Authentic precursors to ribosomal subunits accumulate in Escherichia coli in the absence of functional DnaK chaperone

Molecular Microbiology

Volumn 51, Issue 1, 2004, Pages 189-201

  El Hage, Aziz ^a   Alix, Jean Hervé ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; PROTEIN DNAK; RIBOSOME RNA; RNA 5S;

BACTERIUM MUTANT; BIOGENESIS; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; ISOTOPE LABELING; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; RIBOSOME; RIBOSOME SUBUNIT; SHORT SURVEY; STOICHIOMETRY; TEMPERATURE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BASE SEQUENCE; DNA, BACTERIAL; DNA, RIBOSOMAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; HSP70 HEAT-SHOCK PROTEINS; KINETICS; MOLECULAR CHAPERONES; OLIGONUCLEOTIDE PROBES; RIBOSOMES; RIFAMPIN; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 23S; RNA, RIBOSOMAL, 5S;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0347595319     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03813.x     Document Type: Short Survey

References (54)

1. Adachi, K., and Sells, B.H. (1979) The effect of magnesium starvation on the dissociation of ribosomal proteins from Escherichia coli K-12 ribosomes. Biochim Biophys Acta 563: 163-170.
2. Alix, J.H. (1993) Extrinsic factors in ribosome assembly. In The Translational Apparatus. Nierhaus, K.H. (ed.). New York: Plenum Press, pp. 173-184.
3. Alix, J.H., and Guérin, M.F. (1993) Mutant DnaK chaperones cause ribosome assembly defects in Escherichia coli. Proc Natl Acad Sci USA 90: 9725-9729.
4. Alix, J.H., and Nierhaus, K.H. (2003) DnaK-facilitated ribosome assembly in Escherichia coli revisited. RNA 9: 787-793.
5. Arsene, F., Tomoyasu, T., and Bukau, B. (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55: 3-9.
6. Burkholder, W., and Gottesman, M. (1999) Genetic evidence for the roles of molecular chaperones in E. coli metabolism. In Molecular Chaperones and Folding Catalysts: Regulation, Cellular Function and Mechanisms. Bukau, B. (ed.). Amsterdam: Harwood Academic Publishers, pp. 105-138.
7. Butler, P.D., Sims, P.F., and Wild, D.G. (1980) Intermediates in the assembly of ribosomes by a mutant of Escherichia coli. Biochem J 190: 157-170.
8. Charollais, J., Pflieger, D., Vinh, J., Dreyfus, M., and Iost, I. (2003) The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli. Mol Microbiol 48: 1253-1265.
9. Cheng, Z.F., and Deutscher, M.P. (2003) Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc Natl Acad Sci USA 100: 6388-6393.
10. Craig, E.A., and Gross, C.A. (1991) Is hsp70 the cellular thermometer? Trends Biochem Sci 16: 135-140.
11. Culver, G.M. (2003) Assembly of the 30S ribosomal subunit. Biopolymers 68: 234-249.
12. Dennis, P.P. (1974) Synthesis and stability of individual ribosomal proteins in the presence of rifampicin. Mol Gen Genet 134: 39-47.
13. Deuerling, E., Patzelt, H., Vorderwulbecke, S., Rauch, T., Kramer, G., Schaffitzel, E., et al. (2003) Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Mol Microbiol 47: 1317-1328.
14. Diedrich, G., Spahn, C.M., Stelzl, U., Schafer, M.A., Wooten, T., Bochkariov, D.E., et al. (2000) Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. EMBO J 19: 5241-5250.
15. Duncan, M.J., and Gorini, L. (1975) A ribonucleoprotein precursor of both the 30S and 50S subunits of Escherichia coli. Proc Natl Acad Sci USA 72: 1533-1537.
16. El Hage, A., Sbai, M., and Alix, J.H. (2001) The chaperonin GroEL and other heat-shock proteins, besides DnaK, participate in ribosome biogenesis in Escherichia coli. Mol Gen Genet 264: 796-808.
17. Flynn, J.M., Neher, S.B., Kim, Y.I., Sauer, R.T., and Baker, T.A. (2003) Proteomic discovery of cellular substrates of the CIpXP protease reveals five classes of CIpX-recognition signals. Mol Cell 11: 671-683.
18. Gausing, K. (1974) Ribosomal protein in E. coli: rate of synthesis and pool size at different growth rates. Mol Gen Genet 129: 61-75.
19. Ghosh, J., Basu, A., Pal, S., Chowdhuri, S., Bhattacharya, A., Pal, D., et al. (2003) Ribosome-DnaK interactions in relation to protein folding. Mol Microbiol 48: 1679-1692.
20. Gupta, R.S., and Singh, U.N. (1972) Biogenesis of ribosomes: free ribosomal protein pools in Escherichia coli. J Mol Biol 69: 279-301.
21. Hayes, F., and Hayes, D.H. (1971) Biosynthesis of ribosomes in E. coli. I. Properties of ribosomal precursor particles and their RNA components. Biochimie 53: 369-382.
22. Hesterkamp, T., and Bukau, B. (1998) Role of the DnaK and HscA homologs of Hsp70 chaperones in protein folding in E. coli. EMBO J 17: 4818-4828.
23. Kalschmidt, E., and Whittmann, H.G. (1970) Ribosomal proteins. VII. Two-dimensional polyacrylamide gel electrophoresis for fingerprinting of ribosomal proteins. Anal Biochem 36: 401-412.
24. Kuroda, A., Nomura, K., Ohtomo, R., Kato, J., Ikeda, T., Takiguchi, N., et al. (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293: 705-708.
