Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems

Microbiology

Volumn 151, Issue 5, 2005, Pages 1577-1592

  Pietiäinen, Milla ^a   Gardemeister, Marika ^a   Mecklin, Maria ^a   Leskelä, Soile ^a   Sarvas, Matti ^a   Kontinen, Vesa P ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DEFENSIN 1; METHYLTRANSFERASE; PEPTIDE DERIVATIVE; PG 1; POLYLYSINE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN SIGM; PROTEIN SIGW; REGULATOR PROTEIN; SIGMA FACTOR; TRANSCRIPTION FACTOR; TRITON X 100; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL MEMBRANE; CONTROLLED STUDY; DNA DETERMINATION; DRUG SPECIFICITY; EXTRACELLULAR SPACE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INDUCTION; NONHUMAN; PRIORITY JOURNAL; REGULON; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STRESS;

ANTIMICROBIAL CATIONIC PEPTIDES; BACILLUS SUBTILIS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEOME; SIGMA FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS;

EID: 19044379164     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27761-0     Document Type: Article

References (41)

1. Abachin, E., Poyart, C., Pellegrini, E., Milohanic, E., Fiedler, F., Berche, P. & Trieu Cuot, P. (2002). Formation of D-alanyllipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol Microbiol 43, 1-14.
2. Anagnostopoulos, C. &, Spizizen, J. (1961). Requirements for transformation of Bacillus subtilis. J Bacteriol 81, 741-746.
3. Asai, K., Yamaguchi, H., Kang, C. M., Yoshida, K., Fujita, Y. & Sadaie, Y. (2003). DNA microarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett 220, 155-160.
4. Aumelas, A., Mangoni, M., Roumestand, C., Chiche, L., Despaux, E., Grassy, G., Calas, B. & Chavanieu, A. (1996). Synthesis and solution structure of the antimicrobial peptide protegrin-1. Eur J Biochem 237, 575-583.
5. Breukink, E., Wiedemann, I., van Kraaij, C., Kuipers, O. P., Sahl, H. & de Kruijff, B. (1999). Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286, 2361-2364.
6. Brotz, H., Josten, M., Wiedemann, I., Schneider, U., Gotz, F., Bierbaum, G. & Sahl, H. G. (1998). Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics. Mol Microbiol 30, 317-327.
7. Cao, M. & Helmann, J. D. (2002). Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors. J Bacteriol 184, 6123-6129.
8. X factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J Bacteriol 186, 1136-1146.
9. Cao, M., Kobel, P. A., Morshedi, M. M., Wu, M. F., Paddon, C. & Helmann, J. D. (2002a). Defining the Bacillus subtilis sigma (W) regulon: a comparative analysis of promoter consensus search, runoff transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J Mol Biol 316, 443-457.
10. Cao, M., Wang, T., Ye, R. & Helmann, J. D. (2002b). Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis sigma (W) and sigma (M) regulons. Mol Microbiol 45, 1267-1276.
11. Fahrner, R. L., Dieckmann, T., Harwig, S. S., Lehrer, R. I., Eisenberg, D. & Feigon, J. (1996). Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes. Chem Biol 3, 543-550.
12. Harwig, S. S., Waring, A., Yang, H. J., Cho, Y., Tan, L. & Lehrer, R. I. (1996). Intramolecular disulfide bonds enhance the antimicrobial and lytic activities of protegrins at physiological sodium chloride concentrations. Eur J Biochem 240, 352-357.
13. Helmann, J. D. (2002). The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46, 47-110.
14. Henzler Wildman, K. A., Lee, D. K. & Ramamoorthy, A. (2003). Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry 42, 6545-6558.
15. Horsburgh, M. J. & Moir, A. (1999). Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol Microbiol 32, 41-50.
16. Huang, X. & Helmann, J. D. (1998). Identification of target promoters for the Bacillus subtilis sigma X factor using a consensus-directed search. J Mol Biol 279, 165-173.
17. Huang, X., Fredrick, K. L. & Helmann, J. D. (1998). Promoter recognition by Bacillus subtilis sigma W: autoregulation and partial overlap with the sigma X regulon. J Bacteriol 180, 3765-3770.
18. Huang, X., Gaballa, A., Cao, M. & Helmann, J. D. (1999). Identification of target promoters for the Bacillus subtilis extracytoplasmic function sigma factor, sigma W. Mol Microbiol 31, 361-371.
