The role of thiol oxidative stress response in heat-induced protein aggregate formation during thermotolerance in Bacillus subtilis

Molecular Microbiology

Volumn 91, Issue 5, 2014, Pages 1036-1052

  Runde, Stephanie ^a,b   Molière, Noël ^a,b   Heinz, Anja ^a,d   Maisonneuve, Etienne ^a,e   Janczikowski, Armgard ^b   Elsholz, Alexander K W ^c,f   Gerth, Ulf ^c   Hecker, Michael ^c   Turgay, Kürşad ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; THIOREDOXIN;

ANAEROBIC GROWTH; ARTICLE; BACILLUS SUBTILIS; CELL SURVIVAL; HEAT SHOCK; HEAT TOLERANCE; IN VIVO STUDY; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN PROCESSING; REGULON; WILD TYPE;

BACILLUS SUBTILIS;

ADAPTATION, PHYSIOLOGICAL; ANAEROBIOSIS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; HEAT-SHOCK RESPONSE; HOMEOSTASIS; HOT TEMPERATURE; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; MUTATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN STRUCTURE, QUATERNARY; SULFHYDRYL COMPOUNDS;

EID: 84896718349     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12521     Document Type: Article

References (70)

1. Antelmann, H., and Helmann, J.D. (2011) Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14: 1049-1063.
2. Battesti, A., and Gottesman, S. (2013) Roles of adaptor proteins in regulation of bacterial proteolysis. Curr Opin Microbiol 16: 140-147.
3. Berndt, C., Lillig, C.H., and Holmgren, A. (2008) Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta 1783: 641-650.
4. Elsholz, A.K.W., Michalik, S., Zühlke, D., Hecker, M., and Gerth, U. (2010) CtsR, the Gram-positive master regulator of protein quality control, feels the heat. EMBO J 29: 3621-3629.
5. Elsholz, A.K.W., Turgay, K., Michalik, S., Hessling, B., Gronau, K., Oertel, D., etal. (2012) Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc Natl Acad Sci USA 109: 7451-7456.
6. Engman, J., Rogstam, A., Frees, D., Ingmer, H., and von Wachenfeldt, C. (2012) The YjbH adaptor protein enhances proteolysis of the transcriptional regulator Spx in Staphylococcus aureus. J Bacteriol 194: 1186-1194.
7. Eymann, C., Homuth, G., Scharf, C., and Hecker, M. (2002) Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J Bacteriol 184: 2500-2520.
8. Frees, D., Qazi, S.N.A., Hill, P.J., and Ingmer, H. (2003) Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol Microbiol 48: 1565-1578.
9. Frees, D., Savijoki, K., Varmanen, P., and Ingmer, H. (2007) Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria. Mol Microbiol 63: 1285-1295.
10. Frees, D., Brøndsted, L., and Ingmer, H. (2013) Bacterial proteases and virulence. Subcell Biochem 66: 161-192.
11. Garg, S.K., Kommineni, S., Henslee, L., Zhang, Y., and Zuber, P. (2009) The YjbH protein of Bacillus subtilis enhances ClpXP-catalyzed proteolysis of Spx. J Bacteriol 191: 1268-1277.
12. Glover, J.R., and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82.
13. Göhring, N., Fedtke, I., Xia, G., Jorge, A.M., Pinho, M.G., Bertsche, U., and Peschel, A. (2011) New role of the disulfide stress effector YjbH in β-lactam susceptibility of Staphylococcus aureus. Antimicrob Agents Chemother 55: 5452-5458.
14. Hartl, F.U., Bracher, A., and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332.
15. Hecker, M., Pané-Farré, J., and Völker, U. (2007) SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61: 215-236.
