The Escherichia coli replication inhibitor CspD is subject to growth-regulated degradation by the Lon protease

Molecular Microbiology

Volumn 80, Issue 5, 2011, Pages 1313-1325

  Langklotz, Sina ^a   Narberhaus, Franz ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLD SHOCK PROTEIN D; ENDOPEPTIDASE LA; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; ESCHERICHIA COLI; GROWTH CURVE; GROWTH DISORDER; GROWTH RATE; GROWTH REGULATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; PLASMID; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PURIFICATION; PROTEIN STABILITY;

DNA REPLICATION; DOWN-REGULATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; PROTEASE LA; PROTEIN STABILITY;

ESCHERICHIA COLI;

EID: 79957445913     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07646.x     Document Type: Article

References (66)

1. Bachmann, B.J. (1972) Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 36: 525-557.
2. Balaban, N.Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
3. Barembruch, C., and Hengge, R. (2007) Cellular levels and activity of the flagellar sigma factor FliA of Escherichia coli are controlled by FlgM-modulated proteolysis. Mol Microbiol 65: 76-89.
4. S. Mol Microbiol 39: 1153-1165.
5. + Lon protease. Mol Microbiol 75: 1539-1549.
6. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
7. Butland, G., Peregrin-Alvarez, J.M., Li, J., Yang, W., Yang, X., Canadien, V., etal. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433: 531-537.
8. Charette, M.F., Henderson, G.W., and Markovitz, A. (1981) ATP hydrolysis-dependent protease activity of the lon (capR) protein of Escherichia coli K-12. Proc Natl Acad Sci USA 78: 4728-4732.
9. Choy, J.S., Aung, L.L., and Karzai, A.W. (2007) Lon protease degrades transfer-messenger RNA-tagged proteins. J Bacteriol 189: 6564-6571.
10. Christensen, S.K., Mikkelsen, M., Pedersen, K., and Gerdes, K. (2001) RelE, a global inhibitor of translation, is activated during nutritional stress. Proc Natl Acad Sci USA 98: 14328-14333.
11. Christensen, S.K., Pedersen, K., Hansen, F.G., and Gerdes, K. (2003) Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J Mol Biol 332: 809-819.
12. De Groote, V.N., Verstraeten, N., Fauvart, M., Kint, C.I., Verbeeck, A.M., Beullens, S., etal. (2009) Novel persistence genes in Pseudomonas aeruginosa identified by high-throughput screening. FEMS Microbiol Lett 297: 73-79.
13. Dienes, L., and Weinberger, H.J. (1951) The L forms of bacteria. Bacteriol Rev 15: 245-288.
14. Domingue, G.J., Sr, and Woody, H.B. (1997) Bacterial persistence and expression of disease. Clin Microbiol Rev 10: 320-344.
15. Dörr, T., Vulic, M., and Lewis, K. (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8: e1000317.
16. Führer, F., Langklotz, S., and Narberhaus, F. (2006) The C-terminal end of LpxC is required for degradation by the FtsH protease. Mol Microbiol 59: 1025-1036.
17. Führer, F., Müller, A., Baumann, H., Langklotz, S., Kutscher, B., and Narberhaus, F. (2007) Sequence and length recognition of the C-terminal turnover element of LpxC, a soluble substrate of the membrane-bound FtsH protease. J Mol Biol 372: 485-496.
18. Gerdes, K., Christensen, S.K., and Lobner-Olesen, A. (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3: 371-382.
19. Gerth, U., Kock, H., Kusters, I., Michalik, S., Switzer, R.L., and Hecker, M. (2008) Clp-dependent proteolysis down-regulates central metabolic pathways in glucose-starved Bacillus subtilis. J Bacteriol 190: 321-331.
20. Giangrossi, M., Exley, R.M., Hegarat, F.L., and Pon, C.L. (2001) Different in vivo localization of the Escherichia coli proteins CspD and CspA. FEMS Microbiol Lett 202: 171-176.
21. Glover, W.A., Yang, Y., and Zhang, Y. (2009) Insights into the molecular basis of L-form formation and survival in Escherichia coli. PLoS ONE 4: e7316.
22. Gonzalez, M., Frank, E.G., Levine, A.S., and Woodgate, R. (1998) Lon-mediated proteolysis of the Escherichia coli UmuD mutagenesis protein: in vitro degradation and identification of residues required for proteolysis. Genes Dev 12: 3889-3899.
23. Gottesman, S., Roche, E., Zhou, Y., and Sauer, R.T. (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12: 1338-1347.
24. Guex, N., and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
25. + protease. Genes Dev 22: 2267-2277.
26. BAD promoter. J Bacteriol 177: 4121-4130.
27. Hansen, S., Lewis, K., and Vulic, M. (2008) Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob Agents Chemother 52: 2718-2726.
28. Harrison, J.J., Ceri, H., Roper, N.J., Badry, E.A., Sproule, K.M., and Turner, R.J. (2005a) Persister cells mediate tolerance to metal oxyanions in Escherichia coli. Microbiology 151: 3181-3195.
29. Harrison, J.J., Turner, R.J., and Ceri, H. (2005b) Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa. Environ Microbiol 7: 981-994.
30. Hengge-Aronis, R., Lange, R., Henneberg, N., and Fischer, D. (1993) Osmotic regulation of rpoS-dependent genes in Escherichia coli. J Bacteriol 175: 259-265.
31. Herbst, K., Bujara, M., Heroven, A.K., Opitz, W., Weichert, M., Zimmermann, A., and Dersch, P. (2009) Intrinsic thermal sensing controls proteolysis of Yersinia virulence regulator RovA. PLoS Pathog 5: e1000435.
