Thermodynamics of Micelle Formation and Membrane Fusion Modulate Antimicrobial Lipopeptide Activity

Biophysical Journal

Volumn 109, Issue 4, 2015, Pages 750-759

  Lin, Dejun ^a   Grossfield, Alan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOGLYCEROL; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLETHANOLAMINE; ANTIINFECTIVE AGENT; LIPID BILAYER; LIPOPEPTIDE; MICELLE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL;

CHEMICAL PHENOMENA; CHEMISTRY; KINETICS; LIPID BILAYER; MEMBRANE FUSION; MICELLE; MOLECULAR DYNAMICS; THERMODYNAMICS;

ANTI-INFECTIVE AGENTS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; LIPID BILAYERS; LIPOPEPTIDES; MEMBRANE FUSION; MICELLES; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; THERMODYNAMICS;

EID: 84941035386     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.07.011     Document Type: Article

References (56)

1. A.R. Koczulla, and R. Bals Antimicrobial peptides: current status and therapeutic potential Drugs 63 2003 389 406
2. H. Jenssen, P. Hamill, and R.E.W. Hancock Peptide antimicrobial agents Clin. Microbiol. Rev. 19 2006 491 511
3. L.J.V. Piddock Multidrug-resistance efflux pumps - not just for resistance Nat. Rev. Microbiol. 4 2006 629 636
4. O. Lomovskaya, and H.I. Zgurskaya W.J. Watkins Waltzing transporters and 'the dance macabre' between humans and bacteria Nat. Rev. Drug Discov. 6 2007 56 65
5. R.E.W. Hancock, and H.-G. Sahl Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 24 2006 1551 1557
6. S.K. Straus, and R.E.W. Hancock Mode of action of the new antibiotic for Gram-positive pathogens daptomycin: comparison with cationic antimicrobial peptides and lipopeptides Biochim. Biophys. Acta 1758 2006 1215 1223
7. Z. Oren, and J.C. Lerman 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 1999 501 513
8. D. Raimondo, and G. Andreotti A. Scaloni A folding-dependent mechanism of antimicrobial peptide resistance to degradation unveiled by solution structure of distinctin Proc. Natl. Acad. Sci. USA 102 2005 6309 6314
9. J. Strahilevitz, and A. Mor Y. Shai Spectrum of antimicrobial activity and assembly of dermaseptin-b and its precursor form in phospholipid membranes Biochemistry 33 1994 10951 10960
10. J.K. Ghosh, and D. Shaool A. Mor Selective cytotoxicity of dermaseptin S3 toward intraerythrocytic Plasmodium falciparum and the underlying molecular basis J. Biol. Chem. 272 1997 31609 31616
11. Z. Oren, and Y. Shai Cyclization of a cytolytic amphipathic α-helical peptide and its diastereomer: effect on structure, interaction with model membranes, and biological function Biochemistry 39 2000 6103 6114
12. R. Feder, A. Dagan, and A. Mor Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerization on selective cytotoxicity J. Biol. Chem. 275 2000 4230 4238
13. I. Kustanovich, and D.E. Shalev A. Mor Structural requirements for potent versus selective cytotoxicity for antimicrobial dermaseptin S4 derivatives J. Biol. Chem. 277 2002 16941 16951
14. N. Sal-Man, Z. Oren, and Y. Shai Preassembly of membrane-active peptides is an important factor in their selectivity toward target cells Biochemistry 41 2002 11921 11930
15. C.D. Fjell, and J.A. Hiss G. Schneider Designing antimicrobial peptides: form follows function Nat. Rev. Drug Discov. 11 2012 37 51
16. C. Neale, and J.C.Y. Hsu R. Pomès Indolicidin binding induces thinning of a lipid bilayer Biophys. J. 106 2014 L29 L31
17. T.D. Romo, and A. Grossfield Unknown unknowns: the challenge of systematic and statistical error in molecular dynamics simulations Biophys. J. 106 2014 1553 1554
18. D. Avrahami, and Y. Shai Bestowing antifungal and antibacterial activities by lipophilic acid conjugation to D,L-amino acid-containing antimicrobial peptides: a plausible mode of action Biochemistry 42 2003 14946 14956
19. D. Avrahami, and Y. Shai A new group of antifungal and antibacterial lipopeptides derived from non-membrane active peptides conjugated to palmitic acid J. Biol. Chem. 279 2004 12277 12285
20. A. Makovitzki, D. Avrahami, and Y. Shai Ultrashort antibacterial and antifungal lipopeptides Proc. Natl. Acad. Sci. USA 103 2006 15997 16002
21. A. Vallon-Eberhard, and A. Makovitzki Y. Shai Efficient clearance of Aspergillus fumigatus in murine lungs by an ultrashort antimicrobial lipopeptide, palmitoyl-lys-ala-D-Ala-lys Antimicrob. Agents Chemother. 52 2008 3118 3126
22. N. Papo, and Z. Oren Y. Shai The consequence of sequence alteration of an amphipathic α-helical antimicrobial peptide and its diastereomers J. Biol. Chem. 277 2002 33913 33921
23. A. Makovitzki, J. Baram, and Y. Shai Antimicrobial lipopolypeptides composed of palmitoyl di- and tricationic peptides: in vitro and in vivo activities, self-assembly to nanostructures, and a plausible mode of action Biochemistry 47 2008 10630 10636
