1887

Microbiology Society logo

Volume 152, Issue 12

tRNA-dependent cleavage of the ColE1 plasmid-encoded RNA I Free

Abstract

Effects of tRNA(UGC) and its derivative devoid of the 3′-ACCA motif [tRNA(UGC)ΔACCA] on the cleavage of the ColE1-like plasmid-derived RNA I were analysed and . In an amino-acid-starved mutant, in which uncharged tRNAs occur in large amounts, three products of specific cleavage of RNA I were observed, in contrast to an otherwise isogenic host. Overexpression of tRNA(UGC), which under such conditions occurs in mostly in an uncharged form, induced RNA I cleavage and resulted in an increase in ColE1-like plasmid DNA copy number. Such effects were not observed during overexpression of the 3′-ACCA-truncated tRNA(UGC). Moreover, tRNA(UGC), but not tRNA(UGC)ΔACCA, caused RNA I cleavage in the presence of MgCl. These results strongly suggest that tRNA-dependent RNA I cleavage occurs in ColE1-like plasmid-bearing , and demonstrate that tRNA(UGC) participates in specific degradation of RNA I and . This reaction is dependent on the presence of the 3′-ACCA motif of tRNA(UGC).

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29134-0
2006-12-01
2023-04-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/12/3467.html?itemId=/content/journal/micro/10.1099/mic.0.29134-0&mimeType=html&fmt=ahah

