Regulation of CtsR activity in low GC, Gram+ bacteria

Advances in Microbial Physiology

Volumn 57, Issue C, 2010, Pages 119-144

  Elsholz, Alexander K W ^a   Gerth, Ulf ^a   Hecker, Michael ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CHAPERONE; CORE PROTEIN; DNA; PROTEIN KINASE; PROTEIN TYROSINE PHOSPHATASE; VIRULENCE FACTOR;

ADAPTATION; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL VIRULENCE; BOOK; DNA BINDING; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GRAM POSITIVE BACTERIUM; HEAT SHOCK; HEAT STRESS; LACTOBACILLUS; LISTERIA MONOCYTOGENES; NONHUMAN; OPERON; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

FIRMICUTES;

EID: 78349271609     PISSN: 00652911     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-381045-8.00003-5     Document Type: Chapter

References (115)

1. Baker T.A., Sauer R.T. ATP-dependent proteases of bacteria: recognition logic and operating principles. Trend Biochem. Sci. 2006, 31:647-653.
2. Banecki B., Wawrzynow A., Puzewicz J., Georgopoulos C., Zylicz M. Structure-function analysis of the zinc-binding region of the Clpx molecular chaperone. J. Biol. Chem. 2001, 276:18843-18848.
3. Beltramo C., Grandvalet C., Pierre F., Guzzo J. Evidence for multiple levels of regulation of Oenococcus oeni clpP-clpL locus expression in response to stress. J. Bacteriol. 2004, 186:2200-2205.
4. Borezée E., Pellegrini E., Beretti J.L., Berche P. SvpA, a novel surface virulence-associated protein required for intracellular survival of Listeria monocytogenes. Microbiology (Reading Engl.) 2001, 147:2913-2923.
5. Böttcher T., Sieber S.A. Beta-lactones as specific inhibitors of ClpP attenuate the production of extracellular virulence factors of Staphylococcus aureus. J. Am. Chem. Soc. 2008, 130:14400-14401.
6. Brötz-Oesterhelt H., Beyer D., Kroll H.-P., Endermann R., Ladel C., Schroeder W., Hinzen B., Raddatz S., Paulsen H., Henninger K., Bandow J.E., Sahl H.-G., Labischinski H. Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat. Med. 2005, 11:1082-1087.
7. Bukau B. Regulation of the Escherichia coli heat-shock response. Mol. Microbiol. 1993, 9:671-680.
8. Charpentier E., Novak R., Tuomanen E. Regulation of growth inhibition at high temperature, autolysis, transformation and adherence in Streptococcus pneumoniae by clpC. Mol. Microbiol. 2000, 37:717-726.
9. Chastanet A., Derre I., Nair S., Msadek T. clpB, a novel member of the Listeria monocytogenes CtsR regulon, is involved in virulence but not in general stress tolerance. J. Bacteriol. 2004, 186:1165-1174.
10. Chastanet A., Fert J., Msadek T. Comparative genomics reveal novel heat shock regulatory mechanisms in Staphylococcus aureus and other Gram-positive bacteria. Mol. Microbiol. 2003, 47:1061-1073.
11. Chastanet A., Msadek T. ClpP of Streptococcus salivarius is a novel member of the dually regulated class of stress response genes in gram-positive bacteria. J. Bacteriol. 2003, 185:683-687.
12. Chastanet A., Prudhomme M., Claverys J.P., Msadek T. Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J. Bacteriol. 2001, 183:7295-7307.
13. Chatterjee I., Becker P., Grundmeier M., Bischoff M., Somerville G.A., Peters G., Sinha B., Harraghy N., Proctor R.A., Herrmann M. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J. Bacteriol. 2005, 187:4488-4496.
14. Craig E.A. The heat shock response. CRC Crit. Rev. Biochem. 1985, 18:239-280.
15. Darwin K.H. Prokaryotic ubiquitin-like protein (Pup), proteasomes and pathogenesis. Nat. Rev. Micro. 2009, 7:485-491.
16. Derré I., Rapoport G., Devine K., Rose M., Msadek T. ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol. Microbiol. 1999, 32:581-593.
