Mutations in the peptidyl transferase center of 23 S rRNA reveal the site of action of sparsomycin, a universal inhibitor of translation

Journal of Molecular Biology

Volumn 261, Issue 2, 1996, Pages 222-230

  Tan, Ghee T ^a   DeBlasio, Alexandra ^a   Mankin, Alexander S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Antibiotics; Peptidyl transferase; Ribosome; rRNA; Sparsomycin

Indexed keywords

NUCLEOTIDE; PEPTIDYLTRANSFERASE; RIBOSOME RNA; RNA 23S; SPARSOMYCIN;

ARTICLE; CONTROLLED STUDY; DRUG BINDING; DRUG RESISTANCE; GENE MUTATION; HALOBACTERIUM SALINARUM; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; RIBOSOME; TRANSLATION REGULATION;

ARCHAEA; HALOBACTERIUM SALINARUM;

EID: 0030590258     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0454     Document Type: Article

References (31)

1. Cline, S. W., Lam, W. L., Charlebois, R. L., Schalkwyk, L. C. & Doolittle, W. F. (1989). Transformation methods for halophilic archaebacteria. Can. J. Microbiol. 35, 148-152.
2. Cundliffe, E. (1981). Antibiotic inhibitors of ribosome function. In The Molecular Basis of Antibiotic Action (Gale, E. F., Cundliffe, E., Reynolds, P. E., Richmond, M. H. & Waring, M. J., eds), pp. 402-545, John Wiley & Sons, London, New York, Sydney, Toronto.
3. Cundliffe, E. (1990). Recognition sites for antibiotics within rRNA. In The Ribosome: Structure, Function and Evolution (Hill, W. E., Dahlberg, A., Garrett, R. A., Moore, P. B., Schlessinger, D. & Warner, J. R., eds), pp. 479-490, American Society for Microbiology, Washington DC.
4. Garrett, R. A. & Rodriguez-Fonseca, C. (1995). The peptidyl transferase center. In Ribosomal RNA: Structure, Evolution, Processing and Function in Protein Biosynthesis (Zimmermann, R. A. & Dahlberg, A. E., eds), pp. 327-355, CRC Press, Boca Raton, New York, London, Tokyo.
5. 3H]-ρ-azidopuromycin photoaffinity labeling of Escherichia coli ribosomes: evidence for site-specific interaction at U2504 and G2502 in domain V of 23 S rRNA. Biochemistry, 27, 3983-3990.
6. Hofman, J. D., Lau, R. H. & Doolittle, W. F. (1979). The number, physical organization and transcription of ribosomal RNA cistrons in archaebacterium Halobacterium halobium. Nucl. Acids Res. 7, 1321-1333.
7. Hummel, H. & Böck, A. (1987). 23 S ribosomal RNA mutations in halobacteria conferring resistance to the anti-80S ribosome-targeted antibiotic anisomycin. Nucl. Acids Res. 15, 2431-1442.
8. Lázaro, E., van den Broek, L. A. G. M., Felix, A. S., Ottenheijm, H. C. J. & Ballesta, J. P. G. (1991a). Chemical, biochemical and genetic endeavours characterizing the interaction of sparsomycin with the ribosome. Biochimie, 73, 1137-1143.
9. Lázaro, E., van den Broek, L. A. G. M., Felix, A. S., Ottenheijm, H. C. J. & Ballesta, J. P. G. (1991b). Biochemical and kinetic characteristics of the interaction of the antitumor antibiotic sparsomycin with prokaryotic and eukaryotic ribosomes. Biochemistry, 30, 9642-9648.
10. Lázaro, E., Rodriguez-Fonseca, C., Porse, B., Ureña, D., Garrett, R. A. & Ballesta, J. P. G. (1996). A sparsomycin-resistant mutant of Halobacterium salinarium lacks a modification at nucleotide U2603 in the peptidyl transferase center of 23 S rRNA. J. Mol. Biol. 261, 231-238.
11. Leviev, I. G., Rodriguez-Fonseca, C., Phan, H., Garrett, R. A., Heilek, G., Noller, H. F. & Mankin, A. S. (1994). A conserved secondary structural motif in 23S rRNA defines the site of interaction of amicetin, a universal inhibitor of peptide bond formation. EMBO J. 13, 1682-1686.
