Molecular Mechanism of Drug-Dependent Ribosome Stalling

Molecular Cell

Volumn 30, Issue 2, 2008, Pages 190-202

  Vazquez Laslop, Nora ^a   Thum, Celine ^a   Mankin, Alexander S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

RNA

Indexed keywords

AMINO ACID; ANTIBIOTIC AGENT; ERYTHROMYCIN; HMR 3004; NUCLEOTIDE; PEPTIDYLTRANSFERASE; RNA 23S; RU 66252; RU 69847; TELITHROMYCIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CISTRON; DRUG BINDING; ERYTHROMYCIN RESISTANCE METHYLTRANSFERASE GENE; GENE; GENE MAPPING; GENE MUTATION; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; RIBOSOME; RNA TRANSLATION;

5' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BASE SEQUENCE; CELL-FREE SYSTEM; DNA FOOTPRINTING; DRUG RESISTANCE, BACTERIAL; ERYTHROMYCIN; ESCHERICHIA COLI; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDYL TRANSFERASES; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, TRANSFER, AMINO ACYL;

EID: 43049089746     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.02.026     Document Type: Article

References (54)

1. Asai T., Zaporojets D., Squires C., and 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 96 (1999) 1971-1976
2. Bailey M., Chettiath T., and Mankin A.S. Induction of erm(C) expression by non-inducing antibiotics. Antimicrob. Agents Chemother. 52 (2008) 866-874
3. Bayfield M.A., Thompson J., and Dahlberg A.E. The A2453-C2499 wobble base pair in Escherichia coli 23S ribosomal RNA is responsible for pH sensitivity of the peptidyltransferase active site conformation. Nucleic Acids Res. 32 (2004) 5512-5518
4. Berisio R., Schluenzen F., Harms J., Bashan A., Auerbach T., Baram D., and Yonath A. Structural insight into the role of the ribosomal tunnel in cellular regulation. Nat. Struct. Biol. 10 (2003) 366-370
5. Bonnefoy A., Girard A.M., Agouridas C., and Chantot J.F. Ketolides lack inducibility properties of MLS(B) resistance phenotype. J. Antimicrob. Chemother. 40 (1997) 85-90
6. Bryskier A. Ketolides-telithromycin, an example of a new class of antibacterial agents. Clin. Microbiol. Infect. 6 (2000) 661-669
7. Cao J., and Geballe A.P. Inhibition of nascent-peptide release at translation termination. Mol. Cell. Biol. 16 (1996) 7109-7114
8. Chittum H.S., and Champney W.S. Ribosomal protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli. J. Bacteriol. 176 (1994) 6192-6198
9. Clarebout G., and Leclercq R. Fluorescence assay for studying the ability of macrolides to induce production of ribosomal methylase. Antimicrob. Agents Chemother. 46 (2002) 2269-2272
10. Cochella L., and Green R. Isolation of antibiotic resistance mutations in the rRNA by using an in vitro selection system. Proc. Natl. Acad. Sci. USA 101 (2004) 3786-3791
11. Cruz-Vera L.R., Rajagopal S., Squires C., and Yanofsky C. Features of ribosome-peptidyl-tRNA interactions essential for tryptophan induction of tna operon expression. Mol. Cell 19 (2005) 333-343
12. Cruz-Vera L.R., Gong M., and Yanofsky C. Changes produced by bound tryptophan in the ribosome peptidyl transferase center in response to TnaC, a nascent leader peptide. Proc. Natl. Acad. Sci. USA 103 (2006) 3598-3603
13. Dale T., and Uhlenbeck O.C. Amino acid specificity in translation. Trends Biochem. Sci. 30 (2005) 659-665
14. Douthwaite S., Powers T., Lee J.Y., and Noller H.F. Defining the structural requirements for a helix in 23S ribosomal RNA that confers erythromycin resistance. J. Mol. Biol. 209 (1989) 655-665