24. J.N. Horn, T.D. Romo, and A. Grossfield Simulating the mechanism of antimicrobial lipopeptides with all-atom molecular dynamics Biochemistry 52 2013 5604 5610
25. J.N. Horn, and J.D. Sengillo A. Grossfield Characterization of a potent antimicrobial lipopeptide via coarse-grained molecular dynamics Biochim. Biophys. Acta 1818 2012 212 218
26. D. Lin, and A. Grossfield Thermodynamics of antimicrobial lipopeptide binding to membranes: origins of affinity and selectivity Biophys. J. 107 2014 1862 1872
27. A.J. Rzepiela, and D. Sengupta S.J. Marrink Membrane poration by antimicrobial peptides combining atomistic and coarse-grained descriptions Faraday Discuss. 144 2010 431 481
28. M. Louhivuori, and H.J. Risselada S.J. Marrink Release of content through mechano-sensitive gates in pressurized liposomes Proc. Natl. Acad. Sci. USA 107 2010 19856 19860
29. S.J. Marrink, A.H. de Vries, and A.E. Mark Coarse grained model for semiquantitative lipid simulations J. Phys. Chem. B 108 2004 750 760
30. S.J. Marrink, and H.J. Risselada A.H. de Vries The MARTINI force field: coarse grained model for biomolecular simulations J. Phys. Chem. B 111 2007 7812 7824
31. H.J. Risselada, and S.J. Marrink The molecular face of lipid rafts in model membranes Proc. Natl. Acad. Sci. USA 105 2008 17367 17372
32. G. Singh, and D.P. Tieleman Using the Wimley-White hydrophobicity scale as a direct quantitative test of force fields: the MARTINI coarse-grained model J. Chem. Theory Comput. 7 2011 2316 2324
33. L. Monticelli, D.P. Tieleman, and P.F.J. Fuchs Interpretation of 2H-NMR experiments on the orientation of the transmembrane helix WALP23 by computer simulations Biophys. J. 99 2010 1455 1464
34. N. Castillo, and L. Monticelli D.P. Tieleman Free energy of WALP23 dimer association in DMPC, DPPC, and DOPC bilayers Chem. Phys. Lipids 169 2013 95 105
35. P.M. Kasson, and N.W. Kelley V.S. Pande Ensemble molecular dynamics yields submillisecond kinetics and intermediates of membrane fusion Proc. Natl. Acad. Sci. USA 103 2006 11916 11921
36. S.O. Yesylevskyy, and L.V. Schäfer S.J. Marrink Polarizable water model for the coarse-grained MARTINI force field PLOS Comput. Biol. 6 2010 e1000810
37. D.H. de Jong, and G. Singh S.J. Marrink Improved parameters for the MARTINI coarse-grained protein force field J. Chem. Theory Comput. 9 2013 687 697
38. G.N. Serrano, G.G. Zhanel, and F. Schweizer Antibacterial activity of ultrashort cationic lipo-β-peptides Antimicrob. Agents Chemother. 53 2009 2215 2217
39. S. Kumar, and J.M. Rosenberg P.A. Kollman The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13 1992 1011 1021
40. J.D. Chodera, and M.R. Shirts Replica exchange and expanded ensemble simulations as Gibbs sampling: simple improvements for enhanced mixing J. Chem. Phys. 135 2011 194110
41. Grossfield, A. WHAM: an implementation of the weighted histogram analysis method. Ver. 2.0.5. http://membrane.urmc.rochester.edu/content/wham/.
42. F. Zhu, and G. Hummer Convergence and error estimation in free energy calculations using the weighted histogram analysis method J. Comput. Chem. 33 2012 453 465
43. W.H. Press, and S.A. Teukolsky B.P. Flannery Numerical Recipes: The Art of Scientific Computing 3rd Ed 2007 Cambridge University Press New York
44. Holoborodko, P. 2008-2014. MPFR C++. http://www.holoborodko.com/pavel/mpfr/.
45. Lin, D. GWHAM: a C++ implementation of generalized weighted histogram analysis method. https://github.com/dejunlin/gwham.
46. W. E, W. Ren, and E. Vanden-Eijnden Simplified and improved string method for computing the minimum energy paths in barrier-crossing events J. Chem. Phys. 126 2007 164103
47. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
48. D. van der Spoel, and E. Lindahl H.J.C. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
49. S. Pronk, and S. Páll E. Lindahl GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 29 2013 845 854
50. S. Nose, and M.L. Klein Constant pressure molecular dynamics for molecular systems Mol. Phys. 50 1983 1055 1076
51. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
52. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190
53. M.N. Melo, R. Ferre, and M.A.R.B. Castanho Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations Nat. Rev. Microbiol. 7 2009 245 250
54. R.M. Epand, and R.F. Epand Lipid domains in bacterial membranes and the action of antimicrobial agents Biochim. Biophys. Acta 1788 2009 289 294
55. R.F. Epand, and L. Maloy R.M. Epand Amphipathic helical cationic antimicrobial peptides promote rapid formation of crystalline states in the presence of phosphatidylglycerol: lipid clustering in anionic membranes Biophys. J. 98 2010 2564 2573
56. R.M. Epand, and R.F. Epand Bacterial membrane lipids in the action of antimicrobial agents J. Pept. Sci. 17 2011 298 305