17. Derré I., Rapoport G., Msadek T. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram positive bacteria. Mol. Microbiol. 1999, 31:117-131.
18. Derré I., Rapoport G., Msadek T. The CtsR regulator of stress response is active as a dimer and specifically degraded in vivo at 37 degrees C. Mol. Microbiol. 2000, 38:335-347.
19. Donegan N.P., Thompson E.T., Fu Z., Cheung A.L. Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus. J. Bacteriol. 2010, 192:1416-1422.
20. Elsholz, A.K.W., Hempel, K., Pöther, D.C., Becher, D., Hecker, M. and Gerth, U. A new mechanism for CtsR inactivation during oxidative stress in low GC, Gram+ bacteria. Manuscript Submitted.
21. Elsholz A.K.W., Michalik S., Zühlke D., Hecker M., Gerth U. CtsR, the Gram positive master regulator of protein quality control, feels the heat. EMBO J 2010.
22. Fiocco D., Capozzi V., Collins M., Gallone A., Hols P., Guzzo J., Weidmann S., Rieu A., Msadek T., Spano G. Characterization of the CtsR stress response regulon in Lactobacillus plantarum. J. Bacteriol. 2010, 192:896-900.
23. Fiocco D., Collins M., Muscariello L., Hols P., Kleerebezem M., Msadek T., Spano G. The Lactobacillus plantarum ftsH gene is a novel member of the CtsR stress response regulon. J. Bacteriol. 2008, 191:1688-1694.
24. Fleury B., Kelley W.L., Lew D., Götz F., Proctor R.A., Vaudaux P. Transcriptomic and metabolic responses of Staphylococcus aureus exposed to supra-physiological temperatures. BMC Microbiol. 2009, 9:76.
25. Frees D., Chastanet A., Qazi S., Sørensen K., Hill P., Msadek T., Ingmer H. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol. Microbiol 2004, 54:1445-1462.
26. Frees D., Ingmer H. ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol. Microbiol. 1999, 31:79-87.
27. Frees D., Qazi S.N.A., Hill P.J., Ingmer H. Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol. Microbiol. 2003, 48:1565-1578.
28. Frees D., Savijoki K., Varmanen P., Ingmer H. Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria. Mol. Microbiol. 2007, 63:1285-1295.
29. Frees D., Vogensen F.K., Ingmer H. Identification of proteins induced at low pH in Lactococcus lactis. Int. J. Food Microbiol. 2003, 87:293-300.
30. Fuhrmann J., Schmidt A., Spiess S., Lehner A., Turgay K., Mechtler K., Charpentier E., Clausen T. McsB is a protein arginine kinase that phosphorylates and inhibits the heat-shock regulator CtsR. Science 2009, 324:1323-1327.
31. Gaillot O., Pellegrini E., Bregenholt S., Nair S., Berche P. The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes. Mol. Microbiol. 2000, 35:1286-1294.
32. Gerth U., Kirstein J., Mostertz J., Waldminghaus T., Miethke M., Kock H., Hecker M. Fine-tuning in regulation of Clp protein content in Bacillus subtilis. J. Bacteriol. 2004, 186:179-191.
33. Gerth U., Kock H., Kusters I., Michalik S., Switzer R.L., Hecker M. Clp dependent proteolysis down-regulates central metabolic pathways in glucose starved Bacillus subtilis. J. Bacteriol. 2008, 190:321-331.
34. Gerth U., Krüger E., Derré I., Msadek T., Hecker M. Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol. Microbiol. 1998, 28:787-802.
35. Gerth U., Wipat A., Harwood C.R., Carter N., Emmerson P.T., Hecker M. Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene 1996, 181:77-83.
36. Gertz S., Engelmann S., Schmid R., Ziebandt A.K., Tischer K., Scharf C., Hacker J., Hecker M. Characterization of the sigma(B) regulon in Staphylococcus aureus. J. Bacteriol. 2000, 182:6983-6991.
