Structures of β-hairpin antimicrobial protegrin peptides in lipopolysaccharide membranes: Mechanism of gram selectivity obtained from solid-state nuclear magnetic resonance

Biochemistry

Volumn 50, Issue 12, 2011, Pages 2072-2083

  Su, Yongchao ^a   Waring, Alan J ^b,c   Ruchala, Piotr ^b   Hong, Mei ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-MICROBIAL ACTIVITY; ARG RESIDUES; DIPOLAR COUPLINGS; ELECTROSTATIC ATTRACTIONS; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIUM; HAIRPIN ANTIMICROBIAL PEPTIDES; HAIRPIN CONFORMATION; INNER MEMBRANES; LINE SHAPE; LIPID CHAINS; LIPOPOLYSACCHARIDES; MEMBRANE SURFACE; ORIENTATIONAL DISORDER; OUTER MEMBRANE; PHYSIOLOGICAL TEMPERATURE; PORE DEFECTS; POTENT ACTIVITY; SOLID STATE NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SOLID-STATE NUCLEAR MAGNETIC RESONANCE; SPIN DIFFUSIONS; STRUCTURAL BASIS; TIME-SCALES; TOPOLOGICAL STRUCTURE; TRANS-MEMBRANE PORES;

AMINO ACIDS; BACTERIA; BACTERIOLOGY; CHROMATOGRAPHY; ELECTROSTATICS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; POLYPEPTIDES; RESONANCE; SURFACE DIFFUSION;

MEMBRANES;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; ANTIBIOTIC AGENT; ARGININE; IB 484; LIPOPOLYSACCHARIDE; PHOSPHORUS 31; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEGRIN; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; CELL MEMBRANE; DISULFIDE BOND; DRUG SELECTIVITY; DRUG STRUCTURE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; MINIMUM INHIBITORY CONCENTRATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PSEUDOMONAS AERUGINOSA; SOLID STATE;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; BIOMIMETICS; CELL MEMBRANE; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; GUANIDINE; LIPOPOLYSACCHARIDES; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; SPECIES SPECIFICITY;

NEGIBACTERIA; POSIBACTERIA;

EID: 79952980526     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101975v     Document Type: Article

References (79)

