Coarse-grained simulation studies of peptide-induced pore formation

Biophysical Journal

Volumn 95, Issue 9, 2008, Pages 4163-4173

  Illya, Gregoria ^a,b   Deserno, Markus ^a,c  

^a MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE;

ADSORPTION; AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; HYDROPHOBICITY; LIPID BILAYER; METABOLISM; MOLECULAR GENETICS; POROSITY; PROTEIN BINDING; THERMODYNAMICS;

ADSORPTION; AMINO ACID SEQUENCE; CELL MEMBRANE; HYDROPHOBICITY; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; POROSITY; PROTEIN BINDING; THERMODYNAMICS;

EID: 58149144259     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.131300     Document Type: Article

References (54)

1. Zasloff, M. 1987. Magainins, a class of antimicrobial peptides from Xenopus skin - isolation, characterization of two active forms, and partial Cdna sequence of a precursor. Proc. Natl. Acad. Sci. USA. 84:5449-5453.
2. Gesell, J., M. Zasloff, and S. Opella. 1997. Two-dimensional H-1 NMR experiments show that the 23-residue magainin antibiotic peptide is an a-helix in dodecylphosphocholine micelles, sodium dodecylsulfate micelles, and trifluoroethanol/water solution. J. Biomol. NMR. 9:127-135.
3. Habermann, E. 1972. Bee wasp venoms. Science. 177:314-322.
4. Hall, J. E., I. Vodyanoy, T. M. Balasubramanian, and G. R. Marshall. 1984. Alamethicin - a rich model for channel behavior. Biophys. J. 45:233-247.
5. Huang, H. W. 2006. Molecular mechanism of antimicrobial peptides: the origin of cooperativity. Biochim. Biophys. Acta. 1758:1292-1302.
6. Matsuzaki, K., K. Sugishita, N. Ishibe, M. Ueha, S. Nakata, K. Miyajima, and R. M. Epand. 1998. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry. 37:11856-11863.
7. Pouny, Y., D. Rapaport, A. Mor, P. Nicolas, and Y. Shai. 1992. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogs with phospholipid-membranes. Biochemistry. 31:12416-12423.
8. Yang, L., T. A. Harroun, T. M. Weiss, L. Ding, and H. W. Huang. 2001. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81:1475-1485.
9. Huang, H. W. 2000. Action of antimicrobial peptides: two-state model. Biochemistry. 39:8347-8352.
10. Bechinger, B., Y. Kim, L. E. Chirlian, J. Gesell, J.-M. Neumann, M. Montal, J. Tomich, M. Zasloff, and S. J. Opella. 1991. Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy. J. Biomol. NMR. 1:167-173.
11. Wieprecht, T., O. Apostolov, M. Beyermann, and J. Seelig. 2000. Membrane binding and pore formation of the antibacterial peptide PGLA: thermodynamic and mechanistic aspects. Biochemistry. 39:442-452.
12. Zemel, A., A. Ben-Shaul, and S. May. 2004. Membrane perturbation induced by interfacially adsorbed peptides. Biophys. J. 86:3607-3619.
13. Longo, M. L., A. J. Waring, L. M. Gordon, and D. A. Hammer. 1998. Area expansion and permeation of phospholipid membrane bilayers by influenza fusion peptides and melittin. Langmuir. 14:2385-2395.
14. Zemel, A., A. Ben-Shaul, and S. May. 2005. Perturbation of a lipid membrane by amphipathic peptides and its role in pore formation. Eur. Biophys. J. 34:230-242.
15. Wu, M. H., E. Maier, R. Benz, and R. E. W. Hancock. 1999. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry. 38:7235-7242.
16. Matsuzaki, K., M. Harada, T. Handa, S. Funakoshi, N. Fujii, H. Yajima, and K. Miyajima. 1989. Magainin 1-induced leakage of entrapped calcein out of negatively-charged lipid vesicles. Biochim. Biophys. Acta. 981:130-134.
17. He, K., S. J. Ludtke, D. L. Worcester, and H. W. Huang. 1996. Neutron scattering in the plane of membranes: structure of alamethicin pores. Biophys. J. 70:2659-2666.
18. Matsuzaki, K., O. Murase, N. Fujii, and K. Miyajima. 1996. An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry. 35:11361-11368.
19. Ludtke, S. J., K. He, W. T. Heller, T. A. Harroun, L. Yang, and H. W. Huang. 1996. Membrane pores induced by magainin. Biochemistry. 35:13723-13728.
20. Leontiadou, H., A. E. Mark, and S. J. Marrink. 2006. Antimicrobial peptides in action. J. Am. Chem. Soc. 128:12156-12161.
21. Lopez, C. F., S. O. Nielsen, P. B. Moore, and M. L. Klein. 2004. Understanding nature's design for a nanosyringe. Proc. Natl. Acad. Sci. USA. 101:4431-4434.
22. Lopez, C. F., S. O. Nielsen, B. Ensing, P. B. Moore, and M. L. Klein. 2005. Structure and dynamics of model pore insertion into a membrane. Biophys. J. 88:3083-3094.
23. Lopez, C. F., S. O. Nielsen, G. Srinivas, W. F. DeGrado, and M. L. Klein. 2006. Probing membrane insertion activity of antimicrobial polymers via coarse-grain molecular dynamics. J. Chem. Theory Comput. 2:649-655.
24. Venturoli, M., B. Smit, and M. M. Sperotto. 2005. Simulation studies of protein-induced bilayer deformations, and lipid-induced protein tilting, on a mesoscopic model for lipid bilayers with embedded proteins. Biophys. J. 88:1778-1798.