37. Gething M.J., Sambrook J. Protein folding in the cell. Nature 1992, 355:33-45.
38. Gottesman S. Proteolysis in bacterial regulatory circuits. Annu. Rev. Cell Dev. Biol. 2003, 19:565-587.
39. Grandvalet C., Coucheney F., Beltramo C., Guzzo J. CtsR is the master regulator of stress response gene expression in Oenococcus oeni. J. Bacteriol. 2005, 187:5614-5623.
40. Hahn J., Kramer N., Briley K., Dubnau D. McsA and B mediate the delocalization of competence proteins from the cell poles of Bacillus subtilis. Mol. Microbiol. 2009, 72:202-215.
41. Hartl F.U., Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 2009, 16:574-581.
42. Hecker M., Pané-Farré J., Völker U. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 2007, 61:215-236.
43. Homuth G., Masuda S., Mogk A., Kobayashi Y., Schumann W. The dnaK operon of Bacillus subtilis is heptacistronic. J. Bacteriol. 1997, 179:1153-1164.
44. Hu Y., Raengpradub S., Schwab U., Loss C., Orsi R.H., Wiedmann M., Boor K.J. Phenotypic and transcriptomic analyses demonstrate interactions between the transcriptional regulators CtsR and Sigma B in Listeria monocytogenes. Appl. Environ. Microbiol. 2007, 73:7967-7980.
45. Hüfner E., Hertel C. Improvement of raw sausage fermentation by stress conditioning of the starter organism Lactobacillus sakei. Curr. Microbiol. 2008, 57:490-496.
46. Hüfner E., Markieton T., Chaillou S., Crutz-Le Coq A.-M., Zagorec M., Hertel C. Identification of Lactobacillus sakei genes induced during meat fermentation and their role in survival and growth. Appl. Environ. Microbiol. 2007, 73:2522-2531.
47. Ibrahim Y.M., Kerr A.R., Silva N.A., Mitchell T.J. Contribution of the ATP dependent protease ClpCP to the autolysis and virulence of Streptococcus pneumoniae. Infect. Immun. 2005, 73:730-740.
48. Ingmer H., Vogensen F.K., Hammer K., Kilstrup M. Disruption and analysis of the clpB, clpC, and clpE genes in Lactococcus lactis: ClpE, a new Clp family in gram-positive bacteria. J. Bacteriol. 1999, 181:2075-2083.
49. Jennings L.D., Lun D.S., Médard M., Licht S. ClpP hydrolyzes a protein substrate processively in the absence of the ClpA ATPase: mechanistic studies of ATP-independent proteolysis. Biochemistry 2008, 47:11536-11546.
50. Kajfasz J.K., Martinez A.R., Rivera-Ramos I., Abranches J., Koo H., Quivey R.G., Lemos J.A. Role of Clp proteins in expression of virulence properties of Streptococcus mutans. J. Bacteriol. 2009, 191:2060-2068.
51. Karatzas K.A.G., Valdramidis V.P., Wells-Bennik M.H.J. Contingency locus in ctsR of Listeria monocytogenes Scott A: a strategy for occurrence of abundant piezo tolerant isolates within clonal populations. Appl. Environ. Microbiol. 2005, 71:8390-8396.
52. Karatzas K.A.G., Wouters J.A., Gahan C.G.M., Hill C., Abee T., Bennik M.H.J. The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezo tolerance, stress resistance, motility and virulence. Mol. Microbiol. 2003, 49:1227-1238.
53. Karatzas K.A.G., Zervos A., Tassou C.C., Mallidis C.G., Humphrey T.J. Piezotolerant small-colony variants with increased thermotolerance, antibiotic susceptibility, and low invasiveness in a clonal Staphylococcus aureus population. Appl. Environ. Microbiol. 2007, 73:1873-1881.
54. Kim Y.I., Levchenko I., Fraczkowska K., Woodruff R.V., Sauer R.T., Baker T.A. Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat. Struct. Biol. 2001, 8:230-233.
55. Kirstein J., Dougan D.A., Gerth U., Hecker M., Turgay K. The tyrosine kinase McsB is a regulated adaptor protein for ClpCP. EMBO J. 2007, 26:2061-2070.