1. Fischbach, M. A. and Walsh, C. T. (2009) Antibiotics for emerging pathogens Science 325, 1089-1093
2. Levy, S. B. and Marshall, B. (2004) Antibacterial resistance worldwide: Causes, challenges and responses Nat. Med. 10, S122-S129
3. Hancock, R. E. and Sahl, H. G. (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 24, 1551-1557 (Pubitemid 44967479)
4. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms Nature 415, 389-395 (Pubitemid 34100944)
5. Brogden, K. A. (2005) Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250 (Pubitemid 40298223)
6. Tang, M. and Hong, M. (2009) Structure and mechanism of β-hairpin antimicrobial peptides in lipid bilayers from solid-state NMR spectroscopy Mol. Biosyst. 5, 317-322
7. Epand, R. M. and Vogel, H. J. (1999) Diversity of antimicrobial peptides and their mechanisms of action Biochim. Biophys. Acta 1462, 11-28
8. Huang, H. W. (2000) Action of antimicrobial peptides: Two-state model Biochemistry 39, 8347-8352 (Pubitemid 30489931)
9. Kagan, B. L., Selsted, M. E., Ganz, T., and Lehrer, R. I. (1990) Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes Proc. Natl. Acad. Sci. U.S.A. 87, 210-214
10. Westerhoff, H. V., Juretić, D., Hendler, R. W., and Zasloff, M. (1989) Magainins and the disruption of membrane-linked free-energy transduction Proc. Natl. Acad. Sci. U.S.A. 86, 6597-6601 (Pubitemid 19236322)
11. Sperandeo, P., Dehò, G., and Polissi, A. (2009) The lipopolysaccharide transport system of Gram-negative bacteria Biochim. Biophys. Acta 1791, 594-602
12. Rosenfeld, Y. and Shai, Y. (2006) Lipopolysaccharide (endotoxin)-host defense antibacterial peptides interactions: Role in bacterial resistance and prevention of sepsis Biochim. Biophys. Acta 1758, 1513-1522 (Pubitemid 44436084)
13. Lehrer, R. I., Barton, A., Daher, K. A., Harwig, S. S., Ganz, T., and Selsted, M. E. (1989) Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity J. Clin. Invest. 84, 553-561 (Pubitemid 19196987)
14. Mares, J., Kumaran, S., Gobbo, M., and Zerbe, O. (2009) Interactions of lipopolysaccharide and polymyxin studied by NMR spectroscopy J. Biol. Chem. 284, 11498-11506
15. Hancock, R. E. and Scott, M. G. (2000) The role of antimicrobial peptides in animal defenses Proc. Natl. Acad. Sci. U.S.A. 97, 8856-8861 (Pubitemid 30626637)
16. Raetz, C. R., Garrett, T. A., Reynolds, C. M., Shaw, W. A., Moore, J. D., Smith, D. C., Ribeiro, A. A., Murphy, R. C., Ulevitch, R. J., Fearns, C., Reichart, D., Glass, C. K., Benner, C., Subramaniam, S., Harkewicz, R., Bowers-Gentry, R. C., Buczynski, M. W., Cooper, J. A., Deems, R. A., and Dennis, E. A. (2006) Kdo2-Lipid A of Escherichia coli, a defined endotoxin that activates macrophages via TLR-4 J. Lipid Res. 47, 1097-1111 (Pubitemid 43764706)
17. Bhunia, A., Domadia, P. N., Torres, J., Hallock, K. J., Ramamoorthy, A., and Bhattacharjya, S. (2010) NMR structure of pardaxin, a pore-forming antimicrobial peptide, in lipopolysaccharide micelles: Mechanism of outer membrane permeabilization J. Biol. Chem. 285, 3883-3895
18. Hammer, M. U., Brauser, A., Olak, C., Brezesinski, G., Goldmann, T., Gutsmann, T., and Andrä, J. (2010) Lipopolysaccharide interaction is decisive for the activity of the antimicrobial peptide NK-2 against Escherichia coli and Proteus mirabilis Biochem. J. 427, 477-488
19. Rosenfeld, Y., Barra, D., Simmaco, M., Shai, Y., and Mangoni, M. L. (2006) A synergism between temporins toward Gram-negative bacteria overcomes resistance imposed by the lipopolysaccharide protective layer J. Biol. Chem. 281, 28565-28574 (Pubitemid 44506999)
20. Zhang, L., Scott, M. G., Yan, H., Mayer, L. D., and Hancock, R. E. (2000) Interaction of polyphemusin I and structural analogs with bacterial membranes, lipopolysaccharide, and lipid monolayers Biochemistry 39, 14504-14514
