Real-time attack of LL-37 on single Bacillus subtilis cells

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 6, 2013, Pages 1511-1520

  Barns, Kenneth J ^a   Weisshaar, James C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Antimicrobial peptide; Bacillus subtilis; Fluorescence microscopy; LL 37

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DYE; SYTOX GREEN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; GROWTH INHIBITION; GROWTH RATE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; SINGLE CELL ANALYSIS; STAINING; TURGOR PRESSURE;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACILLUS SUBTILIS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; MEMBRANE POTENTIALS; MICROBIAL VIABILITY; MICROSCOPY, FLUORESCENCE; TIME FACTORS; TIME-LAPSE IMAGING; VIDEO RECORDING;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 84875361160     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.02.011     Document Type: Article

References (38)

1. K.A. Brogden Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3 2005 238 250
2. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395
3. W.C. Wimley, and K. Hristova Antimicrobial peptides: successes, challenges and unanswered questions J. Membr. Biol. 239 2011 27 34
4. M.N. Melo, R. Ferre, and M.A. Castanho Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations Nat. Rev. Microbiol. 7 2009 245 250
5. J.M. Andrews Determination of minimum inhibitory concentrations J. Antimicrob. Chemother. 48 Suppl. 1 2001 5 16
6. M. Scocchi, A. Tossi, and R. Gennaro Proline-rich antimicrobial peptides: converging to a non-lytic mechanism of action Cell Mol. Life Sci. 68 2011 2317 2330
7. T. Schneider, T. Kruse, R. Wimmer, I. Wiedemann, V. Sass, U. Pag, A. Jansen, A.K. Nielsen, P.H. Mygind, D.S. Raventos, S. Neve, B. Ravn, A.M. Bonvin, L. De Maria, A.S. Andersen, L.K. Gammelgaard, H.G. Sahl, and H.H. Kristensen Plectasin, a fungal defensin, targets the bacterial cell wall precursor Lipid II Science 328 2010 1168 1172
8. M. Pietiainen, M. Gardemeister, M. Mecklin, S. Leskela, M. Sarvas, and V.P. Kontinen Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems Microbiology 151 2005 1577 1592
9. H.W. Huang, F.Y. Chen, and M.T. Lee Molecular mechanism of Peptide-induced pores in membranes Phys. Rev. Lett. 92 2004 198304
10. R.M. Epand, and R.F. Epand Bacterial membrane lipids in the action of antimicrobial agents J. Pept. Sci. 17 2011 298 305
11. Y. Shai Mode of action of membrane active antimicrobial peptides Biopolymers 66 2002 236 248
12. Z. Oren, J.C. Lerman, G.H. Gudmundsson, B. Agerberth, and Y. Shai 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 Pt 3 1999 501 513
13. F. Porcelli, R. Verardi, L. Shi, K.A. Henzler-Wildman, A. Ramamoorthy, and G. Veglia NMR structure of the cathelicidin-derived human antimicrobial peptide LL-37 in dodecylphosphocholine micelles Biochemistry 47 2008 5565 5572
14. C.C. Lee, Y. Sun, S. Qian, and H.W. Huang Transmembrane pores formed by human antimicrobial peptide LL-37 Biophys. J. 100 2011 1688 1696
15. K.A. Henzler Wildman, D.K. Lee, and A. Ramamoorthy Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37 Biochemistry 42 2003 6545 6558
16. D. Sengupta, H. Leontiadou, A.E. Mark, and S.J. Marrink Toroidal pores formed by antimicrobial peptides show significant disorder Biochim. Biophys. Acta 1778 2008 2308 2317
17. H. Leontiadou, A.E. Mark, and S.J. Marrink Antimicrobial peptides in action J. Am. Chem. Soc. 128 2006 12156 12161
