3D hydrophobic moment vectors as a tool to characterize the surface polarity of amphiphilic peptides

Biophysical Journal

Volumn 106, Issue 11, 2014, Pages 2385-2394

  Reißer, Sabine ^a   Strandberg, Erik ^a   Steinbrecher, Thomas ^a   Ulrich, Anne S ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; GRAMICIDIN; LIPID BILAYER; PEPTIDE; PEPTIDE-GLY-LEU-AMIDE; PROTEIN BINDING;

ALGORITHM; AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; CHEMISTRY; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; STATIC ELECTRICITY;

ALGORITHMS; AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; GRAMICIDIN; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; STATIC ELECTRICITY;

EID: 84901992350     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.04.020     Document Type: Article

References (98)

1. J.P. Ulmschneider, and J.C. Smith E. Strandberg Reorientation and dimerization of the membrane-bound antimicrobial peptide PGLa from microsecond all-atom MD simulations Biophys. J. 103 2012 472 482
2. S. Özdirekcan, and C. Etchebest P.F. Fuchs On the orientation of a designed transmembrane peptide: toward the right tilt angle? J. Am. Chem. Soc. 129 2007 15174 15181 (Pubitemid 350247801)
3. J.P. Ulmschneider, and J.P.F. Doux M.B. Ulmschneider Peptide partitioning and folding into lipid bilayers J. Chem. Theory Comput. 5 2009 2202 2205
4. Y. Wang, and D.E. Schlamadinger J.A. McCammon Comparative molecular dynamics simulations of the antimicrobial peptide CM15 in model lipid bilayers Biochim. Biophys. Acta 1818 2012 1402 1409
5. S. Toraya, and N. Javkhlantugs A. Naito Dynamic structure of bombolitin II bound to lipid bilayers as revealed by solid-state NMR and molecular-dynamics simulation Biophys. J. 99 2010 3282 3289
6. S.K. Kandasamy, and R.G. Larson Effect of salt on the interactions of antimicrobial peptides with zwitterionic lipid bilayers Biochim. Biophys. Acta 1758 2006 1274 1284 (Pubitemid 44436074)
7. B.L. Kagan, and H. Jang R. Nussinov Antimicrobial properties of amyloid peptides Mol. Pharm. 9 2012 708 717
8. M. Mihajlovic, and T. Lazaridis Antimicrobial peptides bind more strongly to membrane pores Biochim. Biophys. Acta 1798 2010 1494 1502
9. M.B. Ulmschneider, and J.P. Doux J.P. Ulmschneider Mechanism and kinetics of peptide partitioning into membranes from all-atom simulations of thermostable peptides J. Am. Chem. Soc. 132 2010 3452 3460
10. M. Hartmann, and M. Berditsch A.S. Ulrich Damage of the bacterial cell envelope by antimicrobial peptides gramicidin S and PGLa as revealed by transmission and scanning electron microscopy Antimicrob. Agents Chemother. 54 2010 3132 3142
11. P. Tremouilhac, and E. Strandberg A.S. Ulrich Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin J. Biol. Chem. 281 2006 32089 32094 (Pubitemid 46036763)
12. C.S. Alves, and M.N. Melo M.A. Castanho Escherichia coli cell surface perturbation and disruption induced by antimicrobial peptides BP100 and pepR J. Biol. Chem. 285 2010 27536 27544
13. S.L. Grage, S. Afonin, and A.S. Ulrich Dynamic transitions of membrane-active peptides Methods Mol. Biol. 618 2010 183 207
14. S. Esteban-Martín, and E. Strandberg A.S. Ulrich Solid state NMR analysis of peptides in membranes: influence of dynamics and labeling scheme Biochim. Biophys. Acta 1798 2010 252 257
15. 2H-NMR data Biophys. J. 96 2009 3223 3232
16. 15N PISEMA NMR spectra of membrane proteins: a theoretical analysis Biophys. J. 96 2009 3233 3241
17. 2H solid-state NMR Biophys. J. 86 2004 3709 3721 (Pubitemid 38780249)
18. 2H NMR Biophys. J. 83 2002 1479 1488 (Pubitemid 34977721)
19. 19F-NMR methods for studying biomembranes Prog. Nucl. Magn. Reson. Spectrosc. 46 2005 1 21 (Pubitemid 40357060)