21. Lienkamp, K., Kumar, K. N., Som, A., Nüsslein, K., and Tew, G. N. (2009) "Doubly selective" antimicrobial polymers: How do they differentiate between bacteria? Chem.-Eur. J. 15, 11710-11714
22. Böhling, A., Hagge, S. O., Roes, S., Podschun, R., Sahly, H., Harder, J., Schröder, J. M., Grötzinger, J., Seydel, U., and Gutsmann, T. (2006) Lipid-specific membrane activity of human β-defensin-3 Biochemistry 45, 5663-5670 (Pubitemid 43673196)
23. Bellm, L., Lehrer, R. I., and Ganz, T. (2000) Protegrins: New antibiotics of mammalian origin Expert Opin. Invest. Drugs 9, 1731-1742 (Pubitemid 30639324)
24. Tam, J. P., Wu, C., and Yang, J. L. (2000) Membranolytic selectivity of cystine-stabilized cyclic protegrins Eur. J. Biochem. 267, 3289-3300 (Pubitemid 30341157)
25. Chen, J., Falla, T. J., Liu, H., Hurst, M. A., Fujii, C. A., Mosca, D. A., Embree, J. R., Loury, D. J., Radel, P. A., Cheng, C. C., Gu, L., and Fiddes, J. C. (2000) Development of protegrins for the treatment and prevention of oral mucositis: Structure-activity relationships of synthetic protegrin analogues Biopolymers 55, 88-98
26. Mani, R., Cady, S. D., Tang, M., Waring, A. J., Lehrer, R. I., and Hong, M. (2006) Membrane-dependent oligomeric structure and pore formation of a β-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR Proc. Natl. Acad. Sci. U.S.A. 103, 16242-16247 (Pubitemid 44715181)
27. Tang, M., Waring, A. J., and Hong, M. (2007) Phosphate-Mediated Arginine Insertion into Lipid Membranes and Pore Formation by a Cationic Membrane Peptide from Solid-State NMR J. Am. Chem. Soc. 129, 11438-11446 (Pubitemid 47555563)
28. Mani, R., Tang, M., Wu, X., Buffy, J. J., Waring, A. J., Sherman, M. A., and Hong, M. (2006) Membrane-bound dimer structure of a β-hairpin antimicrobial peptide from rotational-echo double-resonance solid-state NMR Biochemistry 45, 8341-8349 (Pubitemid 44036540)
29. Yamaguchi, S., Hong, T., Waring, A., Lehrer, R. I., and Hong, M. (2002) Solid-state NMR investigations of peptide-lipid interaction and orientation of a β-sheet antimicrobial peptide, protegrin Biochemistry 41, 9852-9862 (Pubitemid 34839733)
30. Buffy, J. J., Waring, A. J., Lehrer, R. I., and Hong, M. (2003) Immobilization and aggregation of the antimicrobial peptide protegrin-1 in lipid bilayers investigated by solid-state NMR Biochemistry 42, 13725-13734 (Pubitemid 37444922)
31. Mani, R., Buffy, J. J., Waring, A. J., Lehrer, R. I., and Hong, M. (2004) Solid-state NMR investigation of the selective disruption of lipid membranes by protegrin-1 Biochemistry 43, 13839-13848 (Pubitemid 39431067)
32. 1H NMR study Biochim. Biophys. Acta 1716, 11-18 (Pubitemid 41379397)
33. 2H solid-state NMR study J. Phys. Chem. B 112, 11402-11414
34. Sasaki, H. and White, S. H. (2008) Aggregation Behavior of an Ultra-Pure Lipopolysaccharide that Stimulates TLR-4 Receptors Biophys. J. 95, 986-993
35. Harwig, S. S., Swiderek, K. M., Lee, T. D., and Lehrer, R. I. (1995) Determination of disulphide bridges in PG-2, an antimicrobial peptide from porcine leukocytes J. Pept. Sci. 1, 207-215
36. Aumelas, A., Mangoni, M., Roumestand, C., Chiche, L., Despaux, E., Grassy, G., Calas, B., and Chavanieu, A. (1996) Synthesis and solution structure of the antimicrobial peptide protegrin-1 Eur. J. Biochem. 237, 575-583 (Pubitemid 26164589)
37. Fahrner, R. L., Dieckmann, T., Harwig, S. S., Lehrer, R. I., Eisenberg, D., and Feigon, J. (1996) Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes Chem. Biol. 3, 543-550 (Pubitemid 26324167)
38. Raetz, C. R. and Whitfield, C. (2002) Lipopolysaccharide Endotoxins Annu. Rev. Biochem. 71, 635-700 (Pubitemid 34800232)
39. 1H dipolar-assisted rotational resonance in magic-angle spinning NMR Chem. Phys. Lett. 344, 631-637 (Pubitemid 33628408)