25. Brannigan, G., and F. L. H. Brown. 2007. Contributions of Gaussian curvature and nonconstant lipid volume to protein deformation of lipid bilayers. Biophys. J. 92:864-876.
26. Monticelli, L., S. K. Kandasamy, X. Periole, R. G. Larson, D. P. Tieleman, and S. J. Marrink. 2008. The MARTINI coarse-grained force field: extension to proteins. J. Chem. Theory Comput. 4:819-834.
27. Müller, M., K. K., and M. Schick. 2006. Biological and synthetic membranes: what can be learned from a coarse-grained description? Phys. Rep. 434:113-176.
28. Venturoli, M., M. M. Sperotto, M. Kranenburg, and B. Smit. 2006. Mesoscopic models of biological membranes. Phys. Rep. 437:1-54.
29. Cooke, I. R., K. Kremer, and M. Deserno. 2005. Tunable generic model for fluid bilayer membranes. Part 1. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72:011506.
30. Cooke, I. R., and M. Deserno. 2005. Solvent-free model for self-assembling fluid bilayer membranes: stabilization of the fluid phase based on broad attractive tail potentials. J. Chem. Phys. 123:224710.
31. Brannigan, G., L. C. L. Lin, and F. L. H. Brown. 2006. Implicit solvent simulation models for biomembranes. Eur. Biophys. J. 35:104-124.
32. Cooke, I. R., and M. Deserno. 2006. Coupling between lipid shape and membrane curvature. Biophys. J. 91:487-495.
33. Harmandaris, V. A., and M. Deserno. 2006. A novel method for measuring the bending rigidity of model lipid membranes by simulating tethers. J. Chem. Phys. 125:204905.
34. Reynwar, B. J., G. Illya, V. A. Harmandaris, M. M. Müller, K. Kremer, and M. Deserno. 2007. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature. 447:461-464.
35. Kechuan, T., D. J. Tobias, and M. L. Klein. 1995. Constant pressure and temperature molecular dynamics simulation of a fully hydrated liquid crystal phase dipalmitoylphosphatidylcholine bilayer. Biophys. J. 69:2558-2562.
36. Hess, B., S. León, N. van der Vegt, and K. Kremer. 2007. Long time atomistic polymer trajectories from coarse grained simulations: bisphenol-A polycarbonate. Soft Matter. 2:409-414.
37. Harmandaris, V. A., N. P. Adhikari, N. F. A. van der Vegt, K. Kremer, B. A. Mann, R. Voelkel, H. Weiss, and C. C. Liew. 2007. Ethylbenzene diffusion in polystyrene: united atom atomistic/coarse-grained simulations and experiments. Macromolar. 40:7026-7035.
38. Limbach, H. J., A. Arnold, B. A. Mann, and C. Holm. 2006. ESPResSo - an extensible simulation package for research on soft matter systems. Comput. Phys. Commun. 174:704-727.
39. Grest, G. S., and K. Kremer. 1986. Molecular-dynamics simulation for polymers in the presence of a heat bath. Phys. Rev. A. 33:3628-3631.
40. Kolb, A., and B. Dünweg. 1999. Optimized constant pressure stochastic dynamics. J. Chem. Phys. 111:4453-4459.
41. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.
42. Reynolds, J. A., D. B. Gilbert, and C. Tanford. 1974. Empirical correlation between hydrophobic free energy and aqueous cavity surface area. Proc. Natl. Acad. Sci. USA. 71:2925-2927.
43. Marcelja, S. 1976. Lipid-mediated protein interaction in membranes. Biochim. Biophys. Acta. 455:1-7.
44. Jähnig, F. 1981. Critical effects from lipid-protein interaction in membranes. Biophys. J. 36:329-345.
45. Sintes, T., and A. Baumgärtner. 1997. Protein attraction in membranes induced by lipid fluctuations. Biophys. J. 73:2251-2259.
46. Dan, N., P. Pincus, and S. A. Safran. 1993. Membrane-induced interactions between inclusions. Langmuir. 9:2768-2771.
47. Dan, N., A. Berman, P. Pincus, and S. A. Safran. 1994. Membrane-induced interactions between inclusions. J. Phys. II (France). 4:1713-1725.
48. Aranda-Espinoza, H., A. Berman, N. Dan, P. Pincus, and S. A. Safran. 1996. Interactions between inclusions embedded in membranes. Biophys. J. 71:648-656.
49. Sperotto, M. M., and O. G. Mouritsen. 1991. Mean-field and Monte Carlo simulation studies of the lateral distribution of proteins in membranes. Eur. Biophys. J. 19:157-168.
50. Zemel, A., D. R. Fattal, and A. Ben-Shaul. 2003. Energetics and self-assembly of amphipathic peptide pores in lipid membranes. Biophys. J. 84:2242-2255.
51. Frink, L. J. D., and A. L. Frischknecht. 2006. Computational investigations of pore forming peptide assemblies in lipid bilayers. Phys. Rev. Lett. 97:208701.
52. Panda, A. K., K. Nag, R. R. Harbottle, F. Possmayer, and N. O. Petersen. 2007. Thermodynamic studies of bovine lung surfactant extract mixing with cholesterol and its palmitate derivative. J. Colloid Interface Sci. 311:551-555.
53. Trabelsi, S., S. Zhang, T. R. Lee, and D. K. Schwartz. 2008. Linactants: surfactant analogues in two dimensions. Phys. Rev. Lett. 100:037802.
54. Lin, J.-H., and A. Baumgaertner. 2000. Stability of a melittin pore in a lipid bilayer: a molecular dynamics study. Biophys. J. 78:1714-1724.