1887

Chapter 14 : Adventures with Frameshift Suppressor tRNAs

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Adventures with Frameshift Suppressor tRNAs, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816810/9781555815387_Chap14-1.gif /docserver/preview/fulltext/10.1128/9781555816810/9781555815387_Chap14-2.gif

Abstract:

During the 1960s it was established that the modified nucleosides present in tRNA and rRNA are synthesized after the primary transcript is made. To obtain tRNA lacking only one modified nucleoside, a mutant defective in the synthesis of one modified nucleoside is required. This paper inspired the author to use a transposon to obtain mutants defective in tRNA methylation. Using such a method, the author discovered the metabolic link between the synthesis of aromatic amino acids and the synthesis of uridine-5-oxyacetic acid (cmoU) and its methyl ester (mcmoU). Provided that the tRNA(mcmoU34)methyltransferase is a multimeric complex, poor translation termination mediated by a defective RF2 would extend the CmoA peptide, making it unable to form a potential complex required for the tRNA(mcmo5U34)methyltransferase activity. The as well as and mutants have suppressor specificity similar to that induced by and . It later emerged that these mutants each contain mutations in two genes: and . The mutants contain the and mutations; mutants, the and mutations; and the mutant, the and mutations. The frameshift tRNA suppressors isolated more than 30 years ago in the laboratory of John Roth have clearly been important tools to study how the ribosome maintains the reading frame. Recent analyses using this collection of frameshift suppressor mutants have revealed new facts of the operational mechanism behind this important and conserved feature of translation.

Citation: Björk G. 2011. Adventures with Frameshift Suppressor tRNAs, p 131-140. In Maloy S, Hughes K, Casadesús J (ed), The Lure of Bacterial Genetics. ASM Press, Washington, DC. doi: 10.1128/9781555816810.ch14

Key Concept Ranking

Aromatic Amino Acids
0.47717014
Frameshift Mutation
0.4768694
Amino Acid Synthesis
0.4576408
Sodium Dodecyl Sulfate
0.4551175
0.47717014
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Synthesis of cmoU34 and its methyl ester mcmoU34 and the link to the synthesis of aromatic amino acids and vitamins ( ). Gray arrows indicate the link between chorismic acid (or an unknown derivative of it) and different steps in the synthesis of cmoU. CmoA possesses an AdoMet binding site. It is likely to be an AdoMet-dependent methyltransferase. Since only one of the carbon atoms in cmoU originates from Met ( ), the CmoA polypeptide may be part of a complex also mediating the formation of the methylester (mcmoU) of cmoU.

Citation: Björk G. 2011. Adventures with Frameshift Suppressor tRNAs, p 131-140. In Maloy S, Hughes K, Casadesús J (ed), The Lure of Bacterial Genetics. ASM Press, Washington, DC. doi: 10.1128/9781555816810.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

(A) The genetic code. The shaded codon boxes are the family codon boxes, which contain four codons representing one amino acid. The six family codon boxes in the lighter shade contain tRNAs having cmoU or mcmoU as the wobble nucleoside. The codon boxes with a white background are the mixed codon boxes. (B) The proline family codon box (CCN). and denote the genes encoding , , and , respectively, and the wobble nucleoside, which is present in position 34, is indicated. The circles correspond to the codon read by a tRNA, and a line connecting two or more circles indicates that the same tRNA reads those codons (e.g., the contains G34 as the wobble nucleoside and reads the CCC and CCU codons). The black circles show the codon reading abilities predicted by the wobble hypothesis ( ) and the revised wobble rules ( ). The gray circle for (codon CCC) indicates that this tRNA reads CCC codons provided that cmoU is present ( ). The , having hoU instead of cmoU as the wobble nucleoside, reads this codon and also CCU less efficiently than the fully modified tRNA as judged by adequate growth rate comparisons ( ). Even in the presence of and , hoU instead of cmoU in the reduces the A-site selection at the CCC codon but not at the CCU codon ( ). Thus, in cells having a normal Pro-tRNA population, the presence of cmoU34 is important for decoding CCC. This is most likely also true for a tRNA having U as the wobble nucleoside, which some of the tRNAs might have in an mutant ( ). (Adapted from reference .)

Citation: Björk G. 2011. Adventures with Frameshift Suppressor tRNAs, p 131-140. In Maloy S, Hughes K, Casadesús J (ed), The Lure of Bacterial Genetics. ASM Press, Washington, DC. doi: 10.1128/9781555816810.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Three models showing how a defective tRNA induces frameshifting in the P-site. (A) The defective tRNA (indicated by a gray diamond) is too slow (indicated by a broken line) in entering the A-site, allowing a third position mismatched tRNA (depicted by a black bar at the wobble position) to decode the A-site codon. After a normal three-nucleotide translocation to the P-site, the third position mismatched tRNA is prone to slip into an overlapping reading frame. (B) The defective tRNA (indicated by a gray diamond) decodes the codon in the A-site, but once it has been translocated into the P-site it may slip on the mRNA. (C) The defective tRNA (indicated by a gray diamond) is too slow (indicated by a broken line) in entering the A-site, providing a pause that allows the cognate P-site tRNA to slip. Broken arrows indicate a slow entry into the +1 frame compared to continued reading in the zero frame. The original (zero) reading frame is indicated in the mRNA with alternating black and gray triplets. “Defective” can either indicate alterations in the primary sequence or hypo-modification of the tRNA. (Reprinted from reference with permission from Elsevier.)