40. Hohwy, M., Rienstra, C. M., Jaroniec, C. P., and Griffinb, R. G. (1999) Fivefold symmetric homonuclear dipolar recoupling in rotating solids: Application to double quantum spectroscopy J. Chem. Phys. 110, 7983-7992
41. Munowitz, M. G., Griffin, R. G., Bodenhausen, G., and Huang, T. H. (1981) Two-dimensional rotational spin-echo nuclear magnetic resonance in solids: Correlation of chemical shift and dipolar interactions J. Am. Chem. Soc. 103, 2529-2533
42. Hong, M., Gross, J. D., Rienstra, C. M., Griffin, R. G., Kumashiro, K. K., and Schmidt-Rohr, K. (1997) Coupling Amplification in 2D MAS NMR and Its Application to Torsion Angle Determination in Peptides J. Magn. Reson. 129, 85-92 (Pubitemid 127454056)
43. Rhim, W. K., Elleman, D. D., and Vaughan, R. W. (1973) Analysis of multiple pulse NMR in solids J. Chem. Phys. 59, 3740-3749
44. Tang, M., Waring, A. J., and Hong, M. (2009) Effects of arginine density on the membrane-bound structure of a cationic antimicrobial peptide from solid-state NMR Biochim. Biophys. Acta 1788, 514-521
45. Luo, W. and Hong, M. (2010) Conformational changes of an ion channel detected through water-protein interactions using solid-state NMR spectroscopy J. Am. Chem. Soc. 132, 2378-2384
46. Ader, C., Schneider, R., Seidel, K., Etzkorn, M., Becker, S., and Baldus, M. (2009) Structural rearrangements of membrane proteins probed by water-edited solid-state NMR spectroscopy J. Am. Chem. Soc. 131, 170-176
47. Hong, M. (2006) Solid-State NMR Studies of the Structure and Dynamics of Disordered and Membrane-Bound Peptides and Proteins Acc. Chem. Res. 39, 176-183
48. 1H Spin Diffusion from Lipids Using Solid-State NMR Spectroscopy J. Am. Chem. Soc. 124, 874-883 (Pubitemid 34112796)
49. Kumashiro, K. K., Schmidt-Rohr, K., Murphy, O. J., Ouellette, K. L., Cramer, W. A., and Thompson, L. K. (1998) A novel tool for probing membrane protein structure: Solid-state NMR with proton spin diffusion and X-nucleus detection J. Am. Chem. Soc. 120, 5043-5051 (Pubitemid 28281196)
50. Gullion, T. and Schaefer, J. (1989) Rotational-echo double-resonance NMR J. Magn. Reson. 81, 196-200
51. 15N-labeled peptides J. Am. Chem. Soc. 123, 3507-3519 (Pubitemid 32884585)
52. Bak, M., Rasmussen, T., and Nielsen, N. C. (2000) SIMPSON: A General Simulation Program for Solid-State NMR Spectroscopy J. Magn. Reson. 147, 296-330
53. Prenner, E. J., Lewis, R. N., Neuman, K. C., Gruner, S. M., Kondejewski, L. H., Hodges, R. S., and McElhaney, R. N. (1997) Nonlamellar phases induced by the interaction of gramicidin S with lipid bilayers. A possible relationship to membrane-disrupting activity Biochemistry 36, 7906-7916 (Pubitemid 27287204)
54. Fried, V. A. and Rothfield, L. I. (1978) Interactions between lipopolysaccharide and phosphatidylethanolamine in molecular monolayers Biochim. Biophys. Acta 514, 69-82 (Pubitemid 9061072)
55. 31P-NMR Spectroscopic and Microscopic Investigations Biophys. J. 95, 1226-1238
56. 31P nuclear magnetic resonance and the headgroup structure of phospholipids in membranes Biochim. Biophys. Acta 515, 105-140 (Pubitemid 8398025)
57. 31P solid-state NMR spectroscopy J. Am. Chem. Soc. 132, 9197-9205
58. Doherty, T., Waring, A. J., and Hong, M. (2006) Peptide-lipid interactions of the β-hairpin antimicrobial peptide tachyplesin and its linear derivatives from solid-state NMR Biochim. Biophys. Acta 1758, 1285-1291 (Pubitemid 44462775)
59. Yamaguchi, S., Huster, D., Waring, A., Lehrer, R. I., Tack, B. F., Kearney, W., and Hong, M. (2001) Orientation and Dynamics of an Antimicrobial Peptide in the Lipid Bilayer by Solid-State NMR Biophys. J. 81, 2203-2214 (Pubitemid 32917169)
