Spontaneous adsorption of coiled-coil model peptides K and e to a mixed lipid bilayer

Journal of Physical Chemistry B

Volumn 119, Issue 12, 2015, Pages 4396-4408

  Pluhackova, Kristyna ^a   Wassenaar, Tsjerk A ^a   Kirsch, Sonja ^a   Bockmann, Rainer A ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADSORPTION; AMINO ACIDS; BINDING ENERGY; BIOINFORMATICS; CELL MEMBRANES; LIPID BILAYERS; MEMBRANES; MOLECULAR DYNAMICS; PEPTIDES; PHOSPHOLIPIDS;

ADSORPTION OF PROTEINS; BACKWARD TRANSFORMATIONS; COARSE-GRAINED FORCE FIELDS; COARSE-GRAINED MOLECULAR DYNAMICS SIMULATIONS; LIPID-PROTEIN INTERACTIONS; MOLECULAR DESCRIPTIONS; REVERSE TRANSFORMATION; SPONTANEOUS ADSORPTION;

PROTEINS;

CHOLESTEROL; ENKEPHALIN; LIPID BILAYER; PEPTIDE E (ADRENAL MEDULLA); PHOSPHOLIPID; PROTEIN BINDING; WATER;

ADSORPTION; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; LIPID BILAYER; MOLECULAR DYNAMICS; PROTEIN SECONDARY STRUCTURE;

ADSORPTION; CHOLESTEROL; ENKEPHALINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; PHOSPHOLIPIDS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; WATER;

EID: 84925957020     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b00434     Document Type: Article

References (65)

