Mechanism of structural transformations induced by antimicrobial peptides in lipid membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 2, 2012, Pages 194-204

  Lam, Kin Lok H ^a,b   Wang, Hao ^a   Siaw, Ting Ann ^a,b   Chapman, Matthew R ^a,b   Waring, Alan J ^c,d   Kindt, James T ^a   Lee, Ka Yee C ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c HARBOR UCLA MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atomic force microscopy; Membrane disruption mechanism; Molecular dynamics; Phospholipid; Pore formation; Protegrin 1

Indexed keywords

DIMYRISTOYLPHOSPHATIDYLCHOLINE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEGRIN 1; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BILAYER MEMBRANE; BIOTRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROPHOBICITY; IONIC STRENGTH; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIMULATION; TEMPERATURE;

ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; MEMBRANE LIPIDS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PROTEIN STRUCTURE, SECONDARY;

EID: 84855453413     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.11.002     Document Type: Article

References (75)

1. L.V. Chernomordik, and M.M. Kozlov The protein coat in membrane fusion: lessons from fission Traffic 3 2002 256 267 (Pubitemid 34303258)
2. S.L. Schmid Clathrin-coated vesicle formation and protein sorting: an integrated process Annu. Rev. Biochem. 66 1997 511 548 (Pubitemid 27274666)
3. M.M. Kozlov Dynamin: possible mechanism of "pinchase" action Biophys. J. 77 1999 604 616 (Pubitemid 29305256)
4. S.L. Schmid, M.A. McNiven, and P.D. Camilli Dynamin and its partners: a progress report Curr. Opin. Cell Biol. 10 1998 504 512 (Pubitemid 28391120)
5. M.M. Kozlov Fission of biological membranes: interplay between dynamin and lipids Traffic 2 2001 51
6. U. Seifert Configurations of fluid membranes and vesicles Adv. Phys. 46 1997 13 137 (Pubitemid 127535649)
7. N. Sciaky, J. Presley, C. Smith, K.J.M. Zaal, N. Cole, J.E. Moreira, M. Terasaki, E. Siggia, and J. Lippincott-Schwartz Golgi tubule traffic and the effects of Brefeldin A visualized in living cells J. Cell Biol. 139 1997 1137 1155 (Pubitemid 27523203)
8. J.A. Killian, I. Salemink, M.R.R. de Planque, G. Lindblom, R.E. Koeppe, and D.V. Greathouse Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane alpha-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans Biochemistry 35 1996 1037 1045 (Pubitemid 26034591)
9. II transition Biophys. J. 76 1999 751 767 (Pubitemid 29264557)
10. B. Christensen, J. Fink, R.B. Merrifield, and D. Mauzerall Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes Proc. Natl. Acad. Sci. 85 1988 5072 5076
11. K. He, S.J. Ludtke, D.L. Worcester, and H.W. Huang Neutron scattering in the plane of membranes: structure of alamethicin pores Biophys. J. 70 1996 2659 2666 (Pubitemid 26000964)
12. P. Juvvadi, S. Vunnam, and R.B. Merrifield Merrifield, synthetic melittin, its enantio, retro, and retroenantio isomers, and selected chimeric analogs: their antibacterial, hemolytic, and lipid bilayer action J. Am. Chem. Soc. 118 1996 8989 8997 (Pubitemid 26342532)
13. S.J. Ludtke, K. He, W.T. Heller, T.A. Harroun, L. Yang, and H.W. Huang Membrane pores induced by magainin Biochemistry 35 1996 13723 13728 (Pubitemid 26363914)
14. K. Matsuzaki, M. Harada, T. Handa, S. Funakoshi, N. Fujii, H. Yajima, and K. Miyajima Magainin 1-induced leakage of entrapped calcein out of negatively-charged lipid vesicles Biochim. Biophys. Acta (BBA) - Biomembr. 981 1989 130 134 (Pubitemid 19127778)
15. K. Matsuzaki, O. Murase, N. Fujii, and K. Miyajima An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation Biochemistry 35 1996 11361 11368 (Pubitemid 26299310)