32. Herman, C., Thévenet, D., Bouloc, P., Walker, G.C., and D'Ari, R. (1998) Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH). Genes Dev 12: 1348-1355.
33. Heuveling, J., Possling, A., and Hengge, R. (2008) A role for Lon protease in the control of the acid resistance genes of Escherichia coli. Mol Microbiol 69: 534-547.
34. Hu, Y., and Coates, A.R. (2005) Transposon mutagenesis identifies genes which control antimicrobial drug tolerance in stationary-phase Escherichia coli. FEMS Microbiol Lett 243: 117-124.
35. Jõers, A., Kaldalu, N., and Tenson, T. (2010) The frequency of persisters in Escherichia coli reflects the kinetics of awakening from dormancy. J Bacteriol 192: 3379-3384.
36. Jones, P.G., and Inouye, M. (1994) The cold-shock response - a hot topic. Mol Microbiol 11: 811-818.
37. Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K. (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186: 8172-8180.
38. Kim, Y., and Wood, T.K. (2010) Toxins Hha and CspD and small RNA regulator Hfq are involved in persister cell formation through MqsR in Escherichia coli. Biochem Biophys Res Commun 391: 209-213.
39. Kim, Y., Wang, X., Zhang, X.S., Grigoriu, S., Page, R., Peti, W., and Wood, T.K. (2010) Escherichia coli toxin/antitoxin pair MqsR/MqsA regulate toxin CspD. Environ Microbiol 12: 1105-1121.
40. Korch, S.B., Henderson, T.A., and Hill, T.M. (2003) Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol Microbiol 50: 1199-1213.
41. Kuroda, A., Murphy, H., Cashel, M., and Kornberg, A. (1997) Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J Biol Chem 272: 21240-21243.
42. Kuroda, A., Nomura, K., Ohtomo, R., Kato, J., Ikeda, T., Takiguchi, N., etal. (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293: 705-708.
43. Lederberg, J. (1956) Bacterial protoplasts induced by penicillin. Proc Natl Acad Sci USA 42: 574-577.
44. Lewis, K. (2010) Persister cells. Annu Rev Microbiol 64: 357-372.
45. Magnuson, R.D. (2007) Hypothetical functions of toxin-antitoxin systems. J Bacteriol 189: 6089-6092.
46. Magnusson, L.U., Nystrom, T., and Farewell, A. (2003) Underproduction of s70 mimics a stringent response. A proteome approach. J Biol Chem 278: 968-973.
47. Markova, N., Slavchev, G., Michailova, L., and Jourdanova, M. (2010) Survival of Escherichia coli under lethal heat stress by L-form conversion. Int J Biol Sci 6: 303-315.
48. Mulcahy, L.R., Burns, J.L., Lory, S., and Lewis, K. (2010) Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol 192: 6191-6199.
49. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Schindelin, H., Jiang, W., Inouye, M., and Heinemann, U. (1994) Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 91: 5119-5123.
51. Schmidt, R., Zahn, R., Bukau, B., and Mogk, A. (2009) ClpS is the recognition component for Escherichia coli substrates of the N-end rule degradation pathway. Mol Microbiol 72: 506-517.
52. Shah, D., Zhang, Z., Khodursky, A., Kaldalu, N., Kurg, K., and Lewis, K. (2006) Persisters: a distinct physiological state of E. coli. BMC Microbiol 6: 53.
53. Shenhar, Y., Rasouly, A., Biran, D., and Ron, E.Z. (2009) Adaptation of Escherichia coli to elevated temperatures involves a change in stability of heat shock gene transcripts. Environ Microbiol 11: 2989-2997.
54. da Silva, C.A., Balhesteros, H., Mazzon, R.R., and Marques, M.V. (2010) SpdR, a response regulator required for stationary-phase induction of Caulobacter crescentus cspD. J Bacteriol 192: 5991-6000.
55. Smith, P.A., and Romesberg, F.E. (2007) Combating bacteria and drug resistance by inhibiting mechanisms of persistence and adaptation. Nat Chem Biol 3: 549-556.
56. Spoering, A.L., and Lewis, K. (2001) Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183: 6746-6751.
57. Stewart, P.S., and Costerton, J.W. (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358: 135-138.
58. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185: 60-89.
59. 32in vivo. Mol Microbiol 30: 583-593.
60. 32. EMBO J 14: 2551-2560.
61. Van Melderen, L., and Aertsen, A. (2009) Regulation and quality control by Lon-dependent proteolysis. Res Microbiol 160: 645-651.
62. Van Melderen, L., Thi, M.H., Lecchi, P., Gottesman, S., Couturier, M., and Maurizi, M.R. (1996) ATP-dependent degradation of CcdA by Lon protease. Effects of secondary structure and heterologous subunit interactions. J Biol Chem 271: 27730-27738.
63. Xiao, H., Kalman, M., Ikehara, K., Zemel, S., Glaser, G., and Cashel, M. (1991) Residual guanosine 3', 5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem 266: 5980-5990.
64. Yamanaka, K., and Inouye, M. (1997) Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli. J Bacteriol 179: 5126-5130.
65. Yamanaka, K., Fang, L., and Inouye, M. (1998) The CspA family in Escherichia coli: multiple gene duplication for stress adaptation. Mol Microbiol 27: 247-255.
66. Yamanaka, K., Zheng, W., Crooke, E., Wang, Y.H., and Inouye, M. (2001) CspD, a novel DNA replication inhibitor induced during the stationary phase in Escherichia coli. Mol Microbiol 39: 1572-1584.