Chaperone-protease systems in regulation and protein quality control in Bacillus subtilis

Research in Microbiology

Volumn 160, Issue 9, 2009, Pages 637-644

  Molière, Noël ^a   Turgay, Kürşad ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

AAA+; Bacillus subtilis; Heat shock; Hsp100 Clp; Protein quality control; Regulatory proteolysis

Indexed keywords

ADAPTOR PROTEIN; BACTERIAL PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN; MUTANT PROTEIN; PEPTIDE DERIVATIVE; PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL INCLUSION; CELLULAR DISTRIBUTION; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE CONTROL; GENE DELETION; GENE MUTATION; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SPOROGENESIS;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 72049104795     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2009.08.020     Document Type: Article

References (73)

1. Andersson F.I., Blakytny R., Kirstein J., Turgay K., Bukau B., Mogk A., and Clarke A.K. Cyanobacterial ClpC/HSP100 protein displays intrinsic chaperone activity. J. Biol. Chem. 28 (2006) 5468-5475
2. Baker T.A., and Sauer R.T. ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem. Sci. 31 (2006) 647-653
3. Bewley M.C., Graziano V., Griffin K., and Flanagan J.M. Turned on for degradation: ATPase-independent degradation by ClpP. J. Struct. Biol. 165 (2009) 118-125
4. Brotz-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., and Labischinski H. Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat. Med. 11 (2005) 1082-1087
5. Bukau B., Weissman J., and Horwich A. Molecular chaperones and protein quality control. Cell 125 (2006) 443-451
6. Darmon E., Noone D., Masson A., Bron S., Kuipers O.P., Devine K.M., and van Dijl J.M. A novel class of heat and secretion stress-responsive genes is controlled by the autoregulated CssRS two-component system of Bacillus subtilis. J. Bacteriol. 184 (2002) 5661-5671
7. Darwin K.H. Prokaryotic ubiquitin-like protein (Pup), proteasomes and pathogenesis. Nat. Rev. Microbiol. 7 (2009) 485-491
8. Derre I., Rapoport G., Devine K., Rose M., and Msadek T. ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol. Microbiol. 32 (1999) 581-593
9. Deuerling E., Paeslack B., and Schumann W. The ftsH gene of Bacillus subtilis is transiently induced after osmotic and temperature upshift. J. Bacteriol. 177 (1995) 4105-4112
10. Deuerling E., Schulze-Specking A., Tomoyasu T., Mogk A., and Bukau B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400 (1999) 693-696
11. Dougan D.A., Mogk A., and Bukau B. Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell. Mol. Life Sci. 59 (2002) 1607-1616
12. Dougan D.A., Reid B.G., Horwich A.L., and Bukau B. ClpS, a substrate modulator of the ClpAP machine. Mol. Cell 9 (2002) 673-683
13. Dubnau D., and Roggiani M. Growth medium-independent genetic competence mutants of Bacillus subtilis. J. Bacteriol. 172 7 (1990) 4048-4055
14. Dworkin J., and Losick R. Developmental commitment in a bacterium. Cell 121 (2005) 401-409
15. Erbse A., Schmidt R., Bornemann T., Schneider-Mergener J., Mogk A., Zahn R., Dougan D.A., and Bukau B. ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439 (2006) 753-756
16. Fuhrmann J., Schmidt A., Spiess S., Lehner A., Turgay K., Mechtler K., Charpentier E., and Clausen T. McsB is a protein arginine kinase that phosphorylates and inhibits the heat-shock regulator CtsR. Science 324 (2009) 1323-1327
17. Gamer J., Multhaup G., Tomoyasu T., McCarty J.S., Rudiger S., Schonfeld H.J., Schirra C., Bujard H., and Bukau B. A cycle of binding and release of the DnaK, DnaJ and GrpE chaperones regulates activity of the Escherichia coli heat shock transcription factor sigma32. EMBO J. 15 (1996) 607-617
18. Garg S.K., Kommineni S., Henslee L., Zhang Y., and Zuber P. The YjbH protein of Bacillus subtilis enhances ClpXP-catalyzed proteolysis of Spx. J. Bacteriol. 191 (2009) 1268-1277
19. Genevaux P., Keppel F., Schwager F., Langendijk-Genevaux P.S., Hartl F.U., and Georgopoulos C. In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Rep. 5 (2004) 195-200
20. Gerth U., Wipat A., Harwood C.R., Carter N., Emmerson P.T., and Hecker M. Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene 181 (1996) 77-83
21. Gerth U., Kruger E., Derre I., Msadek T., and 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. 28 (1998) 787-802
