Small-Anion Selective Transmembrane "holes" Induced by an Antimicrobial Peptide Too Short to Span Membranes

Journal of Physical Chemistry B

Volumn 119, Issue 27, 2015, Pages 8553-8560

  Hu, Kan ^a   Jiang, Yunjiang ^a,d   Xie, Yuntao ^a   Liu, Hui ^a   Liu, Rui ^c   Zhao, Zhi ^b   Lai, Ren ^c   Yang, Lihua ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c KUNMING INSTITUTE OF ZOOLOGY   (China)

^d Department of Geology and Geological Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; IONS; MICROORGANISMS; NEGATIVE IONS; PEPTIDES; POLYPEPTIDES;

ANTI-BACTERIAL ACTIVITY; ANTIMICROBIAL PEPTIDE; GRAM-NEGATIVE BACTERIA; INTRINSIC CURVATURE; MEMBRANE DESTABILIZATION; PHARMACEUTICAL DEVELOPMENT; TRANSMEMBRANE CHANNELS; TRANSMEMBRANE TRANSPORT;

MEMBRANES;

1,2-DIOLEOYL-SN-GLYCERO-3-PHOSPHOGLYCEROL; ANION; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; DIOLEOYL PHOSPHATIDYLETHANOLAMINE; ION CHANNEL; LIPOSOME; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL;

BIOLOGICAL MODEL; CELL MEMBRANE; CHEMISTRY; DIMERIZATION; DRUG EFFECTS; ESCHERICHIA COLI; HEMOLYSIS; ION TRANSPORT; METABOLISM; STAPHYLOCOCCUS AUREUS;

ANIONS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; DIMERIZATION; ESCHERICHIA COLI; HEMOLYSIS; ION CHANNELS; ION TRANSPORT; MODELS, BIOLOGICAL; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; STAPHYLOCOCCUS AUREUS; UNILAMELLAR LIPOSOMES;

EID: 84937010336     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b03133     Document Type: Article

References (68)