16. Höper, D., Völker, U., and Hecker, M. (2005) Comprehensive characterization of the contribution of individual SigB-dependent general stress genes to stress resistance of Bacillus subtilis. J Bacteriol 187: 2810-2826.
17. Ingmer, H., and Brøndsted, L. (2009) Proteases in bacterial pathogenesis. Res Microbiol 160: 704-710.
18. Kajfasz, J.K., Martinez, A.R., Rivera-Ramos, I., Abranches, J., Koo, H., Quivey, R.G., Jr, and Lemos, J.A. (2009) Role of Clp proteins in expression of virulence properties of Streptococcus mutans. J Bacteriol 191: 2060-2068.
19. Kajfasz, J.K., Abranches, J., and Lemos, J.A. (2011) Transcriptome analysis reveals that ClpXP proteolysis controls key virulence properties of Streptococcus mutans. Microbiology 157: 2880-2890.
20. Kern, R., Malki, A., Holmgren, A., and Richarme, G. (2003) Chaperone properties of Escherichia coli thioredoxin and thioredoxin reductase. Biochem J 371: 965-972.
21. Kim, M., Lee, U., Small, I., des Francs-Small, C.C., and Vierling, E. (2012) Mutations in an Arabidopsis mitochondrial transcription termination factor-related protein enhance thermotolerance in the absence of the major molecular chaperone HSP101. Plant Cell 24: 3349-3365.
22. Kirstein, J., Strahl, H., Molière, N., Hamoen, L.W., and Turgay, K. (2008) Localization of general and regulatory proteolysis in Bacillus subtilis cells. Mol Microbiol 70: 682-694.
23. Kirstein, J., Molière, N., Dougan, D.A., and Turgay, K. (2009) Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat Rev Microbiol 7: 589-599.
24. Kommineni, S., Garg, S.K., Chan, C.M., and Zuber, P. (2011) YjbH-enhanced proteolysis of Spx by ClpXP in Bacillus subtilis is inhibited by the small protein YirB (YuzO). J Bacteriol 193: 2133-2140.
25. Kouwen, T.R.H.M., Andréll, J., Schrijver, R., Dubois, J.-Y.F., Maher, M.J., Iwata, S., etal. (2008) Thioredoxin A active-site mutants form mixed disulfide dimers that resemble enzyme-substrate reaction intermediates. J Mol Biol 379: 520-534.
26. Krüger, E., Witt, E., Ohlmeier, S., Hanschke, R., and Hecker, M. (2000) The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J Bacteriol 182: 3259-3265.
27. Kthiri, F., Le, H.-T., Gautier, V., Caldas, T., Malki, A., Landoulsi, A., etal. (2010) Protein aggregation in a mutant deficient in yajL, the bacterial homolog of the Parkinsonism-associated protein DJ-1. J Biol Chem 285: 10328-10336.
28. Larsson, J.T., Rogstam, A., and von Wachenfeldt, C. (2007) YjbH is a novel negative effector of the disulphide stress regulator, Spx, in Bacillus subtilis. Mol Microbiol 66: 669-684.
29. Le, H.-T., Gautier, V., Kthiri, F., Malki, A., Messaoudi, N., Mihoub, M., etal. (2012) YajL, prokaryotic homolog of parkinsonism-associated protein DJ-1, functions as a covalent chaperone for thiol proteome. J Biol Chem 287: 5861-5870.
30. Lin, A.A., and Zuber, P. (2012) Evidence that a single monomer of Spx can productively interact with RNA polymerase in Bacillus subtilis. J Bacteriol 194: 1697-1707.
31. Lin, A.A., Walthers, D., and Zuber, P. (2013) Residue substitutions near the redox center of Bacillus subtilis Spx affect RNA polymerase interaction, redox control, and Spx-DNA contact at a conserved cis-acting element. J Bacteriol 195: 3967-3978.
32. Lindner, A.B., Madden, R., Demarez, A., Stewart, E.J., and Taddei, F. (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105: 3076-3081.
33. Lindquist, S. (1986) The heat-shock response. Annu Rev Biochem 55: 1151-1191.
