The SmpB-tmRNA tagging system plays important roles in streptomyces coelicolor growth and development

PLoS ONE

Volumn 4, Issue 2, 2009, Pages

  Yang, Chunzhong ^a   Glover, John R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA; PROTEIN SMPB; PROTEIN SSRA; PROTEIN TAG; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL SURVIVAL; CODON; CONTROLLED STUDY; COSMID VECTOR; GENE AMPLIFICATION; GENE DISRUPTION; GENE SEQUENCE; MUTAGENESIS; NONHUMAN; OPEN READING FRAME; PLASMID; PROTEIN ANALYSIS; PROTEIN DEGRADATION; REPLICON; RNA DEGRADATION; SPOROGENESIS; STREPTOMYCES COELICOLOR; TEMPERATURE SENSITIVITY;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84887212377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004459     Document Type: Article

References (60)

1. Karzai AW, Roche ED, Sauer RT (2000) The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat Struct Biol 7: 449-455.
2. Withey JH, Friedman DI (2003) A salvage pathway for protein structures: tmRNA and trans-translation. Annu Rev Microbiol 57: 101-123.
3. Wower J, Wower IK, Kraal B, Zwieb CW (2001) Quality control of the elongation step of protein synthesis by tmRNP. J Nutr 131: 2978S-2982S.
4. Gottesman S, Roche E, Zhou Y, Sauer RT (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12: 1338-1347.
5. Richards J, Mehta P, Karzai AW (2006) RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol Microbiol 62: 1700-1712.
6. Abo T, Inada T, Ogawa K, Aiba H (2000) SsrA-mediated tagging and proteolysis of LacI and its role in the regulation of lac operon. EMBO J 19: 3762-3769.
7. Keiler KC, Waller PR, Sauer RT (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271: 990-993.
8. Collier J, Binet E, Bouloc P (2002) Competition between SsrA tagging and translational termination at weak stop codons in Escherichia coli. Mol Microbiol 45: 745-754.
9. Hayes CS, Bose B, Sauer RT (2002) Proline Residues at the C Terminus of Nascent Chains Induce SsrA Tagging during Translation Termination. J Biol Chem 277: 33825-33832.
10. Roche ED, Sauer RT (1999) SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity. EMBO J 18: 4579-4589.
11. Withey J, Friedman D (1999) Analysis of the role of trans-translation in the requirement of tmRNA for λimmP22 growth in Escherichia coli. J Bacteriol 181: 2148-2157.
12. Muto A, Fujihara A, Ito KI, Matsuno J, Ushida C, et al. (2000) Requirement of transfer-messenger RNA for the growth of Bacillus subtilis under stresses. Genes Cells 5: 627-635.
13. de la Cruz J, Vioque A (2001) Increased sensitivity to protein synthesis inhibitors in cells lacking tmRNA. RNA 7: 1708-1716.
14. Luidalepp H, Hallier M, Felden B, Tenson T (2005) tmRNA decreases the bactericidal activity of aminoglycosides and the susceptibility to inhibitors of cell wall synthesis. RNA Biol 2: 70-74.
15. Huang C, Wolfgang MC, Withey J, Koomey M, Friedman DI (2000) Charged tmRNA but not tmRNA-mediated proteolysis is essential for Neisseria gonorrhoeae viability. EMBO J 19: 1098-1107.
16. Leskiw BK, Bibb MJ, Chater KF (1991) The use of a rare codon specifically during development? Mol Microbiol 5: 2861-2867.
17. Leskiw BK, Lawlor EJ, Fernandez-Abalos JM, Chater KF (1991) TTA codons in some genes prevent their expression in a class of developmental, antibiotic-negative, Streptomyces mutants. Proc Natl Acad Sci U S A 88: 2461-2465.
18. Li W, Wu J, Tao W, Zhao C, Wang Y, et al. (2007) A genetic and bioinformatic analysis of Streptomyces coelicolor genes containing TTA codons, possible targets for regulation by a developmentally significant tRNA. FEMS Microbiol Lett 266: 20-28.