16. 2-terminal alpha-helical domain 1-18 of dermaseptin is responsible for antimicrobial activity J. Biol. Chem. 269 1994 1934 1939
17. K.L.H. Lam, Y. Ishitsuka, Y. Cheng, K. Chien, A.J. Waring, R.I. Lehrer, and K.Y.C. Lee Mechanism of supported membrane disruption by antimicrobial peptide protegrin-1 J. Phys. Chem. B 110 2006 21282 21286 (Pubitemid 44797403)
18. Y.A. Domanov, and P.K.J. Kinnunen Antimicrobial peptides temporins B and L induce formation of tubular lipid protrusions from supported phospholipid bilayers Biophys. J. 91 2006 4427 4439 (Pubitemid 44904229)
19. D. Gidalevitz, Y. Ishitsuka, A.S. Muresan, O. Konovalov, A.J. Waring, R.I. Lehrer, and K.Y.C. Lee Interaction of antimicrobial peptide protegrin with biomembranes Proc. Natl. Acad. Sci. 100 2003 6302 6307 (Pubitemid 36666576)
20. M. Meincken, D.L. Holroyd, and M. Rautenbach Atomic force microscopy study of the effect of antimicrobial peptides on the cell envelope of Escherichia coli Antimicrob. Agents Chemother. 49 2005 4085 4092 (Pubitemid 41400950)
21. M.P. Nieh, V.A. Raghunathan, C.J. Glinka, T.A. Harroun, G. Pabst, and J. Katsaras Magnetically alignable phase of phospholipid "bicelle" mixtures is a chiral nematic made up of wormlike micelles Langmuir 20 2004 7893 7897
22. Y. Jiang, and J.T. Kindt Simulations of edge behavior in a mixed-lipid bilayer: fluctuation analysis J. Chem. Phys. 126 2007 045105
23. T.A. Harroun, M. Koslowsky, M.P. Nieh, C.F. deLannoy, V.A. Raghunathan, and J. Katsaras Comprehensive examination of mesophases formed by DMPC and DHPC mixtures Langmuir 21 2005 5356 5361 (Pubitemid 40850619)
24. D.S. Bolintineanu, Y.N. Kaznessis, Computational studies of protegrin antimicrobial peptides: A review, Peptides, 32 188-201.
25. H. Khandelia, A.A. Langham, and Y.N. Kaznessis Driving engineering of novel antimicrobial peptides from simulations of peptide-micelle interactions Biochim. Biophys. Acta-Biomembr. 1758 2006 1224 1234 (Pubitemid 44436078)
26. A.A. Langham, H. Khandelia, and Y.N. Kaznessis Simulations of protegrin-1 in sodium dodecylsulfate and dodecylphosphocholine micelles Biophys. J. 88 2005 210a-210a
27. A.A. Langham, H. Khandelia, and Y.N. Kaznessis How can a beta-sheet peptide be both a potent antimicrobial and harmfully toxic? Molecular dynamics simulations of protegrin-1 in micelles Biopolymers 84 2006 219 231
28. A.A. Langham, H. Khandelia, B. Schuster, A.J. Waring, R.I. Lehrer, and Y.N. Kaznessis Correlation between simulated physicochemical properties and hemolycity of protegrin-like antimicrobial peptides: predicting experimental toxicity Peptides 29 2008 1085 1093
29. H. Jang, B. Ma, T.B. Woolf, and R. Nussinov Interaction of protegrin-1 with lipid bilayers: membrane thinning effect Biophys. J. 91 2006 2848 2859 (Pubitemid 44526475)
30. D.S. Bolintineanu, A.A. Langham, H.T. Davis, and Y.N. Kaznessis Molecular dynamics simulations of three protegrin-type antimicrobial peptides: interplay between charges at the termini, β-sheet structure and amphiphilic interactions Mol. Simul. 33 2007 809 819 (Pubitemid 47347013)
31. S.K. Kandasamy, and R.G. Larson Binding modes of protegrin-1, a beta-strand antimicrobial peptide, in lipid bilayers Mol. Simul. 33 2007 799 807 (Pubitemid 47347012)
32. H. Rui, W. Im, Protegrin-1 orientation and physicochemical properties in membrane bilayers studied by potential of mean force calculations, J. Comput. Chem., 31 2859-2867.
33. R. Mani, J.J. Buffy, A.J. Waring, R.I. Lehrer, and M. Hong Solid-state NMR investigation of the selective disruption of lipid membranes by protegrin-1 Biochemistry 43 2004 13839 13848 (Pubitemid 39431067)