1. Tomasz, A. Multiple-Antibiotic-Resistant Pathogenic Bacteria - A Report on the Rockefeller University Workshop N. Engl. J. Med. 1994, 330, 1247-1251
2. Taubes, G. The Bacteria Fight Back Science 2008, 321, 356-361
3. Bush, K.; Courvalin, P.; Dantas, G.; Davies, J.; Eisenstein, B.; Huovinen, P.; Jacoby, G. A.; Kishony, R.; Kreiswirth, B. N.; Kutter, E.; et al. Tackling Antibiotic Resistance Nat. Rev. Microbiol. 2011, 9, 894-896
4. Walsh, C. T.; Wencewicz, T. A. Prospects for New Antibiotics: A Molecule-Centered Perspective J. Antibiot. 2014, 67, 7-22
5. Lewis, K. Antibiotics: Recover the Lost Art of Drug Discovery Nature 2012, 485, 439-440
6. Boman, H. G. Innate Immunity and the Normal Microflora Immunol. Rev. 2000, 173, 5-16
7. Zasloff, M. Antimicrobial Peptides of Multicellular Organisms Nature 2002, 415, 389-395
8. Lehrer, R. I. Primate Defensins Nat. Rev. Microbiol. 2004, 2, 727-738
9. Hancock, R. E. W.; Sahl, H. G. Antimicrobial and Host-Defense Peptides as New Anti-Infective Therapeutic Strategies Nat. Biotechnol. 2006, 24, 1551-1557
10. Fjell, C. D.; Hiss, J. A.; Hancock, R. E. W.; Schneider, G. Designing Antimicrobial Peptides: Form Follows Function Nat. Rev. Drug. Discovery 2012, 11, 37-51
11. Shai, Y. From Innate Immunity to De-Novo Designed Antimicrobial Peptides Curr. Pharm. Des. 2002, 8, 715-725
12. Peschel, A.; Sahl, H. G. The Co-Evolution of Host Cationic Antimicrobial Peptides and Microbial Resistance Nat. Rev. Microbiol. 2006, 4, 529-536
13. Brogden, K. A. Antimicrobial Peptides: Pore Formers or Metabolic Inhibitors in Bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250
14. Selsted, M. E.; Ouellette, A. J. Mammalian Defensins in the Antimicrobial Immune Response Nat. Immunol. 2005, 6, 551-557
15. Ganz, T. Defensins: Antimicrobial Peptides of Innate Immunity Nat. Rev. Immunol. 2003, 3, 710-720
16. Hancock, R. E. W.; Lehrer, R. Cationic Peptides: A New Source of Antibiotics Trends Biotechnol. 1998, 16, 82-88
17. Boman, H. G. Antibacterial Peptides: Basic Facts and Emerging Concepts J. Int. Med. 2003, 254, 197-215
18. Wimley, W. C. Describing the Mechanism of Antimicrobial Peptide Action with the Interfacial Activity Model ACS Chem. Biol. 2010, 5, 905-917
19. Yeaman, M. R.; Yount, N. Y. Mechanisms of Antimicrobial Peptide Action and Resistance Pharmacol. Rev. 2003, 55, 27-55
20. Matsuzaki, K. Why and How Are Peptide-Lipid Interactions Utilized for Self-Defense? Magainins and Tachyplesins as Archetypes Biochim. Biophys. Acta, Biomembr. 1999, 1462, 1-10
21. Yu, Y.; Vroman, J. A.; Bae, S. C.; Granick, S. Vesicle Budding Induced by a Pore-Forming Peptide J. Am. Chem. Soc. 2010, 132, 195-201
22. Shai, Y. Mechanism of the Binding, Insertion and Destabilization of Phospholipid Bilayer Membranes by A-Helical Antimicrobial and Cell Non-Selective Membrane-Lytic Peptides Biochim. Biophys. Acta, Biomembr. 1999, 1462, 55-70
23. Fuertes, G.; Giménez, D.; Esteban-Martín, S.; Sánchez-Muñoz, O.; Salgado, J. A Lipocentric View of Peptide-Induced Pores Eur. Biophys. J. 2011, 40, 399-415
24. Rapaport, D.; Shai, Y. Interaction of Fluorescently Labeled Pardaxin and Its Analogues with Lipid Bilayers J. Biol. Chem. 1991, 266, 23769-23775
25. Rapaport, D.; Shai, Y. Aggregation and Organization of Pardaxin in Phospholipid Membranes. A Fluorescence Energy Transfer Study J. Biol. Chem. 1992, 267, 6502-6509
26. Ludtke, S. J.; He, K.; Heller, W. T.; Harroun, T. A.; Yang, L.; Huang, H. W. Membrane Pores Induced by Magainin Biochemistry 1996, 35, 13723-13728
27. Lee, M. T.; Sun, T. L.; Hung, W. C.; Huang, H. W. Process of Inducing Pores in Membranes by Melittin Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 14243-14248
28. Matsuzaki, K.; Sugishita, K.; Ishibe, N.; Ueha, M.; Nakata, S.; Miyajima, K.; Epand, R. M. Relationship of Membrane Curvature to the Formation of Pores by Magainin 2 Biochemistry 1998, 37, 11856-11863
