Dual Action of BPC194: A Membrane Active Peptide Killing Bacterial Cells

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Moiset, Gemma ^a   Cirac, Anna D ^a,b   Stuart, Marc C A ^a   Marrink, Siewert Jan ^a   Sengupta, Durba ^a,c   Poolman, Bert ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GIRONA   (Spain)

^c NATIONAL CHEMICAL LABORATORY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BPC 194; LIPOSOME; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL INNER MEMBRANE; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BACTERICIDAL ACTIVITY; CELL FUSION; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; DRUG STRUCTURE; ESCHERICHIA COLI; GROWTH INHIBITION; MOLECULAR DYNAMICS; NONHUMAN;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CELL PROLIFERATION; ESCHERICHIA COLI; MEMBRANE FUSION; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MOLECULAR DYNAMICS SIMULATION; PEPTIDES, CYCLIC;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84876455350     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061541     Document Type: Article

References (60)

1. Epand RM, (2003) Fusion peptides and the mechanism of viral fusion. Biochim Biophys Acta 1614: 116-121.
2. Tamm LK, Han X, Li Y, Lai AL, (2002) Structure and function of membrane fusion peptides. Biopolymers 66: 249-260.
3. Brogden KA, (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
4. Järver P, Langel U, (2006) Cell-penetrating peptides-a brief introduction. Biochim Biophys Acta 1758: 260-263.
5. Wadhwani P, Reichert J, Bürck J, Ulrich AS, (2012) Antimicrobial and cell-penetrating peptides induce lipid vesicle fusion by folding and aggregation. Eur Biophys J 41: 177-187.
6. Lai AL, Tamm LK, (2010) Shallow boomerang-shaped influenza hemagglutinin G13A mutant structure promotes leaky membrane fusion. Journal of Biological Chemistry 285: 37467-37475.
7. Yang S-T, Zaitseva E, Chernomordik LV, Melikov K, (2010) Cell-penetrating peptide induces leaky fusion of liposomes containing late endosome-specific anionic lipid. Biophys J 99: 2525-2533.
8. Nicolas P, (2009) Multifunctional host defense peptides: intracellular-targeting antimicrobial peptides. FEBS J 276: 6483-6496.
9. Almeida PF, Pokorny A, (2009) Mechanisms of antimicrobial, cytolytic, and cell-penetrating peptides: from kinetics to thermodynamics. Biochemistry 48: 8083-8093.
10. Hale JD, Hancock RE, (2007) Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev Anti Infect Ther 5: 951-959.
11. Kozlov MM, McMahon HT, Chernomordik LV, (2010) Protein-driven membrane stresses in fusion and fission. Trends Biochem Sci 35: 699-706.
12. Domingues MM, Castanho MARB, Santos NC, (2009) rBPI(21) promotes lipopolysaccharide aggregation and exerts its antimicrobial effects by (hemi)fusion of PG-containing membranes. PLoS ONE 4: e8385.
13. Rausch JM, Marks JR, Rathinakumar R, Wimley WC, (2007) Beta-sheet pore-forming peptides selected from a rational combinatorial library: mechanism of pore formation in lipid vesicles and activity in biological membranes. Biochemistry 46: 12124-12139.
14. Wadhwani P, Epand RF, Heidenreich N, Bürck J, Ulrich AS, et al. (2012) Membrane-active peptides and the clustering of anionic lipids. Biophys J 103: 265-274.
15. Cummings JE, Vanderlick TK, (2007) Aggregation and hemi-fusion of anionic vesicles induced by the antimicrobial peptide cryptdin-4. Biochim Biophys Acta 1768: 1796-1804.
16. Frolov V, Dunina-Barkovskaya AY, Samsonov A, Zimmerberg J, (2003) Membrane permeability changes at early stages of influenza hemagglutinin-mediated fusion. Biophys J 85: 1725-1733.
17. Shai Y, (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66: 236-248.
18. Shai Y, (2002) From innate immunity to de-novo designed antimicrobial peptides. Curr Pharm Des 8: 715-725.
19. Marrink SJ, de Vries AH, Tieleman DP, (2009) Lipids on the move: simulations of membrane pores, domains, stalks and curves. Biochim Biophys Acta 1788: 149-168.
20. Matyus E, Kandt C, Tieleman DP, (2007) Computer Simulation of Antimicrobial Peptides. Curr Med Chem 14: 2789-2798.
21. Bond PJ, Khalid S, (2010) Antimicrobial and cell-penetrating peptides: structure, assembly and mechanisms of membrane lysis via atomistic and coarse-grained molecular dynamics simulations. Protein Pept Lett 17: 1313-1327.
22. Fuertes G, Giménez D, Esteban-Martín S, Sánchez-Muñoz OL, Salgado J, (2011) A lipocentric view of peptide-induced pores. Eur Biophys J 40: 399-415.
23. Mika JT, Moiset G, Cirac AD, Feliu L, Bardají E, et al. (2011) Structural basis for the enhanced activity of cyclic antimicrobial peptides: the case of BPC194. Biochim Biophys Acta 1808: 2197-2205.
24. Monroc S, Badosa E, Feliu L, Planas M, Montesinos E, et al. (2006) De novo designed cyclic cationic peptides as inhibitors of plant pathogenic bacteria. Peptides 27: 2567-2574.
25. Monroc S, Badosa E, Besalú E, Planas M, Bardají E, et al. (2006) Improvement of cyclic decapeptides against plant pathogenic bacteria using a combinatorial chemistry approach. Peptides 27: 2575-2584.
26. Cirac AD, Moiset G, Mika JT, Kocer A, Salvador P, et al. (2011) The molecular basis for antimicrobial activity of pore-forming cyclic peptides. Biophys J 100: 2422-2431.