1. Johnson, J. E.; Cornell, R. B. Amphitropic proteins: regulation by reversible membrane interactions (Review) Mol. Membr. Biol. 1999, 16, 217-235
2. Castanho, M. A. R. B. Membrane-Active Peptides: Methods and Results On Structure and Function; International University Line: La Jolla, CA, 2010.
3. Rzepiela, A. J.; Sengupta, D.; Goga, N.; Marrink, S. J. Membrane poration by antimicrobial peptides combining atomistic and coarse-grained descriptions Faraday Discuss. 2010, 144, 431-443
4. Gidalevitz, D.; Ishitsuka, Y.; Muresan, A. S.; Konovalov, O.; Waring, A. J.; Lehrer, R. I.; Lee, K. Y. C. Interaction of antimicrobial peptide protegrin with biomembranes Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 6302-6307
5. Damodaran, K. V.; Merz, K. M. Interaction of the fusion inhibiting peptide carbobenzoxy- d -Phe- l -Phe-Gly with N -methyldioleoylphosphatidylethanolamine lipid bilayers J. Am. Chem. Soc. 1995, 117, 6561-6571
6. Tieleman, D. P.; Berendsen, H. J. C.; Sansom, M. S. P. Surface binding of alamethicin stabilizes its helical structure: molecular dynamics simulations Biophys. J. 1999, 76, 3186-3191
7. Shepherd, C. M.; Schaus, K. A.; Vogel, H. J.; Juffer, A. H. Molecular dynamics study of peptide-bilayer adsorption Biophys. J. 2001, 80, 579-596
8. Ulmschneider, J. P.; Doux, J. P. F.; Killian, J. A.; Smith, J. C.; Ulmschneider, M. B. Peptide partitioning and folding into lipid bilayers J. Chem. Theory Comput. 2009, 5, 2202-2205
9. Jia, Y.; Qian, Z.; Zhang, Y.; Wei, G. Adsorption and orientation of human islet amyloid polypeptide (hIAPP) monomer at anionic lipid bilayers: Implications for membrane-mediated aggregation Int. J. Mol. Sci. 2013, 14, 6241-6258
10. Kalli, A. C.; Devaney, I.; Sansom, M. S. P. Interactions of phosphatase and tensin homologue (PTEN) proteins with phosphatidylinositol phosphates: Insights from molecular dynamics simulations of PTEN and voltage sensitive phosphatase Biochemistry 2014, 53, 1724-1732
11. Chen, C. H.; Wiedman, G.; Khan, A.; Ulmschneider, M. B. Absorption and folding of melittin onto lipid bilayer membranes via unbiased atomic detail microsecond molecular dynamics simulation Biochim. Biophys. Acta, Biomembr. 2014, 1838, 2243-2249
12. Vivcharuk, V.; Tomberli, B.; Tolokh, I. S.; Gray, C. G. Prediction of binding free energy for adsorption of antimicrobial peptide lactoferricin B on a POPC membrane Phys. Rev. E 2008, 77, 031913
13. Terama, E.; Ollila, O. H. S.; Salonen, E.; Rowat, A. C.; Trandum, C.; Westh, P.; Patra, M.; Karttunen, M.; Vattulainen, I. Influence of ethanol on lipid membranes: From lateral pressure profiles to dynamics and partitioning J. Phys. Chem. B 2008, 112, 4131-4139
14. Griepernau, B.; Leis, S.; Schneider, M. F.; Sikor, M.; Steppich, D.; Bockmann, R. A. 1-Alkanols and membranes: A story of attraction Biochim. Biophys. Acta, Biomembr. 2007, 1768, 2899-2913
15. Griepernau, B.; Bockmann, R. A. The influence of 1-alkanols and external pressure on the lateral pressure profiles of lipid bilayers Biophys. J. 2008, 95, 5766-5778
16. Vemparala, S.; Saiz, L.; Eckenhoff, R. G.; Klein, M. L. Partitioning of anesthetics into a lipid bilayer and their interaction with membrane-bound peptide bundles Biophys. J. 2006, 91, 2815-2825
17. Wassenaar, T. A.; Pluhackova, K.; Moussatova, A.; Sengupta, D.; Marrink, S. J.; Tieleman, D. P.; Bockmann, R. A. High-throughput simulations of dimer and trimer assembly of membrane proteins. The DAFT approach. Submitted, 2015
18. Pawar, A. B.; Deshpande, S. A.; Gopal, S. M.; Wassenaar, T. A.; Athale, C. A.; Sengupta, D. Thermodynamic and kinetic characterization of transmembrane helix association Phys. Chem. Chem. Phys. 2015, 1390-1398
19. Litowski, J. R.; Hodges, R. S. Designing heterodimeric two-stranded -helical coiled-coils: Effects of hydrophobicity and -helical propensity on protein folding, stability, and specificity J. Bio. Chem. 2002, 277, 37272-37279
