Proteomic response of Bacillus subtilis to lantibiotics reflects differences in interaction with the cytoplasmic membrane

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 11, 2012, Pages 5749-5757

  Wenzel, Michaela ^a   Kohl, Bastian ^a   Münch, Daniela ^b   Raatschen, Nadja ^a   Albada, H Bauke ^a   Hamoen, Leendert ^c   Metzler Nolte, Nils ^a   Sahl, Hans Georg ^b   Bandow, Julia E ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACITRACIN; GALLIDERMIN; GRAMICIDIN S; MERSACIDIN; NISIN; VALINOMYCIN; VANCOMYCIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BIOSYNTHESIS; CELL INTERACTION; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CONTROLLED STUDY; DRUG RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BACTERIOCINS; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL WALL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MEMBRANE POTENTIALS; NISIN; PEPTIDES; POTASSIUM; PROTEOME; STRUCTURE-ACTIVITY RELATIONSHIP; URIDINE DIPHOSPHATE N-ACETYLMURAMIC ACID;

EID: 84868028806     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01380-12     Document Type: Article

References (55)

1. Anagnostopoulos C, Spizizen J. 1961. Requirements for transformation in Bacillus subtilis. J. Bacteriol. 81:741-746.
2. Bandow JE. 2005. Proteomic approaches to antibiotic drug discovery. Curr. Protoc. Microbiol. 1:1F.2.
3. Bandow JE, et al. 2008. Improved image analysis workflow for 2D gels enables large-scale 2D gel-based proteomics studies - COPD biomarker discovery study. Proteomics 8:3030-3041.
4. Bandow JE, Brötz H, Leichert LI, Labischinski H, Hecker M. 2003. Proteomic approach to understanding antibiotic action. Antimicrob. Agents Chemother. 47:948-955.
5. Bandow JE, Metzler-Nolte N. 2009. New ways of killing the beast: prospects for inorganic-organic hybrid nanomaterials as antibacterial agents. Chembiochem 10:2847-2850.
6. Barrett MS, Wenzel RP, Jones RN. 1992. In vitro activity of mersacidin (M87-1551), an investigational peptide antibiotic tested against Grampositive bloodstream isolates. Diagn. Microbiol. Infect. Dis. 15:641-644.
7. Bierbaum G, Sahl HG. 2009. Lantibiotics: mode of action, biosynthesis and bioengineering. Curr. Pharm. Biotechnol. 10:2-18.
8. Bonelli RR, Schneider T, Sahl HG, Wiedemann I. 2006. Insights into in vivo activities of lantibiotics from gallidermin and epidermin mode-of-action studies. Antimicrob. Agents Chemother. 50:1449-1457.
9. Breukink E, et al. 2003. Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes. J. Biol. Chem. 278:19898-19903.
10. Brötz-Österhelt H, Sass P. 2010. Postgenomic strategies in antibacterial drug discovery. Future Microbiol. 5:1553-1579.
11. Brötz-Österhelt H, Brunner NA. 2008. How many modes of action should an antibiotic have? Curr. Opin. Pharmacol. 8:564-573.
12. Brötz-Oesterhelt H, et al. 2005. Dysregulation of bacterial proteolytic machinery by a new class of antibiotics. Nat. Med. 11:1082-1087.
13. Brötz H, Sahl HG. 2000. New insights into the mechanism of action of lantibiotics - diverse biological effects by binding to the same molecular target. J. Antimicrob. Chemother. 46:1-6.
14. Brötz H, Bierbaum G, Leopold K, Reynolds PE, Sahl HG. 1998. The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob. Agents Chemother. 42:154-160.
15. Bugg TDH, Braddick D, Dowson CG, Roper DI. 2011. Bacterial cell wall assembly: still an attractive antibacterial target. Trends Biotechnol. 29:167-173.
16. Christ K, et al. 2008. Membrane lipids determine the antibiotic activity of the lantibiotic gallidermin. J. Membr. Biol. 226:9-16.
17. Clejan S, Krulwich TA, Mondrus KR, Seto-Young D. 1986. Membrane lipid composition of obligately and fakultatively alkalophilic strains of Bacillus spp. J. Bacteriol. 168:334-340.
18. Duax WL, et al. 1996. Molecular structure and mechanisms of action of cyclic and linear ion transport antibiotics. Biopolymers 40:141-155.
19. Engl C, et al. 2009. In vivo localizations of membrane stress controllers PspA and PspG in Escherichia coli. Mol. Microbiol. 73:382-396.
20. Eymann C, et al. 2004. A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4:2849-2876.
21. Garti-Levi S, Hazan R, Kain J, Fujita M, Ben-Yehuda S. 2008. The FtsEX ABC transporter directs cellular differentiation in Bacillus subtilis. Mol. Microbiol. 69:1018-1028.
22. + adaptor protein PspA is an oligomeric ring. J. Biol. Chem. 279: 8862-8866.
23. Hasper HE, de Kruijff B, Breukink E. 2004. Assembly and stability of nisin-lipid II pores. Biochemistry 43:11567-11575.
24. Hyyryläinen HL, Sarvay M, Kontinen VP. 2005. Transcriptome analysis of the secretion stress response of Bacillus subtilis. Appl. Microbiol. Biotechnol. 67:389-396.