12. Mankin, A. S. (1995). Selection for spontaneous and engineered mutations in the rRNA genes in halophilic archaea. In Archaea, A Laboratory Manual (Robb, F. T., Place, A. R., Sowers, K. R., Schreier, H. J., DasSarma, S. & Fleischmann, E. M., eds), pp. 209-216, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
13. Mankin, A. S. & Garrett, R. A. (1991). Chloramphenicol resistance mutations in the single 23 S rRNA gene of the archaeon Halobacterium halobium. J. Bacteriol. 173, 3559-3563.
14. Mankin, A. S. & Kagramanova, V. K. (1986). Complete nucleotide sequence of the single ribosomal RNA operon of Halobacterium halobium: secondary structure of the archaebacterial 23 S rRNA. Mol. Gen. Genet. 202, 152-161.
15. Mankin, A. S., Zyrianova, I. M., Kagramanova, V. K. & Garrett, R. A. (1992). Introducing mutations into the single-copy chromosomal 23S rRNA gene of the archaeon Halobacterium halobium by using an rRNA operon-based transformation system. Proc. Natl Acad. Sci. USA, 89, 6535-6539.
16. Mankin, A. S., Derckacheva, N. I., Leviev, I. G., Kagramanova, V. K., Forterre, P. & Garrett, R. A. (1994). Stable maintenance in halobacteria of plasmids harboring rDNA. Syst, Appl. Microbiol. 16, 672-679.
17. Moazed, D. & Noller, H. F. (1987). Chloramphenicol, erythromycin, carbomycin and vernamycin B protect overlapping sites in the peptidyl transferase region of 23S ribosomal RNA. Biochimie, 69, 879-884.
18. Moazed, D. & Noller, H. F. (1989). Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell, 57, 585-597.
19. Moazed, D. & Noller, H. F. (1991). Sites of interaction of the CCA end of peptidyl-tRNA with 23S rRNA. Proc. Natl Acad. Sci. USA, 88, 3725-3728.
20. Monro, R. E. & Marcker, K. A. (1967). Ribosome-catalyzed reaction of puromycin with a formylmethionine-containing oligonucleotide. J. Mol. Biol. 25, 347-350.
21. Monro, R. E., Celma, M. L. & Vazquez, D. (1969). Action of sparsomycin on ribosome-catalyzed peptidyl transfer. Nature, 222, 356-358.
22. Noller, H. F. (1984). Structure of ribosomal RNA. Annu. Rev. Biochem. 53, 119-162.
23. Noller, H. F. (1993). Peptidyl transferase: protein, ribonucleoprotein, or RNA? J. Bacteriol. 175, 5297-5300.
24. Noller, H. F., Hoffarth, V. & Zimniak, L. (1992). Unusual resistance of peptidyl transferase to protein extraction procedures. Science, 256, 1416-1419.
25. Samaha, R. R., Green, R. & Noller, H. F. (1995). A base-pair between tRNA and 23S rRNA in the peptidyl transferase center of the ribosome. Nature, 377, 309-314.
26. Sigmund, C. D. & Morgan, E. A. (1982). Erythromycin resistance due to mutation in a ribosomal RNA operon of Escherichia coli. Proc. Natl Acad. Sci. USA, 79, 5602-5606.
27. Stern, S., Moazed, D. & Noller, H. F. (1987). Analysis of RNA structure using chemical and enzymatic probing monitored by primer extension. Methods Enzymol. 164, 481-489.
28. Stoeckenius, W. & Kunau, W. H. (1968). Further characterization of particulate fractions from lysed cell envelopes of Halobacterium halobium and isolation of gas vacuole membranes. J. Cell. Biol. 38, 337-357.
29. Theocharis, D. A. & Coutsogeorgopoulos, C. (1992). Mechanism of action of sparsomycin in protein synthesis. Biochemistry, 31, 5861-5868.
30. van den Broek, L. A. G. M., Lázaro, E., Zylicz, Z., Fennis, P. J., Missler, F. A. N., Lelieveld, P., Garzotto, M., Wagener, D. J. T., Ballesta, J. P. G. & Ottenheijm, H. C. J. (1989). Lipophilic analogs of sparsomycin as strong inhibitors of protein synthesis and tumor growth: a structure-activity relationship study. J. Med. Chem. 32, 2002-2015.
31. Vazquez, D. (1979). Inhibitors of Protein Biosynthesis. Springer-Verlag, Berlin, Heidelberg, New York.