15. Ettayebi M., Prasad S.M., and Morgan E.A. Chloramphenicol-erythromycin resistance mutations in a 23S rRNA gene of Escherichia coli. J. Bacteriol. 162 (1985) 551-557
16. Gabashvili I.S., Gregory S.T., Valle M., Grassucci R., Worbs M., Wahl M.C., Dahlberg A.E., and Frank J. The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol. Cell 8 (2001) 181-188
17. Garza-Ramos G., Xiong L., Zhong P., and Mankin A. Binding site of macrolide antibiotics on the ribosome: new resistance mutation identifies a specific interaction of ketolides with rRNA. J. Bacteriol. 183 (2001) 6898-6907
18. Gong F., and Yanofsky C. Instruction of translating ribosome by nascent peptide. Science 297 (2002) 1864-1867
19. Gong F., Ito K., Nakamura Y., and Yanofsky C. The mechanism of tryptophan induction of tryptophanase operon expression: tryptophan inhibits release factor-mediated cleavage of TnaC-peptidyl-tRNA(Pro). Proc. Natl. Acad. Sci. USA 98 (2001) 8997-9001
20. Gryczan T.J., Grandi G., Hahn J., Grandi R., and Dubnau D. Conformational alteration of mRNA structure and the posttranscriptional regulation of erythromycin-induced drug resistance. Nucleic Acids Res. 8 (1980) 6081-6097
21. Hansen J.L., Ippolito J.A., Ban N., Nissen P., Moore P.B., and Steitz T.A. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol. Cell 10 (2002) 117-128
22. Hardy K., and Haefeli C. Expression in Escherichia coli of a staphylococcal gene for resistance to macrolide, lincosamide, and streptogramin type B antibiotics. J. Bacteriol. 152 (1982) 524-526
23. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., Bartels H., Franceschi F., and Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107 (2001) 679-688
24. Hartz D., McPheeters D.S., Traut R., and Gold L. Extension inhibition analysis of translation initiation complexes. Methods Enzymol. 164 (1988) 419-425
25. Hesslein A.E., Katunin V.I., Beringer M., Kosek A.B., Rodnina M.V., and Strobel S.A. Exploration of the conserved A+C wobble pair within the ribosomal peptidyl transferase center using affinity purified mutant ribosomes. Nucleic Acids Res. 32 (2004) 3760-3770
26. Horinouchi S., and Weisblum B. Posttranscriptional modification of mRNA conformation: mechanism that regulates erythromycin-induced resistance. Proc. Natl. Acad. Sci. USA 77 (1980) 7079-7083
27. Jenni S., and Ban N. The chemistry of protein synthesis and voyage through the ribosomal tunnel. Curr. Opin. Struct. Biol. 13 (2003) 212-219
28. Krayevsky A.A., and Kukhanova M.K. The peptidyltransferase center of ribosomes. Prog. Nucleic Acid Res. Mol. Biol. 23 (1979) 1-51
29. Lovmar M., Tenson T., and Ehrenberg M. Kinetics of macrolide action: the josamycin and erythromycin cases. J. Biol. Chem. 279 (2004) 53506-53515
30. Mayford M., and Weisblum B. ermC leader peptide. Amino acid sequence critical for induction by translational attenuation. J. Mol. Biol. 206 (1989) 69-79
31. Mayford M., and Weisblum B. The ermC leader peptide: amino acid alterations leading to differential efficiency of induction by macrolide-lincosamide-streptogramin B antibiotics. J. Bacteriol. 172 (1990) 3772-3779
32. Mitra K., Schaffitzel C., Fabiola F., Chapman M.S., Ban N., and Frank J. Elongation arrest by SecM via a cascade of ribosomal RNA rearrangements. Mol. Cell 22 (2006) 533-543
33. Moazed D., and Noller H.F. Intermediate states in the movement of transfer RNA in the ribosome. Nature 342 (1989) 142-148
34. Muth G.W., Ortoleva-Donnelly L., and Strobel S.A. A single adenosine with a neutral pKa in the ribosomal peptidyl transferase center. Science 289 (2000) 947-950
35. Muto H., Nakatogawa H., and Ito K. Genetically encoded but nonpolypeptide prolyl-tRNA functions in the A site for SecM-mediated ribosomal stall. Mol. Cell 22 (2006) 545-552
36. Nakatogawa H., and Ito K. Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol. Cell 7 (2001) 185-192
37. Nakatogawa H., and Ito K. The ribosomal exit tunnel functions as a discriminating gate. Cell 108 (2002) 629-636
38. Narayanan C.S., and Dubnau D. Evidence for the translational attenuation model: ribosome-binding studies and structural analysis with an in vitro run-off transcript of ermC. Nucleic Acids Res. 13 (1985) 7307-7326
39. Nissen P., Hansen J., Ban N., Moore P.B., and Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science 289 (2000) 920-930
40. Ohashi H., Shimizu Y., Ying B.W., and Ueda T. Efficient protein selection based on ribosome display system with purified components. Biochem. Biophys. Res. Commun. 352 (2007) 270-276
41. Onouchi H., Nagami Y., Haraguchi Y., Nakamoto M., Nishimura Y., Sakurai R., Nagao N., Kawasaki D., Kadokura Y., and Naito S. Nascent peptide-mediated translation elongation arrest coupled with mRNA degradation in the CGS1 gene of Arabidopsis. Genes Dev. 19 (2005) 1799-1810
42. Rosato A., Vicarini H., Bonnefoy A., Chantot J.F., and Leclercq R. A new ketolide, HMR 3004, active against streptococci inducibly resistant to erythromycin. Antimicrob. Agents Chemother. 42 (1998) 1392-1396
43. Schlünzen F., Zarivach R., Harms J., Bashan A., Tocilj A., Albrecht R., Yonath A., and Franceschi F. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413 (2001) 814-821
44. Schlünzen F., Harms J.M., Franceschi F., Hansen H.A., Bartels H., Zarivach R., and Yonath A. Structural basis for the antibiotic activity of ketolides and azalides. Structure 11 (2003) 329-338
45. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310 (2005) 827-834
46. Shimizu Y., Inoue A., Tomari Y., Suzuki T., Yokogawa T., Nishikawa K., and Ueda T. Cell-free translation reconstituted with purified components. Nat. Biotechnol. 19 (2001) 751-755
47. Shivakumar A.G., Hahn J., Grandi G., Kozlov Y., and Dubnau D. Posttranscriptional regulation of an erythromycin resistance protein specified by plasmic pE194. Proc. Natl. Acad. Sci. USA 77 (1980) 3903-3907
48. Tenson T., Lovmar M., and Ehrenberg M. The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome. J. Mol. Biol. 330 (2003) 1005-1014
49. Tu D., Blaha G., Moore P.B., and Steitz T.A. Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121 (2005) 257-270
50. Vazquez D. The Macrolide Antibiotics. In: Corcoran J.W., and Hahn F.E. (Eds). Antibiotics III. Mechanism of action of antimicrobial and antitumor agents (1975), Springer-Verlag, New York 459-479
51. Wang Z., and Sachs M.S. Ribosome stalling is responsible for arginine-specific translational attenuation in Neurospora crassa. Mol. Cell. Biol. 17 (1997) 4904-4913
52. Weisblum B. Insights into erythromycin action from studies of its activity as inducer of resistance. Antimicrob. Agents Chemother. 39 (1995) 797-805
53. Woolhead C.A., Johnson A.E., and Bernstein H.D. Translation arrest requires two-way communication between a nascent polypeptide and the ribosome. Mol. Cell 22 (2006) 587-598
54. Zaporojets D., French S., and Squires C.L. Products transcribed from rearranged rrn genes of Escherichia coli can assemble to form functional ribosomes. J. Bacteriol. 185 (2003) 6921-6927