How reliable are molecular dynamics simulations of membrane active antimicrobial peptides?

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 9, 2014, Pages 2280-2288

  Wang, Yukun ^a,b   Zhao, Tangzheng ^a,b   Wei, Dongqing ^a,b   Strandberg, Erik ^c   Ulrich, Anne S ^c   Ulmschneider, Jakob P ^b  

^a Shanghai Jiao Tong University   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Antimicrobial peptide PGLa; BP100; Lipid bilayer membrane; Maculatin; MD force field; Melittin

Indexed keywords

BP100; MACULATIN; MELITTIN; PEPTIDE; PGLA PEPTIDE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPUTER SIMULATION; CONTROLLED STUDY; FORCE FIELD PARAMETERS; MOLECULAR DYNAMICS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING;

ANTIMICROBIAL PEPTIDE PGLA; BP100; LIPID BILAYER MEMBRANE; MACULATIN; MD FORCE FIELD; MELITTIN;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; COMPUTER SIMULATION; HUMANS; LIPID BILAYERS; MELITTEN; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; OLIGOPEPTIDES; PROTEIN PRECURSORS;

EID: 84903753931     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.04.009     Document Type: Article

References (46)

1. R.M. Epand, and H.J. Vogel Diversity of antimicrobial peptides and their mechanisms of action Biochim. Biophys. Acta (BBA) 1462 1999 11 28
2. W. van 't Hof, E.C. Veerman, E.J. Helmerhorst, and A.V. Amerongen Antimicrobial peptides: properties and applicability Biol. Chem. 382 2001 597 619 (Pubitemid 32472171)
3. L.T. Nguyen, E.F. Haney, and H.J. Vogel The expanding scope of antimicrobial peptide structures and their modes of action Trends Biotechnol. 29 2011 464 472
4. A.A. Gurtovenko, J. Anwar, and I. Vattulainen Defect-mediated trafficking across cell membranes: insights from in silico modeling Chem. Rev. 110 2010 6077 6103
5. G. Bocchinfuso, S. Bobone, C. Mazzuca, A. Palleschi, and L. Stella Fluorescence spectroscopy and molecular dynamics simulations in studies on the mechanism of membrane destabilization by antimicrobial peptides Cell. Mol. Life Sci. 68 2011 2281 2301
6. J. Bürck, S. Roth, P. Wadhwani, S. Afonin, N. Kanithasen, E. Strandberg, and A.S. Ulrich Conformation and membrane orientation of amphiphilic helical peptides by oriented circular dichroism Biophys. J. 95 2008 3872 3881
7. E. Strandberg, and A.S. Ulrich NMR methods for studying membrane-active antimicrobial peptides Concepts Magn. Reson. Part A 23A 2004 89 120 (Pubitemid 40646213)
8. 19F NMR methods for studying biomembranes Prog. Nucl. Magn. Reson. Spectrosc. 46 2005 1 21 (Pubitemid 40357060)
9. H.J.C. Berendsen, D. van der Spoel, and R. van Drunen GROMACS: a message-passing parallel molecular dynamics implementation Comp. Phys. Comm. 95 1995 43 56
10. A.D. MacKerell, D. Bashford, R.L. Dunbrack Bellott, J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Kuczera, F.T.K. Lau, C. Mattos, S. Michnick, T. Ngo, D.T. Nguyen, B. Prodhom, W.E. Reiher, B. Roux, M. Schlenkrich, J.C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiórkiewicz-Kuczera, D. Yin, and M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins † J. Phys. Chem. B 102 1998 3586 3616 (Pubitemid 128576688)
11. W.L. Jorgensen, D.S. Maxwell, and J. Tirado-Rives Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids J. Am. Chem. Soc. 118 1996 11225 11236 (Pubitemid 26399746)
12. C. Oostenbrink, A. Villa, A.E. Mark, and W.F. Van Gunsteren A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 25 2004 1656 1676
13. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
14. J.B. Klauda, R.M. Venable, J.A. Freites, J.W. O'Connor, D.J. Tobias, C. Mondragon-Ramirez, I. Vorobyov, A.D. MacKerell, and R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipids types J. Phys. Chem. B 114 2010 7830 7843
15. J.P. Ulmschneider, and M.B. Ulmschneider United atom lipids parameters for combination with the optimized potentials for liquid simulations all-atom force field J. Chem. Theory Comput. 5 2009 1803 1813
16. O. Berger, O. Edholm, and F. Jahnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidycholine at full hydration, constant pressure and constant temperature Biophys. J. 72 1997 2002 2013 (Pubitemid 27184429)
17. B. Hess, H. Bekker, H.J.C. Berendsen, and J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comp. Chem. 18 1997 1463 1472 (Pubitemid 127637344)
18. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101
19. H.J.C. Berendsen, J.P.M. Postma, W.F. Vangunsteren, A. Dinola, and J.R. Haak Molecular-dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
20. J.P. Ulmschneider, J.C. Smith, M.B. Ulmschneider, A.S. Ulrich, and E. Strandberg Reorientation and dimerization of the membrane-bound antimicrobial peptide PGLa from microsecond all-atom MD simulations Biophys. J. 103 2012 472 482
21. J.H. Davis The description of membrane lipids conformation, order and dynamics by 2H-NMR Biochim. Biophys. Acta (BBA) 737 1983 117 171 (Pubitemid 13129060)
22. 19F-NMR structure analysis of membrane-bound peptides J. Pept. Sci. 13 2007 614 623 (Pubitemid 47490326)
23. 19F NMR parameters of fluorine-labeled amino acids. Part I: aromatic substituents J. Magn. Res. 191 2008 7 15
24. S.L. Grage, U.H.N. Dürr, S. Afonin, P.K. Mikhailiuk, I.V. Komarov, and A.S. Ulrich Solid state 19F NMR parameters of fluorine-labeled amino acids. Part II: aliphatic substituents J. Magn. Res. 191 2008 16 23
25. 19F-NMR Biophys. J. 90 2006 1676 1686
26. W. Hoffmann, K. Richter, and G. Kreil A novel peptide designated PYLa and its precursor as predicted from cloned mRNA of Xenopus laevis skin EMBO J. 2 1983 711 714
27. K. Richter, H. Aschauer, and G. Kreil Biosynthesis of peptides in the skin of Xenopus laevis: isolation of novel peptides predicted from the sequence of cloned cDNAs Peptides 6 Suppl. 3 1985 17 21 (Pubitemid 16104135)
28. D. Andreu, H. Aschauer, G. Kreil, and R.B. Merrifield Solid-phase synthesis of PYLa and isolation of its natural counterpart, PGLa [PYLa-(4-24)] from skin secretion of Xenopus laevis Eur. J. Biochem. 149 1985 531 535
29. M. Andersson, Jakob P. Ulmschneider, Martin B. Ulmschneider, and Stephen H. White Conformational states of melittin at a bilayer interface Biophys. J. 104 2013 L12 L14
30. A.S. Ladokhin, and S.H. White Folding of amphipathic alpha-helices on membranes: energetics of helix formation by melittin J. Mol. Biol. 285 1999 1363 1369 (Pubitemid 29060439)
31. C.E. Dempsey, and G.S. Butler Helical structure and orientation of melittin in dispersed phospholipids membranes from amide exchange analysis in situ Biochemistry 31 1992 11973 11977 (Pubitemid 23011338)
32. H. Vogel, and F. Jähnig The structure of melittin in membranes Biophys. J. 50 1986 573 582
33. P.F. Almeida, and A. Pokorny Mechanisms of antimicrobial, cytolytic, and cell-penetrating peptides: from kinetics to thermodynamics Biochemistry 48 2009 8083 8093
34. A. Ladokhin, M. Fernández-Vidal, and S. White CD spectroscopy of peptides and proteins bound to large unilamellar vesicles J. Membr. Biol. 236 2010 247 253
35. E. Strandberg, P. Tremouilhac, P. Wadhwani, and A.S. Ulrich Synergistic transmembrane insertion of the heterodimeric PGLa/magainin 2 complex studied by solid-state NMR Biochim. Biophys. Acta (BBA) 1788 2009 1667 1679
36. T. Rozek, R.J. Waugh, S.T. Steinborner, J.H. Bowie, M.J. Tyler, and J.C. Wallace The maculatin peptides from the skin glands of the tree frog Litoria genimaculata: a comparison of the structures and antibacterial activities of maculatin 1.1 and caerin 1.1 J. Pept. Sci. 4 1998 111 115 (Pubitemid 128543157)
37. E. Badosa, R. Ferre, M. Planas, L. Feliu, E. Besalú, J. Cabrefiga, E. Bardají, and E. Montesinos A library of linear undecapeptides with bactericidal activity against phytopathogenic bacteria Peptides 28 2007 2276 2285 (Pubitemid 350116307)
38. K. Eggenberger, C. Mink, P. Wadhwani, A.S. Ulrich, and P. Nick Using the peptide BP100 as a cell-penetrating tool for the chemical engineering of actin filaments within living plant cells Chembiochem 12 2011 132 137
39. P. Wadhwani, E. Strandberg, J. van den Berg, C. Mink, J. Bürck, R. Ciriello, and A.S. Ulrich Dynamical structure of the short multifunctional peptide BP100 in membranes Biochim. Biophys. Acta (BBA) 1838 2014 940 949
40. E. Strandberg, S. Esteban-Martín, J. Salgado, and A.S. Ulrich Orientation and dynamics of peptides in membranes calculated from 2H-NMR data Biophys. J. 96 2009 3223 3232
41. 19F-NMR Biophys. J. 88 2005 3392 3397 (Pubitemid 40586589)
42. 2H-NMR Biochim. Biophys. Acta (BBA) 1758 2006 1330 1342 (Pubitemid 44436073)
43. 19F NMR spectroscopy J. Am. Chem. Soc. 130 2008 16512 16514
44. M.B. Ulmschneider, and J.P. Ulmschneider Folding peptides into lipids bilayer membranes J. Chem. Theory Comput. 4 2008 1807 1809
45. J.P. Ulmschneider, J.P.F. Doux, J.A. Killian, J.C. Smith, and M.B. Ulmschneider Peptide partitioning and folding into lipids bilayers J. Chem. Theory Comput. 5 2009 2202 2205
46. M.B. Ulmschneider, J.P.F. Doux, J.A. Killian, J. Smith, and J.P. Ulmschneider Mechanism and kinetics of peptide partitioning into membranes J. Am. Chem. Soc. 132 2010 3452 3460