References

  1. Been M. D, Wickham G. S. 1997; Self-cleaving ribozymes of hepatitis delta virus RNA. Eur J Biochem 247:741–753 [CrossRef]
     [Google Scholar]
  2. Behlke M. A. 2006; Progress towards in vivo use of siRNAs. Mol Ther 13:644–670 [CrossRef]
     [Google Scholar]
  3. Binnie U, Wong K, McAteer S, Masters M. 1999; Absence of RNase III alters the pathway by which RNA I, the antisense inhibitor of ColE1 replication, decays. Microbiology 145:3089–3100
     [Google Scholar]
  4. Birikh K. R, Heaton P. A, Eckstein F. 1997; The structure, function and application of the hammerhead ribozyme. Eur J Biochem 245:1–16 [CrossRef]
     [Google Scholar]
  5. Cashel M, Gentry D. R, Hernandez V. J, Vinella D. others 1996; The stringent response. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp.  1458–1496 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  6. Cayama E, Yepez A, Rotondo F, Bandeira E, Ferreras A. C, Triana-Alonso F. J. 2000; New chromatographic and biochemical strategies for quick preparative isolation of tRNA. Nucleic Acids Res 28:e64 [CrossRef]
     [Google Scholar]
  7. Cesareni G, Helmer-Citterich M, Castagnoli L. 1991; Control of ColE1 plasmid replication by antisense RNA. Trends Genet 7:230–235 [CrossRef]
     [Google Scholar]
  8. Chatterji D, Ojha A. K. 2001; Revisiting the stringent response, ppGpp and starvation signaling. Curr Opin Microbiol 4:160–165 [CrossRef]
     [Google Scholar]
  9. Chatwin H. M, Summers D. K. 2001; Monomer-dimer control of the ColE1 P(cer) promoter. Microbiology 147:3071–3081
     [Google Scholar]
  10. Collins R. A. 2002; The Neurospora Varkud satellite ribozyme. Biochem Soc Trans 30:1122–1126
     [Google Scholar]
  11. Dittmar K. A, Mobley E. M, Radek A. J, Pan T. 2004; Exploring the regulation of tRNA distribution on the genomic scale. J Mol Biol 337:31–47 [CrossRef]
     [Google Scholar]
  12. Doi N, Zenno S, Ueda R, Ohki-Hamazaki H, Ui-Tei K, Saigo K. 2003; Short-interfering-RNA-mediated gene silencing in mammalian cells requires Dicer and eIF2C translation initiation factors. Curr Biol 13:41–46 [CrossRef]
     [Google Scholar]
  13. Dorsett Y, Tuschl T. 2004; siRNAs: applications in functional genomics and potential as therapeutics. Nat Rev Drug Discov 3:318–329 [CrossRef]
     [Google Scholar]
  14. Doudna J. A, Cech T. R. 2002; The chemical repertoire of natural ribozymes. Nature 418:222–228 [CrossRef]
     [Google Scholar]
  15. Fedor M. J. 2000; Structure and function of the hairpin ribozyme. J Mol Biol 297:269–291 [CrossRef]
     [Google Scholar]
  16. Fedor M. J. 2002; The role of metal ions in RNA catalysis. Curr Opin Struct Biol 12:289–295 [CrossRef]
     [Google Scholar]
  17. Fedor M. J, Williamson J. R. 2005; The catalytic diversity of RNAs. Nat Rev Mol Cell Biol 6:399–412
     [Google Scholar]
  18. Fiil N, Friesen J. D. 1968; Isolation of “relaxed” mutants of Escherichia coli . J Bacteriol 95:729–731
     [Google Scholar]
  19. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. 1983; The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–857 [CrossRef]
     [Google Scholar]
  20. He L, Wagner E. G. H, Binnie U, Binns N, Masters M, Söderbom F. 1993; PcnB is required for the rapid degradation of RNA I, the antisense RNA that controls the copy number of ColE1-related plasmids. Mol Microbiol 9:1131–1142 [CrossRef]
     [Google Scholar]
  21. Hoagland M. B, Stephenson M. L, Scott J. F, Hecht L. I, Zamecnik P. C. 1958; A soluble ribonucleic acid intermediate in protein synthesis. J Biol Chem 231:241–257
     [Google Scholar]
  22. Jacquier A. 1996; Group II introns: elaborate ribozymes. Biochimie 78:474–487 [CrossRef]
     [Google Scholar]
  23. Jasiecki J, Węgrzyn G. 2003; Growth-rate dependent RNA polyadenylation in Escherichia coli . EMBO Rep 4:172–177 [CrossRef]
     [Google Scholar]
  24. Jasiecki J, Węgrzyn G. 2006; Transcription start sites in the promoter region of the Escherichia coli pcnB (plasmid copy number) gene coding for poly(A) polymerase I. Plasmid 55:169–172 [CrossRef]
     [Google Scholar]
  25. Kim D, Rhee Y, Rhodes D, Sharma V, Sorenson O, Greener A, Smider V. 2005a; Directed evolution and identification of control regions of ColE1 plasmid replication origins using only nucleotide deletions. J Mol Biol 351:763–775 [CrossRef]
     [Google Scholar]
  26. Kim J, Jung J. H, Reyes J. L. 9 other authors 2005b; microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42:84–94 [CrossRef]
     [Google Scholar]
  27. Kruger K, Grabowski P. J, Zaug A. J, Sands J, Gottschling D. E, Cech T. R. 1982; Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena . Cell 31:147–157 [CrossRef]
     [Google Scholar]
  28. Kues U, Stahl U. 1989; Replication of plasmids in gram-negative bacteria. Microbiol Rev 53:491–516
     [Google Scholar]
  29. Lee Y. S, Nakahara K, Pham J. W, Kim K, He Z, Sontheimer E. J, Carthew R. W. 2004; Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117:69–81 [CrossRef]
     [Google Scholar]
  30. Lilley D. M. J. 1999; Structure, folding and catalysis of the small nucleolytic ribozymes. Curr Opin Struct Biol 9:330–338 [CrossRef]
     [Google Scholar]
  31. Lin-Chao S, Cohen S. N. 1991; The rate of processing and degradation of antisense RNA I regulates the replication of ColE1-type plasmids in vivo. Cell 65:1233–1242 [CrossRef]
     [Google Scholar]
  32. Lopilato J, Bortner S, Beckwith J. 1986; Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB , reduce plasmid copy number of pBR322 and its derivatives. Mol Gen Genet 205:285–290 [CrossRef]