18. K.A. Sochacki, K.J. Barns, R. Bucki, and J.C. Weisshaar Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37 Proc. Natl. Acad. Sci. U. S. A. 108 2011 E77 E81
19. A.K. Dunn, and J. Handelsman A vector for promoter trapping in Bacillus cereus Gene 226 1999 297 305
20. C.R. Harwood, and S.M. Cutting Molecular biological methods for Bacillus 1990 John Wiley & Sons
21. M.M. Nakano, Y.P. Dailly, P. Zuber, and D.P. Clark Characterization of anaerobic fermentative growth of Bacillus subtilis: identification of fermentation end products and genes required for growth J. Bacteriol. 179 1997 6749 6755
22. W.S. Rasband ImageJ B. 1997 U.S. National Institutes of Health Maryland, USA (http://rsb.info.nih.gov/ij/)
23. O. Sliusarenko, J. Heinritz, T. Emonet, and C. Jacobs-Wagner High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics Mol. Microbiol. 80 2011 612 627
24. B.L. Roth, M. Poot, S.T. Yue, and P.J. Millard Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain Appl. Environ. Microbiol. 63 1997 2421 2431
25. R. Briandet, P. Lacroix-Gueu, M. Renault, S. Lecart, T. Meylheuc, E. Bidnenko, K. Steenkeste, M.N. Bellon-Fontaine, and M.P. Fontaine-Aupart Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms Appl. Environ. Microbiol. 74 2008 2135 2143
26. M.B. Elowitz, M.G. Surette, P.E. Wolf, J.B. Stock, and S. Leibler Protein mobility in the cytoplasm of Escherichia coli J. Bacteriol. 181 1999 197 203
27. M.C. Konopka, I.A. Shkel, S. Cayley, M.T. Record, and J.C. Weisshaar Crowding and confinement effects on protein diffusion in vivo J. Bacteriol. 188 2006 6115 6123
28. K.A. Martinez II, R.D. Kitko, J.P. Mershon, H.E. Adcox, K.A. Malek, M.B. Berkmen, and J.L. Slonczewski Cytoplasmic pH response to acid stress in individual cells of Escherichia coli and Bacillus subtilis observed by fluorescence ratio imaging microscopy Appl. Environ. Microbiol. 78 2012 3706 3714
29. P. Breeuwer, J. Drocourt, F.M. Rombouts, and T. Abee A novel method for continuous determination of the intracellular pH in bacteria with the internally conjugated fluorescent probe 5 (and 6-)-carboxyfluorescein succinimidyl ester Appl. Environ. Microbiol. 62 1996 178 183
30. R.D. Kitko, R.L. Cleeton, E.I. Armentrout, G.E. Lee, K. Noguchi, M.B. Berkmen, B.D. Jones, and J.L. Slonczewski Cytoplasmic acidification and the benzoate transcriptome in Bacillus subtilis PLoS One 4 2009 e8255
31. P.J. Henderson, J.D. McGivan, and J.B. Chappell The action of certain antibiotics on mitochondrial, erythrocyte and artificial phospholipid membranes. The role of induced proton permeability Biochem. J. 111 1969 521 535
32. A. Lamsa, W.T. Liu, P.C. Dorrestein, and K. Pogliano The Bacillus subtilis cannibalism toxin SDP collapses the proton motive force and induces autolysis Mol. Microbiol. 84 2012 486 500
33. B.S. Schuwirth, M.A. Borovinskaya, C.W. Hau, W. Zhang, A. Vila-Sanjurjo, J.M. Holton, and J.H. Cate Structures of the bacterial ribosome at 3.5 A resolution Science 310 2005 827 834
34. P. Demchick, and A.L. Koch The permeability of the wall fabric of Escherichia coli and Bacillus subtilis J. Bacteriol. 178 1996 768 773
35. T.J. Smith, S.A. Blackman, and S.J. Foster Autolysins of Bacillus subtilis: multiple enzymes with multiple functions Microbiology 146 Pt 2 2000 249 262
36. W. Vollmer, B. Joris, P. Charlier, and S. Foster Bacterial peptidoglycan (murein) hydrolases FEMS Microbiol. Rev. 32 2008 259 286
37. K.A. Sochacki, in: Chemistry, vol. PhD, University of Wisconsin-Madison, Madison, WI, 2011.
38. H.W. Huang Molecular mechanism of antimicrobial peptides: the origin of cooperativity Biochim. Biophys. Acta 1758 2006 1292 1302