22. Grossman A.D., Erickson J.W., and Gross C.A. The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38 (1984) 383-390
23. Hahn J., Kramer N., Briley Jr. K., and Dubnau D. McsA and B mediate the delocalization of competence proteins from the cell poles of Bacillus subtilis. Mol. Microbiol. 72 (2009) 202-215
24. Hartl F.U., and Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16 (2009) 574-581
25. Hou J.Y., Sauer R.T., and Baker T.A. Distinct structural elements of the adaptor ClpS are required for regulating degradation by ClpAP. Nat. Struct. Mol. Biol. 15 (2008) 288-294
26. Hyyrylainen H.L., Bolhuis A., Darmon E., Muukkonen L., Koski P., Vitikainen M., Sarvas M., Pragai Z., Bron S., van Dijl J.M., and Kontinen V.P. A novel two-component regulatory system in Bacillus subtilis for the survival of severe secretion stress. Mol. Microbiol. 41 (2001) 1159-1172
27. Jenal U., and Fuchs T. An essential protease involved in bacterial cell-cycle control. EMBO J. 17 (1998) 5658-5669
28. Jennings L.D., Lun D.S., Medard M., and Licht S. ClpP hydrolyzes a protein substrate processively in the absence of the ClpA ATPase: mechanistic studies of ATP-independent proteolysis. Biochemistry 47 (2008) 11536-11546
29. Jurgen B., Hanschke R., Sarvas M., Hecker M., and Schweder T. Proteome and transcriptome based analysis of Bacillus subtilis cells overproducing an insoluble heterologous protein. Appl. Microbiol. Biotechnol. 55 (2001) 326-332
30. Kain J., He G.G., and Losick R. Polar localization and compartmentalization of ClpP proteases during growth and sporulation in Bacillus subtilis. J. Bacteriol. 190 (2008) 6749-6757
31. Kirstein J., and Turgay K. A new tyrosine phosphorylation mechanism involved in signal transduction in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 9 (2005) 182-188
32. Kirstein J., Zuhlke D., Gerth U., Turgay K., and Hecker M. A tyrosine kinase and its activator control the activity of the CtsR heat shock repressor in B. subtilis. EMBO J. 24 (2005) 3435-3445
33. Kirstein J., Schlothauer T., Dougan D.A., Lilie H., Tischendorf G., Mogk A., Bukau B., and Turgay K. Adaptor protein controlled oligomerization activates the AAA+ protein ClpC. EMBO J. 25 7 (2006) 1481-1491
34. Kirstein J., Dougan D.A., Gerth U., Hecker M., and Turgay K. The tyrosine kinase McsB is a regulated adaptor protein for ClpCP. EMBO J. 26 (2007) 2061-2070
35. Kirstein J., Strahl H., Moliere N., Hamoen L.W., and Turgay K. Localization of general and regulatory proteolysis in Bacillus subtilis cells. Mol. Microbiol. 70 3 (2008) 682-694
36. Kirstein J., Hoffmann A., Lilie H., Schmidt R., Rübsamen-Waigmann H., Brötz-Oesterhelt H., Mogk A., and Turgay K. The antibiotic ADEP reprogrammes ClpP, switching it from a regulated to an uncontrolled protease. EMBO Mol. Med. 1 (2009) 37-49
37. Kirstein J., Moliere N., Dougan D., and Turgay K. Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat. Rev. Microbiol. 7 (2009) 589-599
38. Kock H., Gerth U., and Hecker M. MurAA, catalysing the first committed step in peptidoglycan biosynthesis, is a target of Clp-dependent proteolysis in Bacillus subtilis. Mol. Microbiol. 51 (2004) 1087-1102
39. Kock H., Gerth U., and Hecker M. The ClpP peptidase is the major determinant of bulk protein turnover in Bacillus subtilis. J. Bacteriol. 186 17 (2004) 5856-5864
40. Kojetin D.J., McLaughlin P.D., Thompson R.J., Dubnau D., Prepiak P., Rance M., and Cavanagh J. Structural and motional contributions of the Bacillus subtilis ClpC N-domain to adaptor protein interactions. J. Mol. Biol. 387 (2009) 639-652
41. Kong L., and Dubnau D. Regulation of competence-specific gene expression by Mec-mediated protein-protein interaction in Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 5793-5797
42. Kramer G., Boehringer D., Ban N., and Bukau B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16 (2009) 589-597
43. Kruger E., and Hecker M. The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J. Bacteriol. 180 (1998) 6681-6688
44. Kruger E., Witt E., Ohlmeier S., Hanschke R., and Hecker M. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J. Bacteriol. 182 (2000) 3259-3265
45. Larsson J.T., Rogstam A., and von Wachenfeldt C. YjbH is a novel negative effector of the disulphide stress regulator, Spx, in Bacillus subtilis. Mol. Microbiol. 66 (2007) 669-684
46. Levchenko I., Seidel M., Sauer R.T., and Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science 289 5488 (2000) 2354-2356
