITY; RNA, BACTERIAL; RNA, MESSENGER; RNA, RIBOSOMAL; RNA, TRANSFER; THERMUS THERMOPHILUS;

EID: 84912565442     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.09.021     Document Type: Article

References (53)

1. Allamand V., Bidou L., Arakawa M., Floquet C., Shiozuka M., Paturneau-Jouas M., Gartioux C., Butler-Browne G.S., Mouly V., Rousset J.P., et al. Drug-induced readthrough of premature stop codons leads to the stabilization of laminin alpha2 chain mRNA in CMD myotubes. J.Gene Med. 2008, 10:217-224.
2. Arakawa M., Shiozuka M., Nakayama Y., Hara T., Hamada M., Kondo S., Ikeda D., Takahashi Y., Sawa R., Nonomura Y., et al. Negamycin restores dystrophin expression in skeletal and cardiac muscles of mdx mice. J.Biochem. 2003, 134:751-758.
3. Asai T., Zaporojets D., Squires C., Squires C.L. An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc. Natl. Acad. Sci. USA 1999, 96:1971-1976.
4. Ben-Shem A., Garreau de Loubresse N., Melnikov S., Jenner L., Yusupova G., Yusupov M. The structure of the eukaryotic ribosome at 3.0Å resolution. Science 2011, 334:1524-1529.
5. Blanchard S.C., Gonzalez R.L., Kim H.D., Chu S., Puglisi J.D. tRNA selection and kinetic proofreading in translation. Nat. Struct. Mol. Biol. 2004, 11:1008-1014.
6. Bollenbach T., Quan S., Chait R., Kishony R. Nonoptimal microbial response to antibiotics underlies suppressive drug interactions. Cell 2009, 139:707-718.
7. Borovinskaya M.A., Pai R.D., Zhang W., Schuwirth B.S., Holton J.M., Hirokawa G., Kaji H., Kaji A., Cate J.H. Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat. Struct. Mol. Biol. 2007, 14:727-732.
8. Borovinskaya M.A., Shoji S., Holton J.M., Fredrick K., Cate J.H. A steric block in translation caused by the antibiotic spectinomycin. ACS Chem. Biol. 2007, 2:545-552.
9. Brodersen D.E., Clemons W.M., Carter A.P., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 2000, 103:1143-1154.
10. Brodersen D.E., Carter A.P., Clemons W.M., Morgan-Warren R.J., Murphy F.V., Ogle J.M., Tarry M.J., Wimberly B.T., Ramakrishnan V. Atomic structures of the 30S subunit and its complexes with ligands and antibiotics. Cold Spring Harb. Symp. Quant. Biol. 2001, 66:17-32.
11. Carter A.P., Clemons W.M., Brodersen D.E., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 2000, 407:340-348.
12. Corchuelo M.C., Herzog A., Desmarez L., Lavallé R., Bollen A. Resistance to the peptide-like antibiotic negamycin in Escherichia coli. Biochem. Biophys. Res. Commun. 1981, 100:1497-1503.
13. Dailidiene D., Bertoli M.T., Miciuleviciene J., Mukhopadhyay A.K., Dailide G., Pascasio M.A., Kupcinskas L., Berg D.E. Emergence of tetracycline resistance in Helicobacter pylori: multiple mutational changes in 16S ribosomal DNA and other genetic loci. Antimicrob. Agents Chemother. 2002, 46:3940-3946.
14. Dönhöfer A., Franckenberg S., Wickles S., Berninghausen O., Beckmann R., Wilson D.N. Structural basis for TetM-mediated tetracycline resistance. Proc. Natl. Acad. Sci. USA 2012, 109:16900-16905.
15. Douthwaite S., Powers T., Lee J.Y., Noller H.F. Defining the structural requirements for a helix in 23S ribosomal RNA that confers erythromycin resistance. J.Mol. Biol. 1989, 209:655-665.
16. Floquet C., Rousset J.P., Bidou L. Readthrough of premature termination codons in the adenomatous polyposis coli gene restores its biological activity in human cancer cells. PLoS ONE 2011, 6:e24125.