20. Pahler, G.; Panse, C.; Diederichsen, U.; Janshoff, A. Coiled-coil formation on lipid bilayers-implications for docking and fusion efficiency Biophys. J. 2012, 103, 2295-2303
21. Robson Marsden, H.; Elbers, N. A.; Bomans, P. H. H.; Sommerdijk, N. A. J. M.; Kros, A. A reduced SNARE model for membrane fusion Angew. Chem., Int. Ed. Engl. 2009, 48, 2330-2333
22. Versluis, F.; Voskuhl, J.; van Kolck, B.; Zope, H.; Bremmer, M.; Albregtse, T.; Kros, A. In situ modification of plain liposomes with lipidated coiled coil forming peptides induces membrane fusion J. Am. Chem. Soc. 2013, 135, 8057-8062
23. Lindhout, D. A.; Litowski, J. R.; Mercier, P.; Hodges, R. S.; Sykes, B. D. NMR solution structure of a highly stable de novo heterodimeric coiled-coil Biopolymers 2004, 75, 367-375
24. Rabe, M.; Schwieger, C.; Zope, H. R.; Versluis, F.; Kros, A. Membrane interactions of fusogenic coiled-coil peptides: Implications for lipopeptide mediated vesicle fusion Langmuir 2014, 30, 7724-7735
25. Pluhackova, K.; Wassenaar, T. A.; Bockmann, R. A. Methods in Molecular Biology. In Membrane Biogenesis; Rapaport, D.; Herrmann, J. M., Eds.; Humana Press: New York, 2013; Vol. 1033, pp 85-101.
26. Wassenaar, T. A.; Ingolfsson, H. I.; Bockmann, R. A.; Tieleman, D. P.; Marrink, S. J. Computational lipidomics with insane: A versatile tool for generating custom membranes for molecular simulations. Submitted, 2015
27. Marrink, S. J.; Risselada, H. J.; Yefimov, S.; Tieleman, D. P.; de Vries, A. H. The MARTINI force field: Coarse grained model for biomolecular simulations J. Phys. Chem. B 2007, 111, 7812-7824
28. Marrink, S. J.; de Vries, A. H.; Mark, A. E. Coarse grained model for semiquantitative lipid simulations J. Phys. Chem. B 2004, 108, 750-760
29. Monticelli, L.; Kandasamy, S. K.; Periole, X.; Larson, R. G.; Tieleman, D. P.; Marrink, S.-J. The MARTINI Coarse-Grained Force Field: Extension to Proteins J. Chem. Theory Comput. 2008, 4, 819-834
30. Lopez, C. A.; Rzepiela, A. J.; de Vries, A. H.; Dijkhuizen, L.; Hunenberger, P. H.; Marrink, S.-J. Martini Coarse-Grained Force Field: Extension to Carbohydrates J. Chem. Theory Comput. 2009, 5, 3195-3210
31. Khalfa, A.; Tarek, M. On the antibacterial action of cyclic peptides: Insights from coarse-grained MD simulations J. Phys. Chem. B 2010, 114, 2676-2684
32. Thøgersen, L.; Schiøtt, B.; Vosegaard, T.; Nielsen, N. C.; Tajkhorshid, E. Peptide aggregation and pore formation in a lipid bilayer: A combined coarse-grained and all atom molecular dynamics study Biophys. J. 2008, 95, 4337-4347
33. Bennett, W. F. D.; Tieleman, D. P. Water defect and pore formation in atomistic and coarse-grained lipid membranes: Pushing the limits of coarse graining J. Chem. Theory Comput. 2011, 7, 2981-2988
34. de Jong, D. H.; Singh, G.; Bennett, W. F. D.; Arnarez, C.; Wassenaar, T. A.; Schafer, L. V.; Periole, X.; Tieleman, D. P.; Marrink, S. J. Improved parameters for the Martini coarse-grained protein force field J. Chem. Theory Comput. 2013, 9, 687-697
35. Kleinschmidt, J. H. Membrane protein folding on the example of outer membrane protein A of Escherichia coli Cell. Mol. Life Sci. 2003, 60, 1547-1558
36. Sinthuvanich, C.; Veiga, A. S.; Gupta, K.; Gaspar, D.; Blumenthal, R.; Schneider, J. P. Anticancer -hairpin peptides: Membrane-induced folding triggers activity J. Am. Chem. Soc. 2012, 134, 6210-6217
37. Wassenaar, T. A.; Pluhackova, K.; Bockmann, R. A.; Marrink, S. J.; Tieleman, D. P. Going backward: A flexible geometric approach to reverse transformation from coarse grained to atomistic models J. Chem. Theory Comput. 2014, 10, 676-690
38. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for highly efficient load-balanced and scalable molecular simulations J. Chem. Theory Comput. 2008, 4, 435-447