56. Kirstein J., Molière N., Dougan D.A., Turgay K. Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat. Rev. Micro. 2009, 7:589-599.
57. Kirstein J., Schlothauer T., Dougan D.A., Lilie H., Tischendorf G., Mogk A., Bukau B., Turgay K. Adaptor protein controlled oligomerization activates the AAA+ protein ClpC. EMBO J. 2006, 25:1481-1491.
58. Kirstein J., Zühlke D., Gerth U., Turgay K., Hecker M. A tyrosine kinase and its activator control the activity of the CtsR heat shock repressor in B. subtilis. EMBO J. 2005, 24:3435-3445.
59. Kock H., Gerth U., Hecker M. MurAA, catalysing the first committed step in peptidoglycan biosynthesis, is a target of Clp-dependent proteolysis in Bacillus subtilis. Mol. Microbiol. 2004, 51:1087-1102.
60. Kock H., Gerth U., Hecker M. The ClpP peptidase is the major determinant of bulk protein turnover in Bacillus subtilis. J. Bacteriol. 2004, 186:5856-5864.
61. Krüger E., Msadek T., Hecker M. Alternate promoters direct stress-induced transcription of the Bacillus subtilis clpC operon. Mol. Microbiol. 1996, 20:713-723.
62. Krüger E., Msadek T., Ohlmeier S., Hecker M. The Bacillus subtilis clpC operon encodes DNA repair and competence proteins. Microbiology (Reading Engl.) 1997, 143(Pt 4):1309-1316.
63. Krüger E., Völker U., Hecker M. Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J. Bacteriol. 1994, 176:3360-3367.
64. Krüger E., Witt E., Ohlmeier S., Hanschke R., Hecker M. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J. Bacteriol. 2000, 182:3259-3265.
65. Krüger E., Zühlke D., Witt E., Ludwig H., Hecker M. Clp-mediated proteolysis in Gram-positive bacteria is autoregulated by the stability of a repressor. EMBO J. 2001, 20:852-863.
66. Kwon H.-Y., Kim S.-W., Choi M.-H., Ogunniyi A.D., Paton J.C., Park S.-H., Pyo S.-N., Rhee D.-K. Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae. Infect. Immun. 2003, 71:3757-3765.
67. Leichert L.I.O., Scharf C., Hecker M. Global characterization of disulfide stress in Bacillus subtilis. J. Bacteriol. 2003, 185:1967-1975.
68. Lemos J.A., Luzardo Y., Burne R.A. Physiologic effects of forced downregulation of dnaK and groEL expression in Streptococcus mutans. J. Bacteriol. 2007, 189:1582-1588.
69. Lemos J.A.C., Burne R.A. Regulation and physiological significance of ClpC and ClpP in Streptococcus mutans. J. Bacteriol. 2002, 184:6357-6366.
70. Matthews B.W., Nicholson H., Becktel W.J. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:6663-6667.
71. Miethke M., Hecker M., Gerth U. Involvement of Bacillus subtilis ClpE in CtsR degradation and protein quality control. J. Bacteriol. 2006, 188:4610-4619.
72. Mogk A., Homuth G., Scholz C., Kim L., Schmid F.X., Schumann W. The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J. 1997, 16:4579-4590.
73. Mostertz J., Scharf C., Hecker M., Homuth G. Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology (Reading Engl.) 2004, 150:497-512.
74. Moxon R., Bayliss C., Hood D. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet. 2006, 40:307-333.
75. Msadek T., Dartois V., Kunst F., Herbaud M.L., Denizot F., Rapoport G. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol. Microbiol. 1998, 27:899-914.
76. Msadek T., Kunst F., Rapoport G. MecB of Bacillus subtilis, a member of the ClpC ATPase family, is a pleiotropic regulator controlling competence gene expression and growth at high temperature. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:5788-5792.
77. Nair S., Derré I., Msadek T., Gaillot O., Berche P. CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Mol. Microbiol. 2000, 35:800-811.
