Thermodynamics of antimicrobial lipopeptide binding to membranes: Origins of affinity and selectivity

Biophysical Journal

Volumn 107, Issue 8, 2014, Pages 1862-1872

  Lin, Dejun ^a   Grossfield, Alan ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; LIPID BILAYER; LIPOPEPTIDE; PROTEIN BINDING;

ANIMAL; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; LIPID BILAYER; METABOLISM; STATIC ELECTRICITY; THERMODYNAMICS;

ANIMALS; ANTI-INFECTIVE AGENTS; CELL MEMBRANE; LIPID BILAYERS; LIPOPEPTIDES; PROTEIN BINDING; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84908267646     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.08.026     Document Type: Article

References (57)

1. H.G. Boman Peptide antibiotics and their role in innate immunity Annu. Rev. Immunol. 13 1995 61 92
2. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395
3. A.R. Koczulla, and R. Bals Antimicrobial peptides: current status and therapeutic potential Drugs 63 2003 389 406
4. H. Jenssen, P. Hamill, and R.E.W. Hancock Peptide antimicrobial agents Clin. Microbiol. Rev. 19 2006 491 511
5. R.M. Epand, and H.J. Vogel Diversity of antimicrobial peptides and their mechanisms of action Biochim. Biophys. Acta 1462 1999 11 28
6. G. Ehrenstein, and H. Lecar Electrically gated ionic channels in lipid bilayers Q. Rev. Biophys. 10 1977 1 34
7. Y. Shai, and Z. Oren From "carpet" mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides Peptides 22 2001 1629 1641
8. 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
9. 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
10. 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
11. 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
12. A. Makovitzki, D. Avrahami, and Y. Shai Ultrashort antibacterial and antifungal lipopeptides Proc. Natl. Acad. Sci. USA 103 2006 15997 16002
13. A. Vallon-Eberhard, and A. Makovitzki Y. Shai Efficient clearance of Aspergillus fumigatus in murine lungs by an ultrashort antimicrobial lipopeptide, palmitoyl-lys-ala-DAla-lys Antimicrob. Agents Chemother. 52 2008 3118 3126
14. C. Anzo, and A.H. de Vries S.-J. Marrink Methodological issues in lipid bilayer simulations J. Phys. Chem. B 107 2003 9424 9433
15. R.W. Pastor, and S.E. Feller Time scales of lipid dynamics and molecular dynamics Biological Membranes: A Molecular Perspective from Computation and Experiment 1996 Birkhauser Basel, Switzerland
16. H. Heller, M. Schaefer, and K. Schulten Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid crystal phase J. Phys. Chem. 97 1993 8343 8360
17. E. Mátyus, C. Kandt, and D.P. Tieleman Computer simulation of antimicrobial peptides Curr. Med. Chem. 14 2007 2789 2798
18. 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
19. A.J. Rzepiela, and D. Sengupta S.J. Marrink Membrane poration by antimicrobial peptides combining atomistic and coarse-grained descriptions Faraday Discuss. 144 2010 431 443
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. 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
28. L. Monticelli, and S.K. Kandasamy S.-J. Marrink The MARTINI coarse-grained force field: extension to proteins J. Chem. Theory Comput. 4 2008 819 834
29. G.N. Serrano, G.G. Zhanel, and F. Schweizer Antibacterial activity of ultrashort cationic lipo-β-peptides Antimicrob. Agents Chemother. 53 2009 2215 2217
30. 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
31. Grossfield, A. 2011. WHAM, Ver. 2.05: an implementation of the weighted histogram analysis method. http://membrane.urmc.rochester.edu/content/wham.
32. 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
33. D. van Der Spoel, and E. Lindahl H.J.C. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
34. S. Nose, and M.L. Klein Constant pressure molecular dynamics for molecular systems Mol. Phys. 50 1983 1055 1076
35. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
36. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190
37. W.D. Bennett, and D.P. Tieleman Water defect and pore formation in atomistic and coarse-grained lipid membranes: pushing the limits of coarse graining J. Chem. Theory Comput. 7 2011 2981 2988
38. J.A. Nelder, and R. Mead A simplex method for function minimization Comput. J. 7 1965 308 313
39. P.V. Khadikar, and D. Mandloi S. Joshi QSAR study on solubility of alkanes in water and their partition coefficients in different solvent systems using PI index Bioorg. Med. Chem. Lett. 13 2003 419 422
40. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 3 1996 842 848
41. C. Neale, and J.C.Y. Hsu R. Pomès Indolicidin binding induces thinning of a lipid bilayer Biophys. J. 106 2014 L29 L31
42. 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
43. E. Sikorska, and M. Dawgul W. Kamysz Self-assembly and interactions of short antimicrobial cationic lipopeptides with membrane lipids: ITC, FTIR and molecular dynamics studies Biochim. Biophys. Acta 1838 2014 2625 2634
44. A. Radzicka, and R. Wolfenden Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution Biochemistry 27 1988 1664 1670
45. R. Wolfenden Experimental measures of amino acid hydrophobicity and the topology of transmembrane and globular proteins J. Gen. Physiol. 129 2007 357 362
46. J.L. MacCallum, W.F.D. Bennett, and D.P. Tieleman Partitioning of amino acid side chains into lipid bilayers: results from computer simulations and comparison to experiment J. Gen. Physiol. 129 2007 371 377
47. J.L. MacCallum, W.F.D. Bennett, and D.P. Tieleman Distribution of amino acids in a lipid bilayer from computer simulations Biophys. J. 94 2008 3393 3404
48. C.P. Moon, and K.G. Fleming Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers Proc. Natl. Acad. Sci. USA 108 2011 10174 10177
49. T. Hessa, and H. Kim G. von Heijne Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433 2005 377 381
50. T. Hessa, and N.M. Meindl-Beinker G. von Heijne Molecular code for transmembrane-helix recognition by the Sec61 translocon Nature 450 2007 1026 1030
51. J.L. MacCallum, W.F. Bennett, and D.P. Tieleman Transfer of arginine into lipid bilayers is nonadditive Biophys. J. 101 2011 110 117
52. E.E. Lattman, and G.D. Rose Protein folding - what's the question? Proc. Natl. Acad. Sci. USA 90 1993 439 441
53. T.D. Romo, and L.A. Bradney A. Grossfield Membrane binding of an acyl-lactoferricin B antimicrobial peptide from solid-state NMR experiments and molecular dynamics simulations Biochim. Biophys. Acta 1808 2011 2019 2030
54. I. Vorobyov, L. Li, and T.W. Allen Assessing atomistic and coarse-grained force fields for protein-lipid interactions: the formidable challenge of an ionizable side chain in a membrane J. Phys. Chem. B 112 2008 9588 9602
55. Z. Wu, Q. Cui, and A. Yethiraj A new coarse-grained force field for membrane-peptide simulations J. Chem. Theory Comput. 7 2011 3793 3802
56. 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
57. 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