17. Gerrits M.M., de Zoete M.R., Arents N.L., Kuipers E.J., Kusters J.G. 16S rRNA mutation-mediated tetracycline resistance in Helicobacter pylori. Antimicrob. Agents Chemother. 2002, 46:2996-3000.
18. Gerrits M.M., Berning M., Van Vliet A.H., Kuipers E.J., Kusters J.G. Effects of 16S rRNA gene mutations on tetracycline resistance in Helicobacter pylori. Antimicrob. Agents Chemother. 2003, 47:2984-2986.
19. Griffey R.H., Hofstadler S.A., Sannes-Lowery K.A., Ecker D.J., Crooke S.T. Determinants of aminoglycoside-binding specificity for rRNA by using mass spectrometry. Proc. Natl. Acad. Sci. USA 1999, 96:10129-10133.
20. Hamada M., Takeuchi T., Kondo S., Ikeda Y., Naganawa H. A new antibiotic, negamycin. J.Antibiot. 1970, 23:170-171.
21. Hartz D., McPheeters D.S., Traut R., Gold L. Extension inhibition analysis of translation initiation complexes. Methods Enzymol. 1988, 164:419-425.
22. Jenner L., Starosta A.L., Terry D.S., Mikolajka A., Filonava L., Yusupov M., Blanchard S.C., Wilson D.N., Yusupova G. Structural basis for potent inhibitory activity of the antibiotic tigecycline during protein synthesis. Proc. Natl. Acad. Sci. USA 2013, 110:3812-3816.
23. Jerinic O., Joseph S. Conformational changes in the ribosome induced by translational miscoding agents. J.Mol. Biol. 2000, 304:707-713.
24. Jünemann R., Wadzack J., Triana-Alonso F.J., Bittner J.U., Caillet J., Meinnel T., Vanatalu K., Nierhaus K.H. Invivo deuteration of transfer RNAs: overexpression and large-scale purification of deuterated specific tRNAs. Nucleic Acids Res. 1996, 24:907-913.
25. Karimi R., Ehrenberg M. Dissociation rate of cognate peptidyl-tRNA from the A-site of hyper-accurate and error-prone ribosomes. Eur. J. Biochem. 1994, 226:355-360.
26. Laurberg M., Asahara H., Korostelev A., Zhu J., Trakhanov S., Noller H.F. Structural basis for translation termination on the 70S ribosome. Nature 2008, 454:852-857.
27. Mikolajka A., Liu H., Chen Y., Starosta A.L., Márquez V., Ivanova M., Cooperman B.S., Wilson D.N. Differential effects of thiopeptide and orthosomycin antibiotics on translational GTPases. Chem. Biol. 2011, 18:589-600.
28. Mizuno S., Nitta K., Umezawa H. Mechanism of action of negamycin in Escherichia coli K12. I. Inhibition of initiation of protein synthesis. J.Antibiot. 1970, 23:581-588.
29. Mizuno S., Nitta K., Umezawa H. Mechanism of action of negamycin in Escherichia coli K12. II. Miscoding activity in polypeptide synthesis directed by snythetic polynucleotide. J.Antibiot. 1970, 23:589-594.
30. Nonaka L., Connell S.R., Taylor D.E. 16S rRNA mutations that confer tetracycline resistance in Helicobacter pylori decrease drug binding in Escherichia coli ribosomes. J.Bacteriol. 2005, 187:3708-3712.
31. O'Callaghan C.H., Morris A., Kirby S.M., Shingler A.H. Novel method for detection of beta-lactamases by using a chromogenic cephalosporin substrate. Antimicrob. Agents Chemother. 1972, 1:283-288.
32. Ogle J.M., Ramakrishnan V. Structural insights into translational fidelity. Annu. Rev. Biochem. 2005, 74:129-177.
33. Orelle C., Carlson S., Kaushal B., Almutairi M.M., Liu H., Ochabowicz A., Quan S., Pham V.C., Squires C.L., Murphy B.T., Mankin A.S. Tools for characterizing bacterial protein synthesis inhibitors. Antimicrob. Agents Chemother. 2013, 57:5994-6004.
34. Peske F., Savelsbergh A., Katunin V.I., Rodnina M.V., Wintermeyer W. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J.Mol. Biol. 2004, 343:1183-1194.