Citation: Björk G. 2011. Adventures with Frameshift Suppressor tRNAs, p 131-140. In Maloy S, Hughes K, Casadesús J (ed), The Lure of Bacterial Genetics. ASM Press, Washington, DC. doi: 10.1128/9781555816810.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816810.ch14
1. Atkins, J. F.,and, G. R. Björk. 2009. A gripping tale of ribosomal frameshifting: extragenic suppressors of frameshift mutations spotlight P-site realignment. Microbiol. Mol. Biol. Rev., 73:178210.
2. Atkins, J. F.,and, S. Ryce. 1974. UGA and non-triplet suppressor reading of the genetic code. Nature 249:527530.
3. Ball, C. B.,, M. D. Mendenhall,, M. G. Sand-baken, and , M. R. Culbertson. 1988. The yeast SUF5 frameshift suppressor encodes a mutant glycine tRNA(CCC). Nucleic Acids Res. 16:8712.
4. Björk, G. R. 1980. A novel link between the biosynthesis of aromatic amino acids and transfer RNA modification in Escherichia coli. J. Mol. Biol. 140:391410.
5. Björk, G. R.,and, L. A. Isaksson. 1970. Isolation of mutants of Escherichia coli lacking 5-methyluracil in transfer ribonucleic acid or 1-methylguanine in ribosomal RNA. J. Mol. Biol. 51:83100.
6. Bossi, L.,, T. Kohno, and , J. R. Roth. 1983. Genetic characterization of the sufJ frameshift suppressor in Salmonella typhimurium. Genetics 103:3142.
7. Bossi, L.,and, J. R. Roth. 1981. Four-base codons ACCA, ACCU and ACCC are recognized by frameshift suppressor sufJ. Cell 25:489496.
8. Chen, P.,, P. F. Crain,, S. J. Näsvall,, S. C. Pomerantz, and, G. R. Björk. 2005. A “gain of function” mutation in a protein mediates production of novel modified nucleosides. EMBO J 24:18421851.
9. Crick, F. H. C. 1966. Codon-anticodon pairing. The wobble hypothesis. J. Mol. Biol. 19:548555.
10. Fleissner, E.,and, E. Borek. 1962. A new enzyme of RNA synthesis: RNA methylase. Proc. Natl. Acad. Sci. USA 48:11991203.
11. Hagervall, T. G.,, Y. H. Jönsson,, C. G. Edmonds,, J. A. McCloskey, and , G. R. Björk. 1990. Chorismic acid, a key metabolite in modification of tRNA.J. Bacteriol. 172:252259.
12. Kawakami, K.,, Y. H. Jönsson,, G. R. Björk,, H. Ikeda, and , Y. Nakamura. 1988. Chromosomal location and structure of the operon encoding peptide-chain-release factor 2 of Escherichia coli. Proc. Natl. Acad. Sci. USA 85:56205624.
13. Kleckner, N.,, J. Roth, and , D. Botstein. 1977. Genetic engineering in vivo using translocatable drug-resistance elements. New methods in bacterial genetics. J. Mol. Biol. 116:125159.
14. Kohno, T.,, L. Bossi, and , J. R. Roth. 1983. New suppressors of frameshift mutations in Salmonella typhimurium. Genetics 103:2329.
15. Kohno, T.,and, J. R. Roth. 1978. A Salmonella frameshift suppressor that acts at runs of A residues in the messenger RNA. J. Mol. Biol. 126:3752.
16. Leipuviene, R.,and, G. R. Björk. 2005. A reduced level of charged triggers the wild-type peptidyl-tRNA to frameshift. RNA 11:796807.
17. Li, J. N.,and, G. R. Björk. 1999. Structural alterations of the tRNA(m1G37)methyltransferase from Salmonella typhimurium affect tRNA substrate specificity. RNA 5:395408.
18. Li, J. N.,, B. Esberg,, J. F. Curran, and , G. R. Björk. 1997. Three modified nucleosides present in the anticodon stem and loop influence the in vivo aa-tRNA selection in a tRNA-dependent manner. J. Mol. Biol. 271:209221.
19. Mendenhall, M. D.,and, M. R. Culbertson. 1988. The yeast SUF3 frameshift suppressor encodes a mutant glycine tRNA(CCC). Nucleic Acids Res. 16:8713.
20. Näsvall, S. J.,, P. Chen, and , G. R. Björk. 2004. The modified wobble nucleoside uridine-5-oxy-acetic acid in promotes reading of all four proline codons in vivo. RNA 10:16621673.
21. Näsvall, S. J.,, P. Chen, and , G. R. Björk. 2007. The wobble hypothesis revisited: uridine-5-oxyacetic acid is critical for reading of G-ending codons. RNA 13:21512164.
22. Näsvall, S. J.,, K. Nilsson, and , G. R. Björk. 2009. The ribosomal grip of the peptidyl-tRNA is critical for reading frame maintenance. J. Mol. Biol. 385:350367.
23. Newmark, R. A.,and, C. R. Cantor. 1968. Nuclear magnetic resonance study of the interactions of guanosine and cytidine in dimethyl sulfoxide. J. Am. Chem. Soc. 90:50105017.
24. O’Connor, M. 2002. Insertions in the anticodon loop of and tRNALys promote quadruplet decoding of CAAA. Nucleic Acids Res. 30:19851990.
25. Pope, W. T.,, A. Brown, and , R. H. Reeves. 1978. The identification of the tRNA substrates for the supK tRNA methylase. Nucleic Acids Res. 5:10411057.
26. Pope, W. T.,and, R. H. Reeves. 1978. Purification and characterization of a tRNA methylase from Salmonella typhimurium. J. Bacteriol. 136:191200.
27. Qian, Q.,and, G. R. Björk. 1997. Structural alterations far from the anticodon of the tRNA ProQQG of Salmonella typhimurium induce + 1 frameshifting at the peptidyl-site. J. Mol. Biol. 273:978992.
28. Qian, Q.,, J. N. Li,, H. Zhao,, T. G. Hagervall,, P. J. Farabaugh, and , G. R. Björk. 1998. A new model for phenotypic suppression of frameshift mutations by mutant tRNAs. Mol. Cell 1:471482.
29. Reeves, R.,and, J. Roth. 1971. A recessive UGA suppressor. J. Mol. Biol. 56:523533.
30. Reeves, R.,and, J. Roth. 1975. Transfer ribo-nucleic acid methylase deficiency found in UGA suppressor strains. J. Bacteriol. 124:332340.
31. Riddle, D.,and, J. Carbon. 1973. Frameshift suppression: a nucleotide addition in the anticodon of a glycine transfer RNA. Nature 242:230234.
32. Riddle, D.,and, J. Roth. 1970. Suppressors of frameshift mutations in Salmonella typhimurium. J. Mol. Biol. 54:131144.
33. Riddle, D.,and, J. Roth. 1972. Frameshift suppressors. II. Genetic mapping and dominance studies. J. Mol. Biol. 66:483493.
34. Riddle, D.,and, J. Roth. 1972. Frameshift suppressors. III. Effects of suppressor mutations on transfer RNA. J. Mol. Biol. 66:495506.
35. Sanderson, K.,and, J. Hurley. 1987. Linkage map of Salmonella typhimurium, p. 877918. In F. C. Neidhardt,, J. L. Ingraham,, K. B. Low,, B. Magasanik,, M. Schaechter, and , H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology. American Society for Microbiology, Washington, DC.
36. Sroga, G. E.,, F. Nemoto,, Y. Kuchino, and , G. R. Björk. 1992. Insertion (sufB) in the anticodon loop or base substitution (sufC) in the anticodon stem of from Salmonella typhimurium induces suppression of frameshift mutations. Nucleic Acids Res. 20:34633469.
37. Svensson, I.,, H. G. Boman,, K. G. Eriksson, and , K. Kjellin. 1963. Studies on microbial RNA. I. Transfer of methyl groups from methionine to soluble RNA from Escherichia coli. J. Mol. Biol. 7:254271.
38. Weiss, R. B.,, D. M. Dunn,, J. F. Atkins, and , R. F. Gesteland. 1990. Ribosomal frameshifting from −2 to +50 nucleotides. Prog. Nucleic Acid Res. Mol. Biol. 39:159183.
39. Wolfe, M. D.,, F. Ahmed,, G. M. Lacourciere,, C. T. Lauhon,, T. C. Stadtman, and , T. J. Larson. 2004. Functional diversity of the rhodanese homology domain: the Escherichia coli ybbB gene encodes a selenophosphate-dependent tRNA 2-selenouridine synthase. J. Biol. Chem. 279:18011809.
40. Yokoyama, S.,and, S. Nishimura. 1995. Modified nucleosides and codon recognition, p. 207223. In D. Söll and , U. L. Rajbhandary (ed.), tRNA: Structure, Biosynthesis, and Function. ASM Press, Washington, DC.
41. Yourno, J.,and, S. Tanemura. 1970. Restoration of in-phase translation by an unlinked suppressor of a frameshift mutation in Salmonella typhimurium. Nature 225:422426.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error