34. A.A. Langham, A.S. Ahmad, and Y.N. Kaznessis On the nature of antimicrobial activity: a model for protegrin-1 pores J. Am. Chem. Soc. 130 2008 4338 4346 (Pubitemid 351466429)
35. M. Tang, A.J. Waring, and M. Hong Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR J. Am. Chem. Soc. 129 2007 11438 11446 (Pubitemid 47555563)
36. H. Jang, B. Ma, R. Lal, and R. Nussinov Models of toxic β-sheet channels of protegrin-1 suggest a common subunit organization motif shared with toxic Alzheimer β-amyloid ion channels Biophys. J. 95 2008 4631 4642
37. R. Capone, M. Mustata, H. Jang, F.T. Arce, R. Nussinov, R. Lal, Antimicrobial protegrin-1 forms ion channels: Molecular dynamic simulation, atomic force microscopy, and electrical conductance studies, Biophys. J., 98 2644-2652.
38. H. Wang, J. de Joannis, Y. Jiang, J.C. Gaulding, B. Albrecht, F. Yin, K. Khanna, and J.T. Kindt Bilayer edge and curvature effects on partitioning of lipids by tail length: atomistic simulations Biophys. J. 95 2008 2647 2657
39. R.L. Fahrner, T. Dieckmann, S.S. Harwig, R.I. Lehrer, D. Eisenberg, and J. Feigon Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes Chem. Biol. 3 1996 543 550 (Pubitemid 26324167)
40. A.S. Muresan, and K.Y.C. Lee Shape evolution of lipid bilayer patches adsorbed on mica: an atomic force microscopy study J. Phys. Chem. B 105 2001 852 855
41. G. Schwarz Thermodynamics and kinetics of incorporation into a membrane Biochimie 71 1989 3 9 (Pubitemid 19065437)
42. H.J.C. Berendsen, D. van der Spoel, and R. van Drunen Gromacs - a message-passing parallel molecular-dynamics implementation Comput. Phys. Commun. 91 1995 43 56
43. E. Lindahl, B. Hess, and D. van der Spoel GROMACS 3.0: a package for molecular simulation and trajectory analysis J. Mol. Model. 7 2001 306 317 (Pubitemid 36153547)
44. D. van der Spoel, E. Lindahl, B. Hess, G. Groenhof, A.E. Mark, and H.J.C. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718 (Pubitemid 43076182)
45. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 (Pubitemid 26152973)
46. W.L. Jorgensen, and J. Tirado-Rives The OPLS potential functions for proteins - energy minimizations for crystals of cyclic-peptides and crambin J. Am. Chem. Soc. 110 1988 1657 1666
47. O. Berger, O. Edholm, and F. Jahnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013 (Pubitemid 27184429)
48. D.P. Tieleman, J.L. MacCallum, W.L. Ash, C. Kandt, Z.T. Xu, and L. Monticelli Membrane protein simulations with a united-atom lipid and all-atom protein model: lipid-protein interactions, side chain transfer free energies and model proteins J. Phys. Condens. Matter 18 2006 S1221 S1234
49. 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
50. U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
51. S. Miyamoto, and P.A. Kollman SETTLE - an analytical version of the shake and rattle algorithm for rigid water models J. Comput. Chem. 13 1992 952 962
52. B. Hess, H. Bekker, H.J.C. Berendsen, and J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472 (Pubitemid 127637344)
53. S.K. Kandasamy, and R.G. Larson Molecular dynamics simulations of model trans-membrane peptides in lipid bilayers: a systematic investigation of hydrophobic mismatch Biophys. J. 90 2006 2326 2343
54. Y. Jiang, H. Wang, and J.T. Kindt Atomistic simulations of "bicelles" Biophys. J. 98 2010 2895 2903
55. A. Saitoh, K. Takiguchi, Y. Tanaka, and H. Hotani Opening-up of liposomal membranes by alin Proc. Natl. Acad. Sci. 95 1998 1026 1031
56. P.H. Puech, N. Borghi, E. Karatekin, and F. Brochard-Wyart Line thermodynamics: adsorption at a membrane edge Phys. Rev. Lett. 90 2003 128304