20. 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)
21. 19F-NMR analysis of oriented biomembranes G.A. Webb, Modern Magnetic Resonance 2006 Springer Dordrecht, The Netherlands 261 267
22. 19F-labeled amino acids and solid-state NMR I. Ojima, Fluorine in Medicinal Chemistry and Chemical Biology 2009 Blackwell London 463 493
23. J.D. Gehman, and F. Separovic Solid-state NMR of membrane-active proteins and peptides G.A. Webb, Modern Magnetic Resonance 2006 Springer Dordrecht, The Netherlands 305 311
24. 2H NMR study Biochemistry 44 2005 1004 1012 (Pubitemid 40129660)
25. N.J. Gleason, and V.V. Vostrikov R.E. Koeppe 2nd Buried lysine, but not arginine, titrates and alters transmembrane helix tilt Proc. Natl. Acad. Sci. USA 110 2013 1692 1695
26. V.V. Vostrikov, and A.E. Daily R.E. Koeppe 2nd Charged or aromatic anchor residue dependence of transmembrane peptide tilt J. Biol. Chem. 285 2010 31723 31730
27. E. Strandberg, and D. Tiltak A.S. Ulrich Lipid shape is a key factor for membrane interactions of amphipathic helical peptides Biochim. Biophys. Acta 1818 2012 1764 1776
28. E. Strandberg, and S. Esteban-Martín J. Salgado Hydrophobic mismatch of mobile transmembrane helices: merging theory and experiments Biochim. Biophys. Acta 1818 2012 1242 1249
29. E. Strandberg, and N. Kanithasen A.S. Ulrich Solid-state NMR analysis comparing the designer-made antibiotic MSI-103 with its parent peptide PGLa in lipid bilayers Biochemistry 47 2008 2601 2616 (Pubitemid 351304566)
30. 19F-NMR Biophys. J. 90 2006 1676 1686
31. B. Bechinger, and Y. Kim S.J. Opella Orientations of amphipathic helical peptides in membrane bilayers determined by solid-state NMR spectroscopy J. Biomol. NMR 1 1991 167 173
32. A. Ramamoorthy, Y.F. Wei, and D.K. Lee PISEMA solid-state NMR spectroscopy Annu. Rep. NMR Spectrosc. 52 2004 1 52 (Pubitemid 39752334)
33. J.K. Denny, and J.F. Wang J.R. Quine PISEMA powder patterns and PISA wheels J. Magn. Reson. 152 2001 217 226
34. M.S. Balla, J.H. Bowie, and F. Separovic Solid-state NMR study of antimicrobial peptides from Australian frogs in phospholipid membranes Eur. Biophys. J. 33 2004 109 116 (Pubitemid 38987097)
35. 15N-NMR: mobility matters Eur. Biophys. J. 41 2012 475 482
36. d of the twin-arginine translocase from Bacillus subtilis resolved by solid-state NMR spectroscopy J. Am. Chem. Soc. 132 2010 15945 15956
37. 19F-NMR of peptides in native membranes Top. Curr. Chem. 306 2012 89 118
38. 19F NMR J. Am. Chem. Soc. 134 2012 6512 6515
39. 19F NMR analysis of the antimicrobial peptide PGLa bound to native cell membranes from bacterial protoplasts and human erythrocytes J. Am. Chem. Soc. 132 2010 8822 8824
40. 19F NMR analysis of peptaibols in membranes J. Am. Chem. Soc. 131 2009 15596 15597
41. 19F NMR spectroscopy J. Am. Chem. Soc. 130 2008 16512 16514
42. 19F NMR label to monitor and to control peptide aggregation in membranes J. Am. Chem. Soc. 130 2008 16515 16517
43. 19F NMR parameters of fluorine-labeled amino acids. Part I: Aromatic substituents J. Magn. Reson. 191 2008 7 15
44. 19F NMR parameters of fluorine-labeled amino acids. Part II: Aliphatic substituents J. Magn. Reson. 191 2008 16 23
45. 41 participates in the gating mechanism of the M2 proton channel of influenza A virus J. Am. Chem. Soc. 130 2008 918 924
46. 19F-NMR Biophys. J. 88 2005 3392 3397 (Pubitemid 40586589)
47. 3-phenylglycine labels J. Magn. Reson. 168 2004 153 163
48. 19F-NMR J. Biomol. NMR 21 2001 191 208 (Pubitemid 33133421)
49. S. Afonin, and U.H.N. Dürr A.S. Ulrich Solid state NMR structure analysis of the antimicrobial peptide gramicidin S in lipid membranes: concentration-dependent re-alignment and self-assembly as a β-barrel Top. Curr. Chem. 273 2008 139 154