78. Nair S., Frehel C., Nguyen L., Escuyer V., Berche P. ClpE, a novel member of the HSP100 family, is involved in cell division and virulence of Listeria monocytogenes. Mol. Microbiol. 1999, 31:185-196.
79. Nair S., Milohanic E., Berche P. ClpC ATPase is required for cell adhesion and invasion of Listeria monocytogenes. Infect. Immun. 2000, 68:7061-7068.
80. Nakano S., Zheng G., Nakano M.M., Zuber P. Multiple pathways of Spx (YjbD) proteolysis in Bacillus subtilis. J. Bacteriol. 2002, 184:3664-3670.
81. Neher S.B., Villén J., Oakes E.C., Bakalarski C.E., Sauer R.T., Gygi S.P., Baker T.A. Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol. Cell 2006, 22:193-204.
82. Neuwald A.F., Aravind L., Spouge J.L., Koonin E.V. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 1999, 9:27-43.
83. Nguyen T.T.H., Eiamphungporn W., Mäder U., Liebeke M., Lalk M., Hecker M., Helmann J.D., Antelmann H. Genome-wide responses to carbonyl electrophiles in Bacillus subtilis: control of the thiol-dependent formaldehyde dehydrogenase AdhA and cysteine proteinase YraA by the MerR-family regulator YraB (AdhR). Mol. Microbiol. 2009, 71:876-894.
84. Ogura M., Tsukahara K. Autoregulation of the Bacillus subtilis response regulator gene degU is coupled with the proteolysis of DegU-P by ClpCP. Mol. Microbiol. 2010, 75:1592-1596.
85. Pan Q., Garsin D.A., Losick R. Self-reinforcing activation of a cell-specific transcription factor by proteolysis of an anti-sigma factor in B. subtilis. Mol. Cell 2001, 8:873-883.
86. Pickart C.M., Cohen R.E. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell Biol. 2004, 5:177-187.
87. Qoronfleh M.W., Bortner C.A., Schwartzberg P., Wilkinson B.J. Enhanced levels of Staphylococcus aureus stress protein GroEL and DnaK homologs early in infection of human epithelial cells. Infect. Immun. 1998, 66:3024-3027.
88. Qoronfleh M.W., Weraarchakul W., Wilkinson B.J. Antibodies to a range of Staphylococcus aureus and Escherichia coli heat shock proteins in sera from patients with S. aureus endocarditis. Infect. Immun. 1993, 61:1567-1570.
89. Robertson G.T., Ng W.-L., Foley J., Gilmour R., Winkler M.E. Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence. J. Bacteriol. 2002, 184:3508-3520.
90. Rocha E.P.C., Matic I., Taddei F. Over-representation of repeats in stress response genes: a strategy to increase versatility under stressful conditions?. Nucleic Acids Res. 2002, 30:1886-1894.
91. Rouquette C., de Chastellier C., Nair S., Berche P. The ClpC ATPase of Listeria monocytogenes is a general stress protein required for virulence and promoting early bacterial escape from the phagosome of macrophages. Mol. Microbiol. 1998, 27:1235-1245.
92. Rouquette C., Ripio M.T., Pellegrini E., Bolla J.M., Tascon R.I., Vázquez-Boland J.A., Berche P. Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Mol. Microbiol. 1996, 21:977-987.
93. Sauer R.T., Bolon D.N., Burton B.M., Burton R.E., Flynn J.M., Grant R.A., Hersch G.L., Joshi S.A., Kenniston J.A., Levchenko I., Neher S.B., Oakes E.S.C., Siddiqui S.M., Wah D.A., Baker T.A. Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 2004, 119:9-18.
94. Savijoki K., Ingmer H., Frees D., Vogensen F.K., Palva A., Varmanen P. Heat and DNA damage induction of the LexA-like regulator HdiR from Lactococcus lactis is mediated by RecA and ClpP. Mol. Microbiol. 2003, 50:609-621.
95. Schumann W. The Bacillus subtilis heat shock stimulon. Cell Stress Chaperone 2004, 8:207-217.
96. Singh V.K., Utaida S., Jackson L.S., Jayaswal R.K., Wilkinson B.J., Chamberlain N.R. Role for dnaK locus in tolerance of multiple stresses in Staphylococcus aureus. Microbiology (Reading Engl.) 2007, 153:3162-3173.