27. Casadaban MJ, Cohen SN, (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138: 179-207.
28. Van Den Bogaart G, Kusters I, Velásquez J, Mika JT, Krasnikov V, et al. (2008) Dual-color fluorescence-burst analysis to study pore formation and protein-protein interactions. Methods 46: 123-130.
29. Struck DK, Hoekstra D, Pagano RE, (1981) Use of resonance energy transfer to monitor membrane fusion. Biochemistry 20: 4093-4099.
30. Maier O, Oberle V, Hoekstra D, (2002) Fluorescent lipid probes: some properties and applications (a review). Chem Phys Lipids 116: 3-18.
31. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718.
32. van Gunsteren WF, Billeter SR, Eising AA, Hünenberger PH, Krüger P, et al. (1996) Biomolecular Simulation: The {GROMOS96} manual and user guide. vdf Hochschul- verlag AG an der ETH Zürich and BIOMOS b.v., Zürich, Switzerland.
33. Tironi IG, Sperb R, Smith PE, van Gunsteren WF, (1995) A generalized reaction field method for molecular dynamics simulations. The Journal of chemical physics 102: 5451-5459.
34. Berendsen HJC, Postma J, Van Gunsteren W, Hermans J (1981) Interaction models for water in relation to protein hydration. Intermolecular forces 331-342.
35. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM, (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
36. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak J, (1984) Molecular dynamics with coupling to an external bath. The Journal of chemical physics 81: 3684-3690.
37. Leontiadou H, Mark AE, Marrink SJ, (2006) Antimicrobial peptides in action. J Am Chem Soc 128: 12156-12161.
38. Sengupta D, Leontiadou H, Mark AE, Marrink SJ, (2008) Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim Biophys Acta 1778: 2308-2317.
39. Yesylevskyy S, Marrink SJ, Mark AE, (2009) Alternative mechanisms for the interaction of the cell-penetrating peptides penetratin and the TAT peptide with lipid bilayers. Biophys J 97: 40-49.
40. Melo MN, Ferre R, Feliu L, Bardají E, Planas M, et al. (2011) Prediction of Antibacterial Activity from Physicochemical Properties of Antimicrobial Peptides. PLoS ONE 6: e28549.
41. Melo MN, Ferre R, Castanho MARB, (2009) Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 7: 245-250.
42. Ferre R, Melo MN, Correia AD, Feliu L, Bardají E, et al. (2009) Synergistic effects of the membrane actions of cecropin-melittin antimicrobial hybrid peptide BP100. Biophys J 96: 1815-1827.
43. Hobot JA, Carlemalm E, Villiger W, Kellenberger E, (1984) Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J Bacteriol 160: 143-152.
44. Bechinger B, (2009) Rationalizing the membrane interactions of cationic amphipathic antimicrobial peptides by their molecular shape. Curr Opin Colloid Interface Sci 14: 349-355.
45. Smirnova YG, Marrink SJ, Lipowsky R, Knecht V, (2010) Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. J Am Chem Soc 132: 6710-6718.
46. Mirjanian D, Dickey AN, Hoh JH, Woolf TB, Stevens MJ, (2010) Splaying of aliphatic tails plays a central role in barrier crossing during liposome fusion. J Phys Chem B 114: 11061-11068.
47. Baoukina S, Tieleman DP, (2010) Direct simulation of protein-mediated vesicle fusion: lung surfactant protein B. Biophys J. 99: 2134-2142.
48. Risselada HJ, Kutzner C, Grubmüller H, (2011) Caught in the act: visualization of SNARE-mediated fusion events in molecular detail. Chembiochem 12: 1049-1055.
49. Khalfa A, Tarek M, (2010) On the antibacterial action of cyclic peptides: insights from coarse-grained MD simulations. J Phys Chem B 114: 2676-2684.
50. Markvoort AJ, Marrink SJ, (2011) Lipid acrobatics in the membrane fusion arena. Curr Top Memb 68: 259-294.
51. Chernomordik LV, Kozlov MM, (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15: 675-683.
52. Noguchi H, Takasu M, (2001) Fusion pathways of vesicles: a Brownian dynamics simulation. The Journal of chemical physics 115: 9547-9551.
53. Smeijers AF, Markvoort AJ, Pieterse K, Hilbers PAJ, (2006) A detailed look at vesicle fusion. J Phys Chem B 110: 13212-13219.
54. Knecht V, Marrink SJ, (2007) Molecular dynamics simulations of lipid vesicle fusion in atomic detail. Biophys J 92: 4254-4261.
55. Katsov K, Müller M, Schick M, (2006) Field theoretic study of bilayer membrane fusion: II. Mechanism of a stalk-hole complex. Biophys J 90: 915-926.
56. Fuhrmans M, Knecht V, Marrink SJ, (2009) A single bicontinuous cubic phase induced by fusion peptides. J Am Chem Soc 131: 9166-9167.
57. Fuhrmans M, Marrink SJ, (2012) Molecular view of the role of fusion peptides in promoting positive membrane curvature. J Am Chem Soc 134: 1543-1552.
58. Haney EF, Nathoo S, Vogel HJ, Prenner EJ, (2010) Induction of non-lamellar lipid phases by antimicrobial peptides: a potential link to mode of action. Chem Phys Lipids 163: 82-93.
59. Schmidt NW, Mishra A, Lai GH, Davis M, Sanders LK, et al. (2011) Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization. J Am Chem Soc 133: 6720-6727.
60. Risselada HJ, Marelli M, Fuhrmans M, Smirnova YG, Grubmüller H, et al. (2012) Line-tension controlled mechanism for influenza fusion. PLoS ONE 7: e38302.