50. 19F NMR Magn. Reson. Chem. 42 2004 195 203 (Pubitemid 38178089)
51. 19F-NMR structure analysis of membrane-bound peptides J. Pept. Sci. 13 2007 614 623 (Pubitemid 47490326)
52. J. Bürck, and S. Roth A.S. Ulrich Conformation and membrane orientation of amphiphilic helical peptides by oriented circular dichroism Biophys. J. 95 2008 3872 3881
53. G.A. Olah, and H.W. Huang Circular dichroism of oriented α-helices. II. Electric field oriented polypeptides J. Chem. Phys. 89 1988 6956 6962
54. G.A. Olah, and H.W. Huang Circular dichroism of oriented α-helices. I. Proof of the exciton theory J. Chem. Phys. 89 1988 2531 2538
55. Y. Wu, H.W. Huang, and G.A. Olah Method of oriented circular dichroism Biophys. J. 57 1990 797 806 (Pubitemid 20111238)
56. O.V. Nolandt, and T.H. Walther A.S. Ulrich Structure analysis of the membrane protein TatC(d) from the Tat system of B. subtilis by circular dichroism Biochim. Biophys. Acta 1788 2009 2238 2244
57. R. Heinzmann, and S.L. Grage A.S. Ulrich A kinked antimicrobial peptide from Bombina maxima. II. Behavior in phospholipid bilayers Eur. Biophys. J. 40 2011 463 470
58. T. Steinbrecher, and S. Prock A.S. Ulrich Peptide-lipid interactions of the stress-response peptide TisB that induces bacterial persistence Biophys. J. 103 2012 1460 1469
59. 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
60. J.C. Hsu, and C.M. Yip Molecular dynamics simulations of indolicidin association with model lipid bilayers Biophys. J. 92 2007 L100 L102
61. S. Esteban-Martín, and J. Salgado The dynamic orientation of membrane-bound peptides: bridging simulations and experiments Biophys. J. 93 2007 4278 4288 (Pubitemid 350294475)
62. Y. Wang, T. Zhao, D. Wei, A.S. Ulrich, E. Strandberg, and J.P. Ulmschneider How reliable are molecular dynamics simulations of membrane active antimicrobial peptides? Biochim. Biophys. Acta 2014 10.1016/j.bbamem.2014.04.009 In press
63. Q. Du, P.G. Mezey, and K.C. Chou Heuristic molecular lipophilicity potential (HMLP): a 2D-QSAR study to LADH of molecular family pyrazole and derivatives J. Comput. Chem. 26 2005 461 470 (Pubitemid 40449458)
64. R.G. Efremov, and A.O. Chugunov E. Jacoby Molecular lipophilicity in protein modeling and drug design Curr. Med. Chem. 14 2007 393 415
65. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 3 1996 842 848 (Pubitemid 26330634)
66. W.C. Wimley, T.P. Creamer, and S.H. White Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides Biochemistry 35 1996 5109 5124
67. D.M. Engelman, T.A. Steitz, and A. Goldman Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins Annu. Rev. Biophys. Biophys. Chem. 15 1986 321 353
68. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132
69. S.A. Wildman, and G.M. Crippen Prediction of physicochemical parameters by atomic contributions J. Chem. Inf. Comput. Sci. 39 1999 868 873
70. C. Snider, and S. Jayasinghe S.H. White MPEx: a tool for exploring membrane proteins Protein Sci. 18 2009 2624 2628
71. D. Eisenberg, R.M. Weiss, and T.C. Terwilliger The helical hydrophobic moment: a measure of the amphiphilicity of a helix Nature 299 1982 371 374 (Pubitemid 12012871)
72. D. Eisenberg, and R.M. Weiss W. Wilcox Hydrophobic moments and protein structure Faraday Sym.p Chem. Soc. 17 1982 109 120
73. T. Beuming, and H. Weinstein A knowledge-based scale for the analysis and prediction of buried and exposed faces of transmembrane domain proteins Bioinformatics 20 2004 1822 1835 (Pubitemid 39199046)