35. Pioletti M., Schlünzen F., Harms J., Zarivach R., Glühmann M., Avila H., Bashan A., Bartels H., Auerbach T., Jacobi C., et al. Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 2001, 20:1829-1839.
36. Polikanov Y.S., Blaha G.M., Steitz T.A. How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science 2012, 336:915-918.
37. Polikanov Y.S., Osterman I.A., Szal T., Tashlitsky V.N., Serebryakova M.V., Kusochek P., Bulkley D., Malanicheva I.A., Efimenko T.A., Efremenkova O.V., et al. Amicoumacin A inhibits translation by stabilizing mRNA interaction with the ribosome. Mol. Cell 2014, 56:531-540. this issue.
38. Polikanov Y.S., Steitz T.A., Innis C.A. A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat. Struct. Mol. Biol. 2014, 21:787-793.
39. Purohit P., Stern S. Interactions of a small RNA with antibiotic and RNA ligands of the 30S subunit. Nature 1994, 370:659-662.
40. Ross J.I., Eady E.A., Cove J.H., Cunliffe W.J. 16S rRNA mutation associated with tetracycline resistance in a gram-positive bacterium. Antimicrob. Agents Chemother. 1998, 42:1702-1705.
41. Schlünzen F., Harms J.M., Franceschi F., Hansen H.A., Bartels H., Zarivach R., Yonath A. Structural basis for the antibiotic activity of ketolides and azalides. Structure 2003, 11:329-338.
42. Schmitt E., Blanquet S., Mechulam Y. Crystallization and preliminary X-ray analysis of Escherichia coli methionyl-tRNAMet(f) formyltransferase complexed with formyl-methionyl-tRNAMet(f). Acta Crystallogr. Sect. D Biol. Crystallogr. 1999, 55:332-334.
43. Schroeder S.J., Blaha G., Moore P.B. Negamycin binds to the wall of the nascent chain exit tunnel of the 50S ribosomal subunit. Antimicrob. Agents Chemother. 2007, 51:4462-4465.
44. Shoji S., Walker S.E., Fredrick K. Reverse translocation of tRNA in the ribosome. Mol. Cell 2006, 24:931-942.
45. Spahn C.M., Blaha G., Agrawal R.K., Penczek P., Grassucci R.A., Trieber C.A., Connell S.R., Taylor D.E., Nierhaus K.H., Frank J. Localization of the ribosomal protection protein Tet(O) on the ribosome and the mechanism of tetracycline resistance. Mol. Cell 2001, 7:1037-1045.
46. Taguchi A., Nishiguchi S., Shiozuka M., Nomoto T., Ina M., Nojima S., Matsuda R., Nonomura Y., Kiso Y., Yamazaki Y., et al. Negamycin analogue with readthrough-promoting activity as a potential drug candidate for duchenne muscular dystrophy. ACS Med Chem Lett 2012, 3:118-122.
47. Uehara Y., Kondo S., Umezawa H., Suzukake K., Hori M. Negamycin, a miscoding antibiotic with a unique structure. J.Antibiot. 1972, 25:685-688.
48. Uehara Y., Hori M., Umezawa H. Negamycin inhibits termination of protein synthesis directed by phage f2 RNA invitro. Biochim. Biophys. Acta 1974, 374:82-95.
49. Uehara Y., Hori M., Kondo S., Hamada M., Umezawa H. Structure-activity relationships among negamycin analogs. J.Antibiot. 1976, 29:937-943.
50. Uehara Y., Hori M., Umezawa H. Specific inhibition of the termination process of protein synthesis by negamycin. Biochim. Biophys. Acta 1976, 442:251-262.
51. Voorhees R.M., Weixlbaumer A., Loakes D., Kelley A.C., Ramakrishnan V. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 2009, 16:528-533.
52. Voss N.R., Gerstein M., Steitz T.A., Moore P.B. The geometry of the ribosomal polypeptide exit tunnel. J.Mol. Biol. 2006, 360:893-906.
53. Wilson D.N. The A-Z of bacterial translation inhibitors. Crit. Rev. Biochem. Mol. Biol. 2009, 44:393-433.