29. Zemel, A.; Fattal, D. R.; Ben-Shaul, A. Energetics and Self-Assembly of Amphipathic Peptide Pores in Lipid Membranes Biophys. J. 2003, 84, 2242-2255
30. Wu, M. H.; Maier, E.; Benz, R.; Hancock, R. E. W. Mechanism of Interaction of Different Classes of Cationic Antimicrobial Peptides with Planar Bilayers and with the Cytoplasmic Membrane of Escherichia Coli Biochemistry 1999, 38, 7235-7242
31. Bechinger, B. The Structure, Dynamics and Orientation of Antimicrobial Peptides in Membranes by Multidimensional Solid-State NMR Spectroscopy Biochim. Biophys. Acta, Biomembr. 1999, 1462, 157-183
32. Schmidt, N. W.; Mishra, A.; Lai, G. H.; Davis, M.; Sanders, L. K.; Tran, D.; Garcia, A.; Tai, K. P.; McCray, P. B.; Ouellette, A. J.; et al. Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization J. Am. Chem. Soc. 2011, 133, 6720-6727
33. Schmidt, N. W.; Tai, K. P.; Kamdar, K.; Mishra, A.; Lai, G. H.; Zhao, K.; Ouellette, A. J.; Wong, G. C. L. Arginine in A-Defensins: Differential Effects on Bactericidal Activity Correspond to Geometry of Membrane Curvature Generation and Peptide-Lipid Phase Behavior J. Biol. Chem. 2012, 287, 21866-21872
34. Hu, K.; Schmidt, N. W.; Zhu, R.; Jiang, Y.; Lai, G. H.; Wei, G.; Palermo, E. F.; Kuroda, K.; Wong, G. C. L.; Yang, L. A Critical Evaluation of Random Copolymer Mimesis of Homogeneous Antimicrobial Peptides Macromolecules 2013, 46, 1908-1915
35. Lee, M. W.; Chakraborty, S.; Schmidt, N. W.; Murgai, R.; Gellman, S. H.; Wong, G. C. L. Two Interdependent Mechanisms of Antimicrobial Activity Allow for Efficient Killing in Nylon-3-Based Polymeric Mimics of Innate Immunity Peptides Biochim. Biophys. Acta, Biomembr. 2014, 1838, 2269-2279
36. Kelkar, D. A.; Chattopadhyay, A. The Gramicidin Ion Channel: A Model Membrane Protein Biochim. Biophys. Acta, Biomembr. 2007, 1768, 2011-2025
37. Siu, S. W. I.; Böckmann, R. A. Low Free Energy Barrier for Ion Permeation through Double-Helical Gramicidin J. Phys. Chem. B 2009, 113, 3195-3202
38. Mishra, B.; Epand, R. F.; Epand, R. M.; Wang, G. Structural Location Determines Functional Roles of the Basic Amino Acids of KR-12, the Smallest Antimicrobial Peptide from Human Cathelicidin Ll-37 RSC Adv. 2013, 3, 19560-19571
39. Yang, L.; Gordon, V. D.; Mishra, A.; Som, A.; Purdy, K. R.; Davis, M. A.; Tew, G. N.; Wong, G. C. L. Synthetic Antimicrobial Oligomers Induce a Composition-Dependent Topological Transition in Membranes J. Am. Chem. Soc. 2007, 129, 12141-12147
40. Yang, L.; Gordon, V. D.; Trinkle, D. R.; Schmidt, N. W.; Davis, M. A.; DeVries, C.; Som, A.; Cronan, J. E., Jr.; Tew, G. N.; Wong, G. C. L. Mechanism of a Prototypical Synthetic Membrane-Active Antimicrobial: Efficient Hole-Punching Via Interaction with Negative Intrinsic Curvature Lipids Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 20595-20600
41. Som, A.; Yang, L.; Wong, G. C. L.; Tew, G. N. Divalent Metal Ion Triggered Membrane Activity in Cardiolipin Vesicles by Antimicrobial Molecule J. Am. Chem. Soc. 2009, 131, 15102-15103
42. Som, A.; Tew, G. N. Influence of Lipid Composition on Membrane Activity of Antimicrobial Phenylene Ethynylene Oligomers J. Phys. Chem. B 2008, 112, 3495-3502
43. Li, J.; Zhang, C.; Xu, X.; Wang, J.; Yu, H.; Lai, R.; Gong, W. Trypsin Inhibitory Loop Is an Excellent Lead Structure to Design Serine Protease Inhibitors and Antimicrobial Peptides FASEB J. 2007, 21, 2466-2473
44. Needhamf, D.; Evans, E. Structure and Mechanical Properties of Giant Lipid (Dmpc) Vesicle Bilayers from 20.degree.C Below to 10.degree.C above the Liquid Crystal-Crystalline Phase Transition at 24 C Biochemistry 1988, 27, 8261-8269
45. Harper, P. E.; Gruner, S. M.; Lewis, R. N. A. H.; McElhaney, R. N. Electron Density Modeling and Reconstruction of Infinite Periodic Minimal Surfaces (IPMS) Based Phases in Lipid-Water Systems. Ii. Reconstruction of D Surface Based Phases Eur. Phys. J. E 2000, 2, 229-245