19. Fernandez-Moreno MA, Caballero JL, Hopwood DA, Malpartida F (1991) The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell 66: 769-780.
20. Guthrie EP, Flaxman CS, White J, Hodgson DA, Bibb MJ, et al. (1998) A response-regulator-like activator of antibiotic synthesis from Streptomyces coelicolor A3(2) with an amino-terminal domain that lacks a phosphorylation pocket. Microbiology 144(Pt 3): 727-738.
21. Takano E, Tao M, Long F, Bibb MJ, Wang L, et al. (2003) A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol Microbiol 50: 475-486.
22. Anne J, Van Mellaert L (1993) Streptomyces lividans as host for heterologous protein production. FEMS Microbiol Lett 114: 121-128.
23. Binnie C, Cossar JD, Stewart DI (1997) Heterologous biopharmaceutical protein expression in Streptomyces. Trends Biotechnol 15: 315-320s.
24. Brawner M, Poste G, Rosenberg M, Westpheling J (1991) Streptomyces: a host for heterologous gene expression. Curr Opin Biotechnol 2: 674-681.
25. Braud S, Lavire C, Bellier A, Mazodier P (2006) Effect of SsrA (tmRNA) tagging system on translational regulation in Streptomyces. Arch Microbiol 184: 343-352.
26. Wiegert T, Schumann W (2001) SsrA-mediated tagging in Bacillus subtilis. J Bacteriol 183: 3885-3889.
27. Chater KF, Chandra G (2008) The use of the rare UUA codon to define "expression space" for genes involved in secondary metabolism, development and environmental adaptation in streptomyces. J Microbiol 46: 1-11.
28. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, et al. (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49.
29. Muth G, Nussbaumer B, Wholleben W, Puhler A (1989) A vector system with temperature-sensitive replication for gene disruption and mutational cloning in Streptomycetes. Mol Gen Genet 219: 341-348.
30. Blondelet-Rouault MH, Weiser J, Lebrihi A, Branny P, Pernodet JL (1997) Antibiotic resistance gene cassettes derived from the Ω interposon for use in E coli and Streptomyces. Gene 190: 315-317.
31. Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100: 1541-1546.
32. Moore SD, Sauer RT (2005) Ribosome rescue: tmRNA tagging activity and capacity in Escherichia coli. Mol Microbiol 58: 456-466.
33. Roche ED, Sauer RT (2001) Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons. J Biol Chem 276: 28509-28515.
34. Kisselev L, Ehrenberg M, Frolova L (2003) Termination of translation: interplay of mRNA, rRNAs and release factors? EMBO J 22: 175-182.
35. Hayes CS, Sauer RT (2003) Cleavage of the A site mRNA codon during ribosome pausing provides a mechanism for translational quality control. Mol Cell 12: 903-911.
36. Sunohara T, Jojima K, Tagami H, Inada T, Aiba H (2004) Ribosome stalling during translation elongation induces cleavage of mRNA being translated in Escherichia coli. J Biol Chem 279: 15368-15375.
37. Li X, Hirano R, Tagami H, Aiba H (2006) Protein tagging at rare codons is caused by tmRNA action at the 3′ end of nonstop mRNA generated in response to ribosome stalling. RNA 12: 248-255.
38. Mehta P, Richards J, Karzai AW (2006) tmRNA determinants required for facilitating nonstop mRNA decay. RNA 12: 2187-2198.
39. Yamamoto Y, Sunohara T, Jojima K, Inada T, Aiba H (2003) SsrA-mediated trans-translation plays a role in mRNA quality control by facilitating degradation of truncated mRNAs. Rna 9: 408-418.
40. Abe T, Sakaki K, Fujihara A, Ujiie H, Ushida C, et al. (2008) tmRNA-dependent trans-translation is required for sporulation in Bacillus subtilis. Mol Microbiol 69: 1491-1498.
41. Hallier M, Ivanova N, Rametti A, Pavlov M, Ehrenberg M, et al. (2004) Pre-binding of small protein B to a stalled ribosome triggers trans-translation. J Biol Chem 279: 25978-25985.
42. Hanawa-Suetsugu K, Takagi M, Inokuchi H, Himeno H, Muto A (2002) SmpB functions in various steps of trans-translation. Nucleic Acids Res 30: 1620-1629.
43. Keiler KC, Shapiro L (2003) tmRNA in Caulobacter crescentus is cell cycle regulated by temporally controlled transcription and RNA degradation. J Bacteriol 185: 1825-1830.
44. Moore SD, Sauer RT (2007) The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 76: 101-124.
45. Spiers A, Lamb HK, Cocklin S, Wheeler KA, Budworth J, et al. (2002) PDZ domains facilitate binding of high temperature requirement protease A (HtrA) and tail-specific protease (Tsp) to heterologous substrates through recognition of the small stable RNA A (ssrA)-encoded peptide. J Biol Chem 277: 39443-39449.
46. Choy JS, Aung LL, Karzai AW (2007) Lon protease degrades transfer-messenger RNA-tagged proteins. J Bacteriol 189: 6564-6571.
47. de Crecy-Lagard V, Servant-Moisson P, Viala J, Grandvalet C, Mazodier P (1999) Alteration of the synthesis of the Clp ATP-dependent protease affects morphological and physiological differentiation in Streptomyces. Mol Microbiol 32: 505-517.
48. Viala J, Mazodier P (2003) The ATPase ClpX is conditionally involved in the morphological differentiation of Streptomyces lividans. Mol Genet Genomics 268: 563-569.
49. Viala J, Rapoport G, Mazodier P (2000) The clpP multigenic family in Streptomyces lividans: conditional expression of the clpP3 clpP4 operon is controlled by PopR, a novel transcriptional activator. Mol Microbiol 38: 602-612.
50. Leskiw BK, Mah R, Lawlor EJ, Chater KF (1993) Accumulation of bldA-specified tRNA is temporally regulated in Streptomyces coelicolor A3(2). J Bacteriol 175: 1995-2005.
51. Kataoka M, Kosono S, Tsujimoto G (1999) Spatial and temporal regulation of protein expression by bldA within a Streptomyces lividans colony. FEBS Lett 462: 425-429.
52. Hesketh A, Bucca G, Laing E, Flett F, Hotchkiss G, et al. (2007) New pleiotropic effects of eliminating a rare tRNA from Streptomyces coelicolor, revealed by combined proteomic and transcriptomic analysis of liquid cultures. BMC Genomics 8: 261.
53. Chandra G, Chater KF (2008) Evolutionary flux of potentially bldA-dependent Streptomyces genes containing the rare leucine codon TTA. Antonie Van Leeuwenhoek 94: 111-126.
54. Nguyen KT, Tenor J, Stettler H, Nguyen LT, Nguyen LD, et al. (2003) Colonial differentiation in Streptomyces coelicolor depends on translation of a specific codon within the adpA gene. J Bacteriol 185: 7291-7296.
55. Hopwood DA, Lydiate DJ, Malpartida F, Wright HM (1985) Conjugative sex plasmids of Streptomyces. Basic Life Sci 30: 615-634.
56. Chater KF, Bruton CJ, King AA, Suarez JE (1982) The expression of Streptomyces and Escherichia coli drug-resistance determinants cloned into the Streptomyces phage phi C31. Gene 19: 21-32.
57. Ni SX, Cossar D, Man A, Norek K, Miller D, et al. (2003) Purification and characterization of recombinant Streptomyces griseus aminopeptidase. Protein Expr Purif 30: 62-68.
58. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces Genetics. Colney, Norwich, UK: The John Innes Foundation.
59. Harlow E, Lane D (1999) Using antibodies: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Sambrook J, Russell DW (2001) Molecular Cloning A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.