19. Johansson, J., Gudmundsson, G. H., Rottenberg, M. E., Berndt, K. D. & Agerberth, B. (1998). Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J Biol Chem 273, 3718-3724.
20. Joseph, P., Fichant, G., Quentin, Y. & Denizot, F. (2002). Regulatory relationship of two-component and ABC transporter systems and clustering of their genes in the Bacillus/Clostridium group, suggest a functional link between them. J Mol Microbiol Biotechnol 4, 503-513.
21. Kunst, F., Ogasawara, N., Moszer, I. & 148 other authors (1997). The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249-256.
22. Lehrer, R. I. & Ganz, T. (2002). Defensins of vertebrate animals. Curr Opin Immunol 14, 96-102.
23. Mascher, T., Margulis, N. G., Wang, T., Ye, R. W. & Helmann, J. D. (2003). Cell wall stress responses in Bacillus subtilis: the regulatory network of the bacitracin stimulon. Mol Microbiol 50, 1591-1604.
24. Mascher, T., Zimmer, S. L., Smith, T. A. & Helmann, J. D. (2004). Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob Agents Chemother 48, 2888-2896.
25. Ogura, M. & Tanaka, T. (2002). Recent progress in Bacillus subtilis two-component regulation. Front Biosci 7, d1815-d1824.
26. Ohki, R., Tateno, K., Okada, Y., Okajima, H., Asai, K., Sadaie, Y., Murata, M. & Aiso, T. (2003a). A bacitracin-resistant Bacillus subtilis gene encodes a homologue of the membrane-spanning subunit of the Bacillus licheniformis ABC transporter. J Bacteriol 185, 51-59.
27. Ohki, R., Giyanto, Tateno, K., Masuyama, W., Moriya, S., Kobayashi, K. & Ogasawara, N. (2003b). The BceRS two-component regulatory system induces expression of the bacitracin transporter, BceAB, in Bacillus subtilis. Mol Microbiol 49, 1135-1144.
28. Oren, Z., Lerman, J. C., Gudmundsson, G. H., Agerberth, B. & Shai, Y. (1999). Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem J 341, 501-513.
29. Pascale, J., Guiseppi, A., Sorokin, A. & Denizot, F. (2004). Characterization of the Bacillus subtilis YxdJ response regulator as the inducer of expression for the cognate ABC transporter YxdLM. Microbiology 150, 2609-2617.
30. Perego, M., Glaser, P., Minutello, A., Strauch, M. A., Leopold, K. & Fischer, W. (1995). Incorporation of D-alanine into lipoteichoic acid and wall teichoic acid in Bacillus subtilis. Identification of genes and regulation. J Biol Chem 270, 15598-15606.
31. Peschel, A., Otto, M., Jack, R. W., Kalbacher, H., Jung, G. & Gotz, F. (1999). Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins and other antimicrobial peptides. J Biol Chem 274, 8405-8410.
32. Podlesek, Z., Comino, A., Herzog-Velikonja, B., Zgur-Bertok, D., Komel, R. & Grabnar, M. (1995). Bacillus licheniformis bacitracin-resistance ABC transporter: relationship to mammalian multidrug resistance. Mol Microbiol 16, 969-976.
33. Schobel, S., Zellmeier, S., Schumann, W. & Wiegert, T. (2004). The Bacillus subtilis sigmaW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol Microbiol 52, 1091-1105.
34. Thackray, P. D. & Moir, A. (2003). SigM, an extracytoplasmic function sigma factor of Bacillus subtilis, is activated in response to cell wall antibiotics, ethanol, heat, acid, and superoxide stress. J Bacteriol 185, 3491-3498.
35. Turner, J., Cho, Y., Dinh, N. N., Waring, A. J. & Lehrer, R. I. (1998). Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob Agents Chemother 42, 2206-2214.
36. Vaara, M. & Vaara, T. (1983). Polycations as outer membrane-disorganizing agents. Antimicrob Agents Chemother 24, 114-122.
37. Vagner, V., Dervyn, E. & Ehrlich, S. D. (1998). A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144, 3097-3104.
38. Wiegert, T., Homuth, G., Versteeg, S. & Schumann, W. (2001). Alkaline shock induces the Bacillus subtilis sigma (W) regulon. Mol Microbiol 41, 59-71.
39. Yang, L., Weiss, T. M., Lehrer, R. I. & Huang, H. W. (2000). Crystallization of antimicrobial pores in membranes: magainin and protegrin. Biophys J 79, 2002-2009.
40. Yeaman, M. R. & Yount, N. Y. (2003). Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55, 27-55.
41. Zasloff, M. (2002). Antimicrobial peptides of multicellular organisms. Nature 415, 389-395.