46. Imperor-Clerc, M.; Davidson, P.; Davidson, A. Existence of a Microporous Corona around the Mesopores of Silica-Based SBA-15 Materials Templated by Triblock Copolymers J. Am. Chem. Soc. 2000, 122, 11925-11933
47. Turner, D. C.; Gruner, S. M. X-Ray Diffraction Reconstruction of the Inverted Hexagonal (HII) Phase in Lipid-Water Systems Biochemistry 1992, 31, 1340-1355
48. Davis, J. T.; Okunola, O.; Quesada, R. Recent Advances in the Transmembrane Transport of Anions Chem. Soc. Rev. 2010, 39, 3843-62
49. Maskiewicz, R.; Sogah, D.; Bruice, T. C. Chemiluminescent Reactions of Lucigenin.1.Reactions of Lucigenin with Hydrogen Peroxide J. Am. Chem. Soc. 1978, 101, 5347-5354
50. Chen, Y. A Mechanism for Tamoxifen-Mediated Inhibition of Acidification J. Biol. Chem. 1999, 274, 18364-18373
51. Harrell, Jr.; William, A.; Bergmeyer, M. L.; Zavalij, P. Y.; Davis, J. T. Ceraminde-Mediated Transport of Chloride and Bicarbonate across Phospholipid Membranes Chem. Commun. 2010, 46, 3950-3952
52. Wei, G.; Liu, X.; Yuan, L.; Ju, X. J.; Chu, L. Y.; Yang, L. Lipid Composition Influences the Membrane-Disrupting Activity of Antimicrobial Methacrylate Co-Polymers J. Biomater. Sci., Polym. Ed. 2011, 22, 2041-2061
53. Niesman, M. R.; Khoobehi, B.; Peyman, G. A. Encapsulation of Sodium Fluorescein for Dye Release Studies Invest. Ophthalmol. Vis. Sci. 1992, 33, 2113-2119
54. Chin, W.; Yang, C.; Ng, V. W. L.; Huang, Y.; Cheng, J.; Tong, Y. W.; Coady, D. J.; Fan, W.; Hedrick, J. L.; Yang, Y. Y. Biodegradable Broad-Spectrum Antimicrobial Polycarbonates: Investigating the Role of Chemical Structure on Activity and Selectivity Macromolecules 2013, 46, 8797-8807
55. Epand, R. F.; Mowery, B. P.; Lee, S. E.; Stahl, S. S.; Lehrer, R. I.; Gellman, S. H.; Epand, R. M. Dual Mechanism of Bacterial Lethality for a Cationic Sequence-Random Copolymer That Mimics Host-Defense Antimicrobial Peptides J. Mol. Biol. 2008, 379, 38-50
56. Ferdani, R.; Li, R.; Pajewski, R.; Pajewska, J.; Winter, R. K.; Gokel, G. W. Transport of Chloride and Carboxyfluorescein through Phospholipid Vesicle Membranes by Heptapeptide Amphiphiles Org. Biomol. Chem. 2007, 5, 2423-32
57. Mukherjee, S.; Zheng, H.; Derebe, M. G.; Callenberg, K. M.; Partch, C. L.; Rollins, D.; Propheter, D. C.; Rizo, J.; Grabe, M.; Jiang, Q. X. Antibacterial Membrane Attack by a Pore-Forming Intestinal C-Type Lectin Nature 2014, 505, 103-7
58. Volkov, A. G.; Paula, S.; Deamer, D. W. Two Mechanisms of Permeation of Small Neutral Molecules and Hydrated Ions across Phospholipid Bilayers Bioelectrochem. Bioenerg. 1997, 42, 153-160
59. Stella, L.; Mazzuca, C.; Venanzi, M.; Palleschi, A.; Didone, M.; Formaggio, F.; Toniolo, C.; Pispisa, B. Aggregation and Water-Membrane Partition as Major Determinants of the Activity of the Antibiotic Peptide Trichogin Ga Iv Biophys. J. 2004, 86, 936-945
60. Holme, M. N.; Fedotenko, I. A.; Abegg, D.; Althaus, J.; Babel, L.; Favarger, F.; Reiter, R.; Tanasescu, R.; Zaffalon, P. L.; Ziegler, A.; et al. Shear-Stress Sensitive Lenticular Vesicles for Targeted Drug Delivery Nat. Nanotechnol. 2012, 7, 536-543
61. Rossignol, M.; Thomas, P.; Grignon, C. Proton Permeability of Liposomes from Natural Phospholipid Mixtures Biochim. Biophys. Acta, Biomembr. 1982, 684, 195-199
62. Seganish, J. L.; Davis, J. T. Prodigiosin Is a Chloride Carrier That Can Function as an Anion Exchanger Chem. Commun. 2005, 5781-5783
63. Santacroce, P. V.; Okunola, O. A.; Zavalij, P. Y.; Davis, J. T. A Transmembrane Anion Transporter Selective for Nitrate over Chloride Chem. Commun. 2006, 3246-3248
64. Han, J.; Burgess, K. Fluorescent Indicators for Intracellular pH Chem. Rev. 2009, 110, 2709-2728
65. Dunford, R.; Salinaro, A.; Cai, L.; Serpone, N.; Horikoshