Mutations of non-canonical base-pairs in the 3' major domain of Escherichia coli 16 S ribosomal RNA affect the initiation and elongation of protein synthesis

Journal of Molecular Biology

Volumn 259, Issue 2, 1996, Pages 207-215

  Dragon, François ^a,b   Spickler, Catherine ^a   Pinard, Robert ^a   Carrière, Julie ^a   Brakier Gingras, Léa ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

16 S ribosomal RNA; Non canonical base pairs; Site directed mutagenesis; Spectinomycin; Translation initiation

Indexed keywords

BACTERIAL RNA; RNA 16S;

ARTICLE; BACTERIAL GROWTH; ESCHERICHIA COLI; GROWTH INHIBITION; MUTATION; NONHUMAN; OPERON; PLASMID; POLYSOME; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SITE DIRECTED MUTAGENESIS; TRANSLATION INITIATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0029902548     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0313     Document Type: Article

References (48)

1. Baudin, F., Ehresmann, C., Romby P., Mougel, M., Colin, J., Lempereur, L., Bachellerie, J.-P., Ebel, J.-P. & Ehresmann, B. (1987). Higher-order structure of domain III in Escherichia coli 16 S ribosomal RNA, 30 S subunit and 70 S ribosome. Biochimie, 69, 1081-1096.
2. Bhangu, R. & Wollenzien, P. (1992). The mRNA binding track in the Escherichia coli ribosome for mRNAs of different sequences. Biochemistry, 31, 5937-5944.
3. Bilgin, N., Richter, A. A., Ehrenberg, M., Dahlberg, A. E. & Kurland, C. G. (1990). Ribosomal RNA and protein mutants resistant to spectinomycin. EMBO J. 9, 735-739.
4. Brimacombe, R. (1991). RNA-protein interactions in the Escherichia coli ribosome. Biochimie, 73, 927-936.
5. Brosius, J., Ullrich, A., Raker, M. A., Gray, A., Dull, T. J., Gutell, R. R. & Noller, H. F. (1981). Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal operon of E. coli. Plasmid, 6, 112-118.
6. Dahlberg, A. E. (1989). The functional role of ribosomal RNA in protein synthesis. Cell, 57, 525-529.
7. Donstova, O., Dokudovskaya, S., Kopylov, A., Bogdanov, A., Rinke-Appel, J., Jünke, N. & Brimacombe, R. (1992). Three widely separated positions in the 16 S RNA lie in or close to the ribosomal decoding region; a site-directed cross-linking study with mRNA analogues. EMBO J. 11, 3105-3116.
8. Döring, T., Mitchell, P., Osswald, M., Bochkariov, D. & Brimacombe R. (1994). The decoding region of 16 S RNA; a cross-linking study of the ribosomal A, P and E sites using tRNA derivatized at position 32 in the anticodon loop. EMBO J. 13, 2677-2685.
9. Dragon, F. & Brakier-Gingras, L. (1993). Interaction of Escherichia coli ribosomal protein S7 with 16 S rRNA. Nucl. Acids Res. 21, 1199-1203.
10. Dragon, F., Payant, C. & Brakier-Gingras L. (1994). Mutational and structural analysis of the RNA binding site for Escherichia coli ribosomal protein S7. J. Mol. Biol. 244, 74-85.
11. Göringer, H. U., Hijazi, K. A., Murgola, E. J. & Dahlberg, A. E. (1991). Mutations in 16 S rRNA that affect UGA (stop codon)-directed translation termination. Proc. Natl Acad. Sci. USA, 88, 6603-6607.
12. Gourse, R. L., Takebe, Y., Sharrock, R. & Nomura, M. (1985). Feedback regulation of rRNA and tRNA synthesis and accumulation of free ribosomes after conditional expression of rRNA genes. Proc. Natl Acad. Sci. USA, 82, 1069-1073.
13. Gutell, R. R. (1993). Collection of small subunit (16 S-and 16 S-like) ribosomal RNA structures. Nucl. Acids Res. 21, 3051-3054.
14. Gutell, R. R. & Woese, C. R. (1990). Higher order structural elements in ribosomal RNAs: pseudoknots and the use of noncanonical pairs. Proc. Natl Acad. Sci. USA, 87, 663-667.
15. Gutell, R. R., Larsen, N. & Woese, C. R. (1994). Lessons from an evolving rRNA: 16 S and 23 S rRNA structures from a comparative perspective. Microbiol. Rev. 58, 10-26.
16. Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580.
17. Hartz, D., McPheeters, D. D., Traut, R. & Gold, L. (1988). Extension inhibition analysis of translation initiation complexes. Methods Enzymol. 164, 419-425.
18. Jemiolo, D. K., Taurence, J. S. & Giese, S. (1991). Mutations in 16 S rRNA in Escherichia coli at methyl-modified sites: G966, C967, G1207. Nucl. Acids Res. 19, 4259-4265.
19. Johanson, U. & Hughes, D. (1995). A new mutation in 16 S rRNA of Escherichia coli conferring spectinomycin resistance. Nucl. Acids Res. 23, 464-466.
20. Kunkel, T. A., Roberts, J. D. & Zakour, R. A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
21. Leclerc, D. & Brakier-Gingras, L. (1990). Study of the function of Escherichia coli ribosomal RNA through site-directed mutagenesis. Biochem. Cell Biol. 68, 169-179.
22. Makosky P. C. & Dahlberg, A. E. (1987). Spectinomycin resistance at site 1192 in 16 S ribosomal RNA of E. coli: an analysis of three mutants. Biochimie, 69, 885-889.
23. Melançon, P., Leclerc, D. & Brakier-Gingras, L. (1990). A deletion at the 5' end of Escherichia coli 16 S ribosomal RNA. Biochim. Biophys. Acta, 1050, 98-103.
24. Miller, J. H. (1972). Determination of viable cell counts: bacterial growth curves. In Experiments in Molecular Genetics, pp. 31-36, Cold Spring Harbor Laboratory Press, Plainview, NY.
25. Moazed. D. & Noller, H. F. (1987). Interaction of antibiotics with functional sites in 16 S ribosomal RNA. Nature, 327, 389-394.
26. Moazed, D. & Noller, H. F. (1989). Intermediate states in the movement of transfer RNA in the ribosome. Nature, 342, 142-148.
27. Moazed, D. & Noller, H. F. (1990). Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16 S rRNA. J. Mol. Biol. 211, 135-145.
28. Moine, H. & Dahlberg, A. E. (1994). Mutations in helix 34 of Escherichia coli 16 S ribosomal RNA have multiple effects on ribosome function and synthesis. J. Mol. Biol. 243, 402-412.
29. Noller, H. F. (1991). Ribosomal RNA and translation. Annu. Rev. Biochem. 60, 191-227.
30. Noller, H. F. (1993). On the origin of the ribosome: coevolution of subdomains of tRNA and rRNA. In The RNA World (Gesteland, R. F. & Atkins, J. F., eds), pp. 137-156, Cold Spring Harbor Laboratory Press, Plainview, NY.
31. O'Connor, M., Göringer, H. U. & Dahlberg, A. E. (1992). A ribosomal ambiguity mutation in the 530 loop of E. coli 16 S rRNA. Nucl. Acids Res. 20, 4221-4227.
32. O'Connor, M., Brunelli, C. A., Firpo, M. A., Gregory S. T., Lieberman, K. R., Lodmell, J. S., Moine, H., Van Ryk, D. I. & Dahlberg, A. E. (1995). Genetic probes of ribosomal RNA function. Biochem. Cell Biol. 73, 859-868.
33. Pinard, R., Payant, C. & Brakier-Gingras, L. (1995). Mutations at positions 13 and/or 914 in Escherichia coli 16 S ribosomal RNA interfere with the initiation of protein synthesis. Biochemistry, 34, 9611-9616.
34. Prescott, C. D. & Kornau, H.-C. (1992). Mutations in E. coli 16 S rRNA that enhance and decrease the activity of a suppressor tRNA. Nucl. Acids Res. 20, 1567-1571.
35. Rinke-Appel, J., Jünke, N., Brimacombe, R., Lavrik, I., Dokudovskaya, S., Donstova, O. & Bogdanov, A. (1994). Contacts between 16 S ribosomal RNA and mRNA, within the spacer region separating the AUG initiator codon and the Shine-Dalgarno sequence; a site-directed cross-linking study Nucl. Acids Res. 22, 3018-3025.
36. Ron, E. Z., Kohler, R. E. & Davis, B. D. (1966). Polysomes extracted from Escherichia coli by freeze-thawlysozyme lysis. Science, 153, 1119-1120.
37. Rosendahl, G. & Douthwaite, S. (1995). Cooperative assembly of proteins in the ribosomal GTPase centre demonstrated by their interactions with mutant 23 S rRNAs. Nucl. Acids Res. 23, 2396-2403.
38. Samaha, R. R., O'Brien, B., O'Brien, T. W. & Noller, H. F. (1994). Independent in vitro assembly of a ribonucleoprotein particle containing the 3' domain of 16 S rRNA. Proc. Natl Acad. Sci. USA, 91, 7884-7888.
39. Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
40. Santer, U. V., Cekleniak, J. A. & Santer, M. (1993). The 530 loop of 16 S ribosomal RNA. Each base change confers its own phenotype. Mol. Biol. Cell, 4, 420a.
41. Sigmund, C. D., Ettayebi, M. & Morgan, E. A. (1984). Antibiotic resistance mutations in 16 S and 23 S ribosomal RNA genes of E. coli. Nucl. Acids Res. 12, 4653-4663.
42. Sigmund, C. D., Ettayebi, M., Borden, A. & Morgan, E. A. (1988). Antibiotic resistance mutations in ribosomal RNA genes of Escherichia coli. Methods Enzymol. 164, 673-690.
43. Spedding, G., Gluick, T. C. & Draper, D. E. (1993). Ribosome initiation complex formation with the pseudoknotted α operon messenger RNA. J. Mol. Biol. 229, 609-622.
44. Thomas, C. L., Gregory, R. J., Winslow, G., Muto, A. & Zimmermann, R. A. (1988). Mutations within the decoding site of Escherichia coli 16 S rRNA: growth-rate impairment, lethality and intragenic suppression. Nucl. Acids Res. 16, 8129-8146.
45. Triman, K. L. (1995). Mutational analysis of 16 S ribosomal RNA structure and function in Escherichia coli. Advan. Genet. 33, 1-39.
46. Triman, K., Becker, E., Dammel, C., Katz, J., Mori, H., Douthwaite, S., Yapijakis, C., Yoast, S. & Noller, H. F. (1989). Isolation of temperature-sensitive mutants of 16 S rRNA in Escherichia coli. J. Mol. Biol. 209, 645-653.
47. Vester, B. & Garrett, R. A. (1987). A plasmid-coded and site-directed mutation in Escherichia coli 23 S RNA that confers resistance to erythromycin: implications for the mechanism of action of erythromycin. Biochimie, 69, 891-900.
48. von Ahsen, U. & Noller, H. F. (1995). Identification of bases in 16 S rRNA essential for tRNA binding at the 30 S ribosomal P site. Science, 267, 234-237.