47. Li J., and Sha B. Crystal structure of the E. coli Hsp100 ClpB N-terminal domain. Structure 11 (2003) 323-328
48. McGrath P.T., Iniesta A.A., Ryan K.R., Shapiro L., and McAdams H.H. A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124 (2006) 535-547
49. Miethke M., Hecker M., and Gerth U. Involvement of Bacillus subtilis ClpE in CtsR degradation and protein quality control. J. Bacteriol. 188 (2006) 4610-4619
50. Mogk A., Homuth G., Scholz C., Kim L., Schmid F.X., and Schumann W. The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J. 16 (1997) 4579-4590
51. Msadek T., Kunst F., and 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. 91 (1994) 5788-5792
52. Msadek T., Dartois V., Kunst F., Herbaud M.L., Denizot F., and Rapoport G. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol. Microbiol. 27 (1998) 899-914
53. Nakano S., Zheng G., Nakano M.M., and Zuber P. Multiple pathways of Spx (YjbD) proteolysis in Bacillus subtilis. J. Bacteriol. 184 (2002) 3664-3670
54. Paek K.H., and Walker G.C. Escherichia coli dnaK null mutants are inviable at high temperature. J. Bacteriol. 169 (1987) 283-290
55. Pan Q., and Losick R. Unique degradation signal for ClpCP in Bacillus subtilis. J. Bacteriol. 185 (2003) 5275-5278
56. Persuh M., Turgay K., Mandic-Mulec I., and Dubnau D. The N- and C-terminal domains of MecA recognize different partners in the competence molecular switch. Mol. Microbiol. 33 (1999) 886-894
57. Persuh M., Mandic-Mulec I., and Dubnau D. A MecA paralog, YpbH, binds ClpC, affecting both competence and sporulation. J. Bacteriol. 184 (2002) 2310-2313
58. Prepiak P., and Dubnau D. A peptide signal for adapter protein-mediated degradation by the AAA+ protease ClpCP. Mol. Cell. 26 (2007) 639-647
59. Reyes D.Y., and Yoshikawa H. DnaK chaperone machine and trigger factor are only partially required for normal growth of Bacillus subtilis. Biosci. Biotechnol. Biochem. 66 (2002) 1583-1586
60. Riethdorf S., Volker U., Gerth U., Winkler A., Engelmann S., and Hecker M. Cloning, nucleotide sequence, and expression of the Bacillus subtilis lon gene. J. Bacteriol. 176 (1994) 6518-6527
61. Roggiani M., Hahn J., and Dubnau D. Suppression of early competence mutations in Bacillus subtilis by mec mutations. J. Bacteriol. 172 (1990) 4056-4063
62. Schlothauer T., Mogk A., Dougan D.A., Bukau B., and Turgay K. MecA, an adaptor protein necessary for ClpC chaperone activity. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 2306-2311
63. Schulz A., Tzschaschel B., and Schumann W. Isolation and analysis of mutants of the dnaK operon of Bacillus subtilis. Mol. Microbiol. 15 (1995) 421-429
64. Schulz A., and Schumann W. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178 (1996) 1088-1093
65. Simmons L.A., Grossman A.D., and Walker G.C. Clp and Lon proteases occupy distinct subcellular positions in Bacillus subtilis. J. Bacteriol. 190 (2008) 6758-6768
66. Stanne T.M., Pojidaeva E., Andersson F.I., and Clarke A.K. Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J. Biol. Chem. 282 (2007) 14394-14402
67. Tomoyasu T., Ogura T., Tatsuta T., and Bukau B. Levels of DnaK and DnaJ provide tight control of heat shock gene expression and protein repair in Escherichia coli. Mol. Microbiol. 30 (1998) 567-581
68. Turgay K., Hamoen L.W., Venema G., and Dubnau D. Biochemical characterization of a molecular switch involving the heat shock protein ClpC, which controls the activity of ComK, the competence transcription factor of Bacillus subtilis. Genes Dev. 11 (1997) 119-128
69. Turgay K., Hahn J., Burghoorn J., and Dubnau D. Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J. 17 (1998) 6730-6738
70. Volker U., Engelmann S., Maul B., Riethdorf S., Volker A., Schmid R., Mach H., and Hecker M. Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology 140 (1994) 741-752
71. Weibezahn J., Schlieker C., Tessarz P., Mogk A., and Bukau B. Novel insights into the mechanism of chaperone-assisted protein disaggregation. Biol. Chem. 386 (2005) 739-744
72. Young J.C., Agashe V.R., Siegers K., and Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell. Biol. 5 (2004) 781-791
73. Zeth K., Ravelli R.B., Paal K., Cusack S., Bukau B., and Dougan D.A. Structural analysis of the adaptor protein ClpS in complex with the N-terminal domain of ClpA. Nat. Struct. Biol. 9 (2002) 906-911