74. S.B. Vik The transmembrane helices of the L, M, and N subunits of Complex I from E. coli can be assigned on the basis of conservation and hydrophobic moment analysis FEBS Lett. 585 2011 1180 1184
75. E. Soravia, G. Martini, and M. Zasloff Antimicrobial properties of peptides from Xenopus granular gland secretions FEBS Lett. 228 1988 337 340
76. B. Bechinger, M. Zasloff, and S.J. Opella Structure and dynamics of the antibiotic peptide PGLa in membranes by solution and solid-state nuclear magnetic resonance spectroscopy Biophys. J. 74 1998 981 987 (Pubitemid 28345291)
77. 2H-NMR Biochim. Biophys. Acta 1758 2006 1330 1342 (Pubitemid 44436073)
78. E. Strandberg, and D. Tiltak A.S. Ulrich Influence of C-terminal amidation on the antimicrobial and hemolytic activities of cationic α-helical peptides Pure Appl. Chem. 79 2007 717 728
79. E. Strandberg, and P. Tremouilhac A.S. Ulrich Synergistic transmembrane insertion of the heterodimeric PGLa/magainin 2 complex studied by solid-state NMR Biochim. Biophys. Acta 1788 2009 1667 1679
80. G.G. Gause, and M.G. Brazhnikova Gramicidin S and its use in the treatment of infected wounds Nature 154 1944 703
81. G.F. Gause, and M.G. Brazhnikova Gramicidin S. Origin and mode of action Lancet 247 1944 715 716
82. 3-groups in a membrane-bound peptide J. Magn. Reson. 183 2006 77 86 (Pubitemid 44692517)
83. S. Pronk, and S. Páll E. Lindahl GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 29 2013 845 854
84. K. Lindorff-Larsen, and S. Piana D.E. Shaw Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 78 2010 1950 1958
85. J.P.M. Jämbeck, and A.P. Lyubartsev Derivation and systematic validation of a refined all-atom force field for phosphatidylcholine lipids J. Phys. Chem. B 116 2012 3164 3179
86. D.A. Case, and T.A. Darden P.A. Kollman AMBER 12 2012 University of California San Francisco
87. Y. Xu, I.P. Sugár, and N.R. Krishna A variable target intensity-restrained global optimization (VARTIGO) procedure for determining three-dimensional structures of polypeptides from NOESY data: application to gramicidin-S J. Biomol. NMR 5 1995 37 48
88. S. Nosé A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 52 1984 255 268
89. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190 (Pubitemid 12456820)
90. B. Hess, and H. Bekker J.G.E.M. Fraaije LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472 (Pubitemid 127637344)
91. D. Sitkoff, K.A. Sharp, and B. Honig Accurate calculation of hydration free energies using macroscopic solvent models J. Phys. Chem 98 1994 1978 1988
92. S. Decherchi, and W. Rocchia A general and robust ray-casting-based algorithm for triangulating surfaces at the nanoscale PLoS ONE 8 2013 e59744
93. N.A. Baker, and D. Sept J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. USA 98 2001 10037 10041 (Pubitemid 32802969)
94. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28 (Pubitemid 26152973)
95. A. Latal, and G. Degovics K. Lohner Structural aspects of the interaction of peptidyl-glycylleucine-carboxyamide, a highly potent antimicrobial peptide from frog skin, with lipids Eur. J. Biochem. 248 1997 938 946 (Pubitemid 27400053)
96. C. Muhle-Goll, and S. Hoffmann A.S. Ulrich Hydrophobic matching controls the tilt and stability of the dimeric platelet-derived growth factor receptor (PDGFR) β transmembrane segment J. Biol. Chem. 287 2012 26178 26186
97. E. Strandberg, and J. Zerweck A.S. Ulrich Synergistic insertion of antimicrobial magainin-family peptides in membranes depends on the lipid spontaneous curvature Biophys. J. 104 2013 L9 L11
98. 19F-NMR screening of unrelated antimicrobial peptides shows that membrane interactions are governed by lipids Biochim. Biophys. Acta 2014 10.1016/j.bbamem.2014.03.017 In press