97. Thompson M.W., Singh S.K., Maurizi M.R. Processive degradation of proteins by the ATP-dependent Clp protease from Escherichia coli. Requirement for the multiple array of active sites in ClpP but not ATP hydrolysis. J. Biol. Chem. 1994, 269:18209-18215.
98. Treangen T.J., Abraham A.-L., Touchon M., Rocha E.P.C. Genesis, effects and fates of repeats in prokaryotic genomes. FEMS Microbiol. Rev. 2009, 33:539-571.
99. Turgay K., Hahn J., Burghoorn J., Dubnau D. Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J. 1998, 17:6730-6738.
100. van de Guchte M., Penaud S., Grimaldi C., Barbe V., Bryson K., Nicolas P., Robert C., Oztas S., Mangenot S., Couloux A., Loux V., Dervyn R., Bossy R., Bolotin A., Batto J.-M., Walunas T., Gibrat J.-F., Bessières P., Weissenbach J., Ehrlich S.D., Maguin E. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:9274-9279.
101. Varmanen P., Ingmer H., Vogensen F.K. ctsR of Lactococcus lactis encodes a negative regulator of clp gene expression. Microbiology (Reading Engl.) 2000, 146(Pt 6):1447-1455.
102. Varmanen P., Vogensen F.K., Hammer K., Palva A., Ingmer H. ClpE from Lactococcus lactis promotes repression of CtsR-dependent gene expression. J. Bacteriol. 2003, 185:5117-5124.
103. Wang J., Hartling J.A., Flanagan J.M. The structure of ClpP at 2.3Å resolution suggests a model for ATP-dependent proteolysis. Cell 1997, 91:447-456.
104. Weber-Ban E.U., Reid B.G., Miranker A.D., Horwich A.L. Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 1999, 401:90-93.
105. Weibezahn J., Tessarz P., Schlieker C., Zahn R., Maglica Z., Lee S., Zentgraf H., Weber-Ban E.U., Dougan D.A., Tsai F.T.F., Mogk A., Bukau B. Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 2004, 119:653-665.
106. Wickner S., Maurizi M.R., Gottesman S. Posttranslational quality control: folding, refolding, and degrading proteins. Science 1999, 286:1888-1893.
107. Wiegert T., Schumann W. SsrA-mediated tagging in Bacillus subtilis. J. Bacteriol. 2001, 183:3885-3889.
108. Young J.C., Agashe V.R., Siegers K., Hartl F.U. Pathways of chaperone mediated protein folding in the cytosol. Nat. Rev. Mol. Cell Biol. 2004, 5:781-791.
109. Yuan G., Wong S.L. Isolation and characterization of Bacillus subtilis groE regulatory mutants: evidence for orf39 in the dnaK operon as a repressor gene in regulating the expression of both groE and dnaK. J. Bacteriol. 1995, 177:6462-6468.
110. Yura T. Regulation and conservation of the heat-shock transcription factor sigma32. Genes Cells 1996, 1:277-284.
111. Zellmeier S., Schumann W., Wiegert T. Involvement of Clp protease activity in modulating the Bacillus subtilis sigma-w stress response. Mol. Microbiol. 2006, 61:1569-1582.
112. Zhang Q., Xu S.-X., Wang H., Xu W.-C., Zhang X.-M., Wu K.-F., Liu L., Yin Y.-B. Contribution of ClpE to virulence of Streptococcus pneumoniae. Can. J. Microbiol. 2009, 55:1187-1194.
113. Zolkiewski M. A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol. Microbiol. 2006, 61:1094-1100.
114. Zotta T., Asterinou K., Rossano R., Ricciardi A., Varcamonti M., Parente E. Effect of inactivation of stress response regulators on the growth and survival of Streptococcus thermophilus Sfi39. Int. J. Food Microbiol. 2009, 129:211-220.
115. Zuber U., Schumann W. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J. Bacteriol. 1994, 176:1359-1363.