25. Lefkovits, I., and Di Girolamo, M. (1969) Reutilization of ribosomal proteins in vivo for the formation of new ribosomal particles in Escherichia coli B. Biochim Biophys Acta 174: 566-573.
26. Liang, S.T., Ehrenberg, M., Dennis, P., and Bremer, H. (1999) Decay of rplN and lacZ mRNA in Escherichia coli. J Mol Biol 288: 521-538.
27. Lindahl, L. (1975) Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J Mol Biol 92: 15-37.
28. Lund, P.A. (2001) Microbial molecular chaperones. Adv Microb Physiol 44: 93-140.
29. Maki, J.A., Schnobrich, D.J., and Culver, G.M. (2002) The DnaK chaperone system facilitates 30S ribosomal subunit assembly. Mol Cell 10: 129-138.
30. Mandiyan, V., Tumminia, S.J., Wall, J.S., Hainfeld, J.F., and Boublik, M. (1991) Assembly of the Escherichia coli 30S ribosomal subunit reveals protein-dependent folding of the 16S rRNA domains. Proc Natl Acad Sci USA 88: 8174-8178.
31. Marvaldi, J., Pichon, J., Delaage, M., and Marchis-Mouren, G. (1974) Individual ribosomal protein pool size and turnover rate in Escherichia coli. J Mol Biol 84: 83-96.
32. Nakada, D., and Marquisee, M.J. (1965) Relaxed synthesis of ribosomal RNA by a stringent strain of Escherichia coli. J Mol Biol 13: 351-361.
33. de Narvaez, C.C., and Schaup, H.W. (1979) In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J Mol Biol 134: 1-22.
34. Nierhaus, K.H. (1991) The assembly of prokaryotic ribosomes. Biochimie 73: 739-755.
35. Nierhaus, K.H., Bordasch, K., and Homann, H.E. (1973) Ribosomal proteins. 43. In vivo assembly of Escherichia coli ribosomal proteins. J Mol Biol 74: 587-597.
36. Nomura, M. (1990) History of ribosome research: a personal account. In The Ribosome, Structure, Function and Evolution. Hill, W.E., Dahlberg, A.E., Garett, R.A., Moore, P.B., Schlessinger, D., and Warner, J.R. (eds). Washington, DC: American Society for Microbiology Press, pp. 3-55.
37. Okada, S., Okada, T., Aimi, T., Morinaga, T., and Itoh, T. (2000) HSP70 and ribosomal protein L2: novel 5S rRNA binding proteins in Escherichia coli. FEBS Lett 485: 153-156.
38. Pichon, J., Marvaldi, J., and Marchis-Mouren, G. (1975) The in vivo order of protein addition in the course of Escherichia coli 30 S and 50 S subunit biogenesis. J Mol Biol 96: 125-137.
39. Robertson, W.R., Dowsett, S.J., and Hardy, S.J. (1977) Exchange of ribosomal proteins among the ribosomes of Escherichia coli. Mol Gen Genet 157: 205-214.
40. Rüdiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J 16: 1501-1507.
41. + Mol Gen Genet 260: 199-206.
42. Stagg, S.M., Mears, J.A., and Harvey, S.C. (2003) A structural model for the assembly of the 30S subunit of the ribosome. J Mol Biol 328: 49-61.
43. Subramanian, A.R., and van Duin, J. (1977) Exchange of individual ribosomal proteins between ribosomes as studied by heavy isotope-transfer experiments. Mol Gen Genet 158: 1-9.
44. Sykes, J., and Metcalf, E. (1979) The pools of ribosomal proteins and ribosomal ribonucleic acids during relaxed control of Escherichia coli A19. J Gen Microbiol 112: 149-159.
45. Sykes, J., Metcalf, E., and Pickering, J.D. (1977) The nature of the proteins present in the 'relaxed particles' from methionine-starved Escherichia coli A19 (Hfr rel met rns). J Gen Microbiol 98: 17-27.
46. Tal, M., Silberstein, A., and Moyner, K. (1977) In vivo reassembly of 30S ribosomal subunits following their specific destruction by thermal shock. Biochim Biophys Acta 479: 479-496.
47. Torres, M., Condon, C., Balada, J.M., Squires, C., and Squires, C.L. (2001) Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination. EMBO J 20: 3811-3820.
48. Turco, E., Altruda, F., Ponzetto, A., and Mangiarotti, G. (1974) Ribosome biosynthesis in Escherichia coli. Concerning the limiting step. Biochemistry 13: 4752-4757.
49. Ulbrich, B., and Nierhaus, K.H. (1975) Pools of ribosomal proteins in Escherichia coli. Studies on the exchange of proteins between pools and ribosomes. Eur J Biochem 57: 49-54.
50. Wickner, S., Maurizi, M.R., and Gottesman, S. (1999) Post-translational quality control: folding, refolding, and degrading proteins. Science 286: 1888-1893.
51. Wireman, J.W., and Sypherd, P.S. (1975) Temperature dependence for physical and functional reconstitution of 30S ribosomes of E. coli. Biochem Biophys Res Commun 66: 570-577.
52. Wright, M. (1971) Mutants of Escherichia coli lacking endonuclease I, ribonuclease I, or ribonuclease II. J Bacteriol 107: 87-94.
53. Yu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G., and Court, D.L. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97: 5978-5983.
54. Zimmer, C., von Gabain, A., and Henics, T. (2001) Analysis of sequence-specific binding of RNA to Hsp70 and its various homologs indicates the involvement of N- and C-terminal interactions. RNA 7: 1628-1637.