25. Kaprel'iants AS, et al. 1977. Membranes of bacteria and mechanism of action of the antibiotic gramicidin S. Biokhimiia. 42:329-337.
26. Katsu T, et al. 1989. Mechanism of membrane damage induced by the amphiphilic peptides gramicidin S and melittin. Biochim. Biophys. Acta 983:135-141.
27. Kobayashi R, Suzuki T, Yoshida M. 2007. Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66:100-109.
28. Lambert MP, Neuhaus FC. 1972. Mechanism of D-cycloserine action: alanine racemase from Escherichia coliW. J. Bacteriol. 109:1156-1161.
29. Mascher T, Zimmer SL, Smith TA, Helmann JD. 2004. Antibiotic-inducible promotor regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob. Agents Chemother. 48:2888-2896.
30. Mogi T, Ui H, Shiomi K, Omura S, Kita K. 2008. Gramicidin S identified as a potent inhibitor for cytochrome bd-type quinol oxidase. FEBS Lett. 582:2299-2302.
31. Orlov DS, Nguyen T, Lehrer RI. 2002. Potassium release, a useful tool for studying antimicrobial peptides. J. Microbiol. Methods 49:325-328.
32. Peschel A, Sahl HG. 2006. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4:529-536.
33. Pinho MG, de Lencastre H, Tomasz A. 2001. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc. Natl. Acad. Sci. U. S. A. 98:10886-10891.
34. Rabilloud T, Strub JM, Luche S, van Dorsselaer A, Lunardi J. 2001. A comparison between SyproRuby and ruthenium II Tris (bathophenanthroline disulfonate) as fluorescent stains for protein detection in gels. Proteomics 1:699-704.
35. Reisinger P, Seidel H, Tschesche H, Hammes WP. 1980. The effect of nisin on murein synthesis. Arch. Microbiol. 127:187-193.
36. Schneider T, et al. 2010. Plectasin, a fungal defensin, targets the bacterial cell wall precursor lipid II. Science 328:1168-1172.
37. Schneider T, et al. 2009. The lipopeptide antibiotic friulimicin B inhibits cell wall biosynthesis through complex formation with bactoprenol phosphate. Antimicrob. Agents Chemother. 53:1610-1618.
38. Schneider T, Sahl HG. 2010. An oldie but a goodie - cell wall biosynthesis as antibiotic target pathway. Int. J. Med. Microbiol. 300:161-169.
39. Singh VK, Jayaswal RK, Wilkinson BJ. 2001. Cell wall-active antibiotic induced proteins of Staphylococcus aureus identified using a proteomic approach. FEMS Microbiol. Lett. 199:79-84.
40. Standar K, et al. 2008. PspA forms large scaffolds in Escherichia coli. FEBS Lett. 582:3585-3589.
41. Strahl H, Hamoen LW. 2010. Membrane potential is important for bacterial cell division. Proc. Natl. Acad. Sci. U. S. A. 27:12281-12286.
42. Stülke J, Hanschke R, Hecker M. 1993. Temporal activation of betaglucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J. Gen. Microbiol. 139:2041-2045.
43. Vicario PP, Green BG, Katzen HM. 1987. A single assay for simultaneously testing effectors of alanine racemase and/or D-alanine:D-alanine ligase. J. Antibiot. (Tokyo) 40:209-216.
44. Vostroknutova GN, Bulgakova VG, Udalova TP, Sepetov NF, Sibel'dina LA. 1981. Localization of gramicidin S on the cytoplasmic membrane of Bacillus brevis and its effect on the activity of membrane enzymes. Biokhimiia 46:657-666.
45. Wadhwani P, Afonin S, Ieronimo M, Buerck J, Ulrich AS. 2006. Optimized protocol for synthesis of cyclic gramicidin S: starting amino acid is key to high yield. J. Org. Chem. 71:55-61.
46. Wecke T, et al. 2009. Daptomycin versus friulimicn B: in-depth profiling of Bacillus subtilis cell envelope stress responses. Antimicrob. Agents Che-mother. 53:1619-1623.
47. Wenzel M, Bandow JE. 2011. Proteomic signatures in antibiotic research. Proteomics 11:3256-3268.
48. Wenzel M, et al. 2011. Proteomic signature of fatty acid biosynthesis inhibition available for in vivo mechanism-of-action studies. Antimicrob. Agents Chemother. 55:2590-2596.
49. WHO. 2012. The evolving threat of antimicrobial resistance - options for action. World Health Organization, Geneva, Switzerland. http://whqlibdoc.who. int/publications/2012/9789241503181-eng.pdf.
50. Wiedemann I, Benz R, Sahl HG. 2004. Lipid II-mediated pore formation by the peptide antibiotic nisin - a black lipid membrane study. J. Bacteriol. 186:3259-3261.
51. Wolf D, et al. 2010. In-depth profiling of LiaR response in Bacillus subtilis. J. Bacteriol. 192:4680-4693.
52. Xiao Z, Xu P. 2007. Acetoin metabolism in bacteria. Crit. Rev. Microbiol. 33:127-140.
53. Yoshida KI, Fujita Y, Ehrlich SD. 2000. An operon for a putative ATP-binding cassette transport system involved in acetoin utilization of Bacillus subtilis. J. Bacteriol. 182:5454-5461.
54. Zegers I, et al. 2006. Crystal structure of Bacillus subtilis TrmB, the tRNA (m7G46) methyltransferase. Nucleic Acids Res. 34:1925-1934.
55. Zhang L, Dhillon P, Yan H, Farmer S, Hancock REW. 2000. Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44: 3317-3321.