57. P. Chen The line adsorption equation: the one-dimensional counterpart of the Gibbs adsorption equation Colloids Surf. A Physicochem. Eng. Asp. 161 2000 23 30
58. H. Leontiadou, A.E. Mark, and S.J. Marrink Antimicrobial peptides in action J. Am. Chem. Soc. 128 2006 12156 12161 (Pubitemid 44413847)
59. L. van Dam, G. Karlsson, and K. Edwards Direct observation and characterization of DMPC/DHPC aggregates under conditions relevant for biological solution NMR Biochim. Biophys. Acta (BBA) - Biomembr. 1664 2004 241 256 (Pubitemid 39140998)
60. K.L.H. Lam, The Mechanism of Membrane Disruption by Antimicrobal Microbial Peptide, in: Ph.D. Thesis, University of Chicago, 2009.
61. K.Y.C. Lee, A. Gopal, A. von Nahmen, J.A. Zasadzinski, J. Majewski, G.S. Smith, P.B. Howe, and K. Kjaer Influence of palmitic acid and hexadecanol on the phase transition temperature and molecular packing of dipalmitoylphosphatidyl- choline monolayers at the air-water interface J. Chem. Phys. 116 2002 774 783 (Pubitemid 34064608)
62. 2 + Biophys. J. 85 2003 2363 2373 (Pubitemid 37210786)
63. A.J. Waring, J.J. Buffy, R.I. Lehrer, and M. Hong Immobilization and aggregation of the antimicrobial peptide protegrin-1 in lipid bilayers investigated by solid-state NMR Biochemistry 42 2003 13725 13734 (Pubitemid 37444922)
64. J.J. Buffy, R. Mani, A.J. Waring, R.I. Lehrer, and M. Hong Solid-state NMR investigation of the selective disruption of lipid membranes by protegrin-1 Biochemistry 43 2004 13839 13848 (Pubitemid 39431067)
65. S. Yamaguchi, T. Hong, A. Waring, R.I. Lehrer, and M. Hong Solid-state NMR investigations of peptide-lipid interaction and orientation of a beta-sheet antimicrobial peptide, protegrin Biochemistry 41 2002 9852 9862 (Pubitemid 34839733)
66. R. Mani, S.D. Cady, M. Tang, A.J. Waring, R.I. Lehrer, and M. Hong Membrane-dependent oligomeric structure and pore formation of a beta-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR Proc. Natl. Acad. Sci. 103 2006 16242 16247 (Pubitemid 44715181)
67. 1H NMR study Biochim. Biophys. Acta (BBA) - Biomembr. 1716 2005 11 18 (Pubitemid 41379397)
68. C. Roumestand, V. Louis, A. Aumelas, G. Grassy, B. Calas, and A. Chavanieu Oligomerization of protegrin-1 in the presence of DPC micelles. A proton high-resolution NMR study FEBS Lett. 421 1998 263 267 (Pubitemid 28045767)
69. J.J. Buffy, A.J. Waring, R.I. Lehrer, and M. Hong Immobilization and aggregation of the antimicrobial peptide protegrin-1 in lipid bilayers investigated by solid-state NMR Biochemistry 42 2003 13725 13734 (Pubitemid 37444922)
70. 19F spin diffusion NMR J. Am. Chem. Soc. 127 2005 4477 4483 (Pubitemid 40463073)
71. M. Tang, A.J. Waring, and M. Hong Intermolecular packing and alignment of a β-hairpin antimicrobial peptide aggregate from 2D solid-state NMR J. Am. Chem. Soc. 127 2005 13919 13927 (Pubitemid 41437042)
72. R. Mani, M. Tang, X. Wu, J.J. Buffy, A.J. Waring, M.A. Sherman, and M. Hong Membrane-bound dimer structure of a β-hairpin antimicrobial peptide from rotational-echo double-resonance solid-state NMR Biochemistry 45 2006 8341 8349 (Pubitemid 44036540)
73. C.E. Miller, J. Majewski, E.B. Watkins, D.J. Mulder, T. Gog, and T.L. Kuhl Probing the local order of single phospholipid membranes using grazing incidence X-ray diffraction Phys. Rev. Lett. 100 2008 058103
74. G. Wu, J. Majewski, C. Ege, K. Kjaer, M.J. Weygand, and K.Y.C. Lee Interaction between lipid monolayers and poloxamer 188: an X-ray reflectivity and diffraction study Biophys. J. 89 2005 3159 3173 (Pubitemid 41636071)
75. F. Jean-François, J. Elezgaray, P. Berson, P. Vacher, and E.J. Dufourc Pore formation induced by an antimicrobial peptide: electrostatic effects Biophys. J. 95 2008 5748 5756