     [Google Scholar]
  33. Marquet R, Isel C, Ehresmann C, Ehresmann B. 1995; tRNAs as primer of reverse transcriptases. Biochimie 77:113–124 [CrossRef]
     [Google Scholar]
  34. Misra V. K, Draper D. E. 2002; The linkage between magnesium binding and RNA folding. J Mol Biol 317:507–521 [CrossRef]
     [Google Scholar]
  35. Polisky B. 1988; ColE1 replication control circuitry: sense from antisense. Cell 55:929–932 [CrossRef]
     [Google Scholar]
  36. Ronemus M, Vaughn M. W, Martienssen R. A. 2006; MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis . Plant Cell 18:1559–1574 [CrossRef]
     [Google Scholar]
  37. Sago N, Omi K, Tamura Y, Kunugi H, Toyo-oka T, Tokunaga K, Hohjoh H. 2004; RNAi induction and activation in mammalian muscle cells where Dicer and eIF2C translation initiation factors are barely expressed. Biochem Biophys Res Commun 319:50–57 [CrossRef]
     [Google Scholar]
  38. Sambrook J, Fritsch E. F, Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  39. Schmidt U, Budde E, Stahl U. 1992; Self-splicing of a mitochondrial group I intron from the cytochrome b gene of the ascomycete Podospora anserina . Mol Gen Genet 233:71–80 [CrossRef]
     [Google Scholar]
  40. Sharpe M. E, Chatwin H. M, Macpherson C, Withers H. L, Summers D. K. 1999; Analysis of the ColE1 stability determinant Rcd. Microbiology 145:2135–2144 [CrossRef]
     [Google Scholar]
  41. Shen B, Goodman H. M. 2004; Uridine addition after microRNA-directed cleavage. Science 306:997 [CrossRef]
     [Google Scholar]
  42. Sorensen M. A. 2001; Charging levels of four tRNA species in Escherichia coli Rel+ and Rel− strains during amino acid starvation: a simple model for the effect of ppGpp on translational accuracy. J Mol Biol 307:785–798 [CrossRef]
     [Google Scholar]
  43. Sorensen M. A, Elf J, Bouakaz E, Tenson T, Sanyal S, Bjork G. R, Ehrenberg M. 2005; Over expression of a tRNALeu isoacceptor changes charging pattern of leucine tRNAs and reveals new codon reading. J Mol Biol 354:16–24 [CrossRef]
     [Google Scholar]
  44. Tanner N. K. 1999; Ribozymes: the characteristics and properties of catalytic RNAs. FEMS Microbiol Rev 23:257–275 [CrossRef]
     [Google Scholar]
  45. Tomizawa J. 1990; Control of ColE1 plasmid replication. Intermediates in the binding of RNA I and RNA II. J Mol Biol 212:683–694 [CrossRef]
     [Google Scholar]
  46. Valencia-Sanchez M. A, Liu J, Hannon G. J, Parker R. 2006; Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20:515–524 [CrossRef]
     [Google Scholar]
  47. Wagner E. G. H, Simons R. W. 1994; Antisense RNA control in bacteria, phage and plasmids. Annu Rev Microbiol 48:713–742 [CrossRef]
     [Google Scholar]
  48. Wang Z, Le G, Shi Y, Węgrzyn G. 2001; Medium design for plasmid DNA production based on stoichiometric model. Process Biochem 36:1085–1093 [CrossRef]
     [Google Scholar]
  49. Wang Z, Le G, Shi Y, Węgrzyn G, Wróbel B. 2002; A model for regulation of ColE1-like plasmid replication by uncharged tRNAs in amino acid-starved Escherichia coli cells. Plasmid 47:69–78 [CrossRef]
     [Google Scholar]
  50. Wang Z, Yuan Z, Hengge U. R. 2004; Processing of plasmid DNA with ColE1-like replication origin. Plasmid 51:149–161 [CrossRef]
     [Google Scholar]
  51. Wang Z, Xiang L, Shao J, Yuan Z. 2006; The 3′ CCACCA sequence of tRNAAla(UGC) is the motif that is important in inducing Th1-like immune response, and this motif can be recognized by Toll-like receptor 3. Clin Vaccine Immunol 13:733–739 [CrossRef]
     [Google Scholar]
  52. Węgrzyn G. 1999; Replication of plasmids during bacterial response to amino acid starvation. Plasmid 41:1–16 [CrossRef]
     [Google Scholar]
  53. Wong E. M, Polisky B. 1985; Alternative conformations of the ColE1 replication primer modulate its interaction with RNA I. Cell 42:959–966 [CrossRef]
     [Google Scholar]
  54. Wróbel B, Węgrzyn G. 1997; Differential amplification efficiency of pMB1 and p15A (ColE1-type) replicons in Escherichia coli stringent and relaxed strains starved for particular amino acids. Microbiol Res 152:251–255 [CrossRef]
     [Google Scholar]
  55. Wróbel B, Węgrzyn G. 1998; Replication regulation of ColE1-like plasmids in amino acid-starved Escherichia coli . Plasmid 39:48–62 [CrossRef]
     [Google Scholar]
  56. Xu F, Cohen S. N. 1995; RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature 374:180–183 [CrossRef]
     [Google Scholar]
  57. Xu F, Lin-Chao S, Cohen S. N. 1993; The Escherichia coli pcnB gene promotes adenylation of antisense RNA I of ColE1-type plasmids in vivo and degradation of RNA I decay intermediates. Proc Natl Acad Sci U S A 90:6756–6760 [CrossRef]
     [Google Scholar]
  58. Yekta S, Shih I. H, Bartel D. P. 2004; MicroRNA-directed cleavage of HOXB8 mRNA. Science 304:594–596 [CrossRef]
     [Google Scholar]
  59. Zeng Y, Yi R, Cullen B. R. 2003; MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci U S A 100:9779–9784 [CrossRef]
     [Google Scholar]
  60. Zhang H, Kolb F. A, Brondani V, Billy E, Filipowicz W. 2002; Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J 21:5875–5885 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29134-0
Loading
tRNA-dependent cleavage of the ColE1 plasmid-encoded RNA I
Microbiology 152, 3467 (2006); https://doi.org/10.1099/mic.0.29134-0
/content/journal/micro/10.1099/mic.0.29134-0
/content/journal/micro/10.1099/mic.0.29134-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error