60. Buffy, J. J., McCormick, M. J., Wi, S., Waring, A., Lehrer, R. I., and Hong, M. (2004) Solid-State NMR Investigation of the Selective Perturbation of Lipid Bilayers by the Cyclic Antimicrobial Peptide RTD-1 Biochemistry 43, 9800-9812 (Pubitemid 38993829)
61. Aisenbrey, C., Bertani, P., and Bechinger, B. (2010) Solid-state NMR investigations of membrane-associated antimicrobial peptides Methods Mol. Biol. 618, 209-233
62. Auger, M. (2009) Structural and Dynamics Studies of Lipids by Solid-State NMR. Encyclopedia of Magnetic Resonance, John Wiley & Sons, Inc., New York.
63. Brandenburg, K., Koch, M. H., and Seydel, U. (1990) Phase diagram of lipid A from Salmonella minnesota and Escherichia coli rough mutant lipopolysaccharide J. Struct. Biol. 105, 11-21
64. Nomura, K., Maeda, M., Sugase, K., and Kusumoto, S. Lipopolysaccharide induces raft domain expansion in membrane composed of a phospholipid- cholesterol-sphingomyelin ternary system. Innate Immun. 2010, not supplied.
65. Schromm, A. B., Brandenburg, K., Loppnow, H., Zähringer, U., Rietschel, E. T., Carroll, S. F., Koch, M. H., Kusumoto, S., and Seydel, U. (1998) The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity J. Immunol. 161, 5464-5471 (Pubitemid 28519109)
66. Urbán, E., Bóta, A., and Kocsis, B. (2006) Non-bilayer formation in the DPPE-DPPG vesicle system induced by deep rough mutant of Salmonella minnesota R595 lipopolysaccharide Colloids Surf., B 48, 106-111
67. Brandenburg, K., Koch, M. H., and Seydel, U. (1998) Biophysical characterisation of lysozyme binding to LPS Re and lipid A Eur. J. Biochem. 258, 686-695 (Pubitemid 28557934)
68. Seelig, J., MacDonald, P. M., and Scherer, P. G. (1987) Phospholipid head groups as sensors of electric charge in membranes Biochemistry 26, 7535-7541
69. deAzevedo, E. R., Saalwachter, K., Pascui, O., de Souza, A. A., Bonagamba, T. J., and Reichert, D. (2008) Intermediate motions as studied by solid-state separated local field NMR experiments J. Chem. Phys. 128, 104505
70. Jang, H., Ma, B., Lal, R., and Nussinov, R. (2008) 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, 4631-4642
71. Langham, A. A., Ahmad, A. S., and Kaznessis, Y. N. (2008) On the nature of antimicrobial activity: A model for protegrin-1 pores J. Am. Chem. Soc. 130, 4338-4346 (Pubitemid 351466429)
72. Zhang, Y., Lu, W., and Hong, M. (2010) The Membrane-Bound Structure and Topology of a Human α-Defensin Indicate a Dimer Pore Mechanism for Membrane Disruption Biochemistry 49, 9770-9782
73. 19F Solid-State NMR Biochemistry 48, 4587-4595
74. Su, Y., Mani, R., and Hong, M. (2008) Asymmetric insertion of membrane proteins in lipid bilayers by solid-state NMR paramagnetic relaxation enhancement: A cell-penetrating peptide example J. Am. Chem. Soc. 130, 8856-8864 (Pubitemid 351962521)
75. Su, Y., Waring, A. J., Ruchala, P., and Hong, M. (2010) Membrane-bound dynamic structure of an arginine-rich cell-penetrating peptide, the protein transduction domain of HIV TAT, from solid-state NMR Biochemistry 49, 6009-6020
76. Doherty, T., Su, Y., and Hong, M. (2010) High-resolution orientation and depth of insertion of the voltage-sensing S4 helix of a potassium channel in lipid bilayers J. Mol. Biol. 401, 642-652
77. Freites, J. A., Tobias, D. J., von Heijne, G., and White, S. H. (2005) Interface connections of a transmembrane voltage sensor Proc. Natl. Acad. Sci. U.S.A. 102, 15059-15064 (Pubitemid 41513334)
78. Li, S., Su, Y., Luo, W., and Hong, M. (2010) Water-protein interactions of an arginine-rich membrane peptide in lipid bilayers investigated by solid-state nuclear magnetic resonance spectroscopy J. Phys. Chem. B 114, 4063-4069
79. Raetz, C. R. (1978) Enzymology, Genetics, and Regulation of Membrane Phospholipid Synthesis in Escherichia coli Microbiol. Rev. 42, 614-659 (Pubitemid 9044056)