39. Wassenaar, T. A.; Ingolfsson, H. I.; Prieß, M.; Marrink, S. J.; Schafer, L. V. Mixing Martini: Electrostatic coupling in hybrid atomistic-coarse-grained biomolecular simulations J. Phys. Chem. B 2013, 117, 3516-3530
40. The PyMOL Molecular Graphics System, Version 1.3r1; Schrodinger LLC, 2010.
41. Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling J. Chem. Phys. 2007, 126, 014101
42. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
43. van der Spoel, D.; van Maaren, P. J. The origin of layer structure artifacts in simulations of liquid water J. Chem. Theory Comput. 2006, 2, 1-11
44. Yesylevskyy, S. O.; Schafer, L. V.; Sengupta, D.; Marrink, S. J. Polarizable water model for the coarse-grained MARTINI force field PLoS Comput. Biol. 2010, 6, e1000810
45. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98, 10089-10092
46. Best, R. B.; Zhu, X.; Shim, J.; Lopes, P. E. M.; Mittal, J.; Feig, M.; MacKerell, A. D. Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone, and side-chain 1 and 2 dihedral angles J. Chem. Theory Comput. 2012, 8, 3257-3273
47. Klauda, J. B.; Venable, R. M.; Freites, J. A.; OConnor, J. W.; Tobias, D. J.; Mondragon-Ramirez, C.; Vorobyov, I.; MacKerell, A. D.; Pastor, R. W. Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types J. Phys. Chem. B 2010, 114, 7830-7843
48. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
49. Bjelkmar, P.; Larsson, P.; Cuendet, M. A.; Hess, B.; Lindahl, E. Implementation of the CHARMM force field in GROMACS: Analysis of protein stability effects from correction maps, virtual interaction sites, and water models J. Chem. Theory Comput. 2010, 6, 459-466
50. Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method J. Appl. Phys. 1981, 52, 7182-7190
51. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, G. E. M. J LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 1997, 18, 1463-1472
52. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins: Struct., Funct., Bioinf. 2006, 65, 712-725
53. Jambeck, J. P. M.; Lyubartsev, A. P. An extension and further validation of an all-atomistic force field for biological membranes J. Chem. Theory Comput. 2012, 8, 2938-2948
54. Jambeck, J. P. M.; Lyubartsev, A. P. Another piece of the membrane puzzle: Extending Slipids further J. Chem. Theory Comput. 2013, 9, 774-784
55. Nosé, S. A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 1984, 100, 191-198
56. Hoover, W. G. Canonical dynamics: Equilibrium phase-space distributions Phys. Rev. A 1985, 31, 1695-1697
57. R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2008.
58. Pannuzzo, M.; Raudino, A.; Bockmann, R. A. Peptide-induced membrane curvature in edge-stabilized open bilayers: A theoretical and molecular dynamics study J. Chem. Phys. 2014, 141, 024901
59. Nawae, W.; Hannongbua, S.; Ruengjitchatchawalya, M. Defining the membrane disruption mechanism of kalata B1 via coarse-grained molecular dynamics simulations Sci. Rep. 2014, 4, 3933
60. Wang, Z.; Wang, G. APD: The antimicrobial peptide database Nucleic Acids Res. 2004, 32, D590-D592
61. Segrest, J. P.; Jones, M. K.; de Loof, H.; Brouillette, C. G.; Venkatachalapathi, Y. V.; Anantharamaiah, G. M. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function J. Lipid Res. 1992, 33, 141-66
62. Wimley, W. C.; White, S. H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 1996, 3, 842-848
63. Wang, W.; Yang, L.; Huang, H. W. Evidence of cholesterol accumulated in high curvature regions: Implication to the curvature elastic energy for lipid mixtures Biophys. J. 2007, 92, 2819-2830
64. Knecht, V.; Grubmuller, H. Mechanical coupling via the membrane fusion SNARE protein Syntaxin-1A: A molecular dynamics study Biophys. J. 2003, 84, 1527-1547
65. Borisovska, M.; Schwarz, Y. N.; Dhara, M.; Yarzagaray, A.; Hugo, S.; Narzi, D.; Siu, S. W. I.; Kesavan, J.; Mohrmann, R.; Bockmann, R. A.; Bruns, D. Membrane-proximal tryptophans of synaptobrevin II stabilize priming of secretory vesicles J. Neurosci. 2012, 32, 15983-15997