34. Ling, J., Cho, C., Guo, L.-T., Aerni, H.R., Rinehart, J., and Söll, D. (2012) Protein aggregation caused by aminoglycoside action is prevented by a hydrogen peroxide scavenger. Mol Cell 48: 713-722.
35. Luo, Y., and Helmann, J.D. (2012) Analysis of the role of Bacillus subtilis σ(M) in β-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol Microbiol 83: 623-639.
36. Maisonneuve, E., Fraysse, L., Moinier, D., and Dukan, S. (2008a) Existence of abnormal protein aggregates in healthy Escherichia coli cells. J Bacteriol 190: 887-893.
37. Maisonneuve, E., Ezraty, B., and Dukan, S. (2008b) Protein aggregates: an aging factor involved in cell death. J Bacteriol 190: 6070-6075.
38. Mogk, A., Homuth, G., Scholz, C., Kim, L., Schmid, F.X., and Schumann, W. (1997) The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J 16: 4579-4590.
39. Mols, M., and Abee, T. (2011) Primary and secondary oxidative stress in Bacillus. Environ Microbiol 13: 1387-1394.
40. Mostertz, J., Hochgräfe, F., Jürgen, B., Schweder, T., and Hecker, M. (2008) The role of thioredoxin TrxA in Bacillus subtilis: a proteomics and transcriptomics approach. Proteomics 8: 2676-2690.
41. Möller, M.C., and Hederstedt, L. (2008) Extracytoplasmic processes impaired by inactivation of trxA (thioredoxin gene) in Bacillus subtilis. J Bacteriol 190: 4660-4665.
42. Nakano, M.M., and Zuber, P. (1998) Anaerobic growth of a 'strict aerobe' (Bacillus subtilis). Annu Rev Microbiol 52: 165-190.
43. Nakano, M.M., Hajarizadeh, F., Zhu, Y., and Zuber, P. (2001) Loss-of-function mutations in yjbD result in ClpX- and ClpP-independent competence development of Bacillus subtilis. Mol Microbiol 42: 383-394.
44. Nakano, M.M., Lin, A., Zuber, C.S., Newberry, K.J., Brennan, R.G., and Zuber, P. (2010) Promoter recognition by a complex of Spx and the C-terminal domain of the RNA polymerase alpha subunit. PLoS ONE 5: e8664.
45. Nakano, S., Zheng, G., Nakano, M.M., and Zuber, P. (2002) Multiple pathways of Spx (YjbD) proteolysis in Bacillus subtilis. J Bacteriol 184: 3664-3670.
46. Nakano, S., Nakano, M.M., Zhang, Y., Leelakriangsak, M., and Zuber, P. (2003a) A regulatory protein that interferes with activator-stimulated transcription in bacteria. Proc Natl Acad Sci USA 100: 4233-4238.
47. Nakano, S., Küster-Schöck, E., Grossman, A.D., and Zuber, P. (2003b) Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis. Proc Natl Acad Sci USA 100: 13603-13608.
48. Nakano, S., Erwin, K.N., Ralle, M., and Zuber, P. (2005) Redox-sensitive transcriptional control by a thiol/disulphide switch in the global regulator, Spx. Mol Microbiol 55: 498-510.
49. Newberry, K.J., Nakano, S., Zuber, P., and Brennan, R.G. (2005) Crystal structure of the Bacillus subtilis anti-alpha, global transcriptional regulator, Spx, in complex with the alpha C-terminal domain of RNA polymerase. Proc Natl Acad Sci USA 102: 15839-15844.
50. Parsell, D.A., Kowal, A.S., Singer, M.A., and Lindquist, S. (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475-478.
51. Reder, A., Pöther, D.-C., Gerth, U., and Hecker, M. (2012) The modulator of the general stress response, MgsR, of Bacillus subtilis is subject to multiple and complex control mechanisms. Environ Microbiol 14: 2838-2850.
52. Remington, S.J. (2006) Fluorescent proteins: maturation, photochemistry and photophysics. Curr Opin Struct Biol 16: 714-721.
53. Renzoni, A., Andrey, D.O., Jousselin, A., Barras, C., Monod, A., Vaudaux, P., etal. (2011) Whole genome sequencing and complete genetic analysis reveals novel pathways to glycopeptide resistance in Staphylococcus aureus. PLoS ONE 6: e21577.
54. Rochat, T., Nicolas, P., Delumeau, O., Rabatinová, A., Korelusová, J., Leduc, A., etal. (2012) Genome-wide identification of genes directly regulated by the pleiotropic transcription factor Spx in Bacillus subtilis. Nucleic Acids Res 40: 9571-9583.
55. Rogstam, A., Larsson, J.T., Kjelgaard, P., and von Wachenfeldt, C. (2007) Mechanisms of adaptation to nitrosative stress in Bacillus subtilis. J Bacteriol 189: 3063-3071.
56. Scharf, C., Riethdorf, S., Ernst, H., Engelmann, S., Völker, U., and Hecker, M. (1998) Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J Bacteriol 180: 1869-1877.
57. Schlothauer, T., Mogk, A., Dougan, D.A., Bukau, B., and Turgay, K. (2003) MecA, an adaptor protein necessary for ClpC chaperone activity. Proc Natl Acad Sci USA 100: 2306-2311.
58. Schmidt, A., Trentini, D.B., Spiess, S., Fuhrmann, J., Ammerer, G., Mechtler, K., and Clausen, T. (2013) Quantitative phosphoproteomics reveals the role of protein arginine phosphorylation in the bacterial stress response. Mol Cell Proteomics. doi:10.1074/mcp.M113.032292
59. Shoji, M., Cui, L., Iizuka, R., Komoto, A., Neoh, H., Watanabe, Y., etal. (2011) walK and clpP mutations confer reduced vancomycin susceptibility in Staphylococcus aureus. Antimicrob Agents Chemother 55: 3870-3881.
60. Smits, W.K., Dubois, J.-Y.F., Bron, S., Dijl, J.M., and Van Kuipers, O.P. (2005) Tricksy business: transcriptome analysis reveals the involvement of thioredoxin A in redox homeostasis, oxidative stress, sulfur metabolism, and cellular differentiation in Bacillus subtilis. J Bacteriol 187: 3921-3930.
61. Tyedmers, J., Mogk, A., and Bukau, B. (2010) Cellular strategies for controlling protein aggregation. Nat Rev Mol Cell Biol 11: 777-788.
62. Versteeg, S., Mogk, A., and Schumann, W. (1999) The Bacillus subtilis htpG gene is not involved in thermal stress management. Mol Gen Genet 261: 582-588.
63. Völker, U., Mach, H., Schmid, R., and Hecker, M. (1992) Stress proteins and cross-protection by heat shock and salt stress in Bacillus subtilis. J Gen Microbiol 138: 2125-2135.
64. Völker, U., Maul, B., and Hecker, M. (1999) Expression of the sigmaB-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis. J Bacteriol 181: 3942-3948.
65. Weibezahn, J., Tessarz, P., Schlieker, C., Zahn, R., Maglica, Z., Lee, S., etal. (2004) Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119: 653-665.
66. Wickner, S., Maurizi, M.R., and Gottesman, S. (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science 286: 1888-1893.
67. Winkler, J., Seybert, A., König, L., Pruggnaller, S., Haselmann, U., Sourjik, V., etal. (2010) Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J 29: 910-923.
68. Winter, J., Ilbert, M., Graf, P.C.F., Ozcelik, D., and Jakob, U. (2008) Bleach activates a redox-regulated chaperone by oxidative protein unfolding. Cell 135: 691-701.
69. Zhang, Y., and Zuber, P. (2007) Requirement of the zinc-binding domain of ClpX for Spx proteolysis in Bacillus subtilis and effects of disulfide stress on ClpXP activity. J Bacteriol 189: 7669-7680.
70. Zuber, P. (2009) Management of oxidative stress in Bacillus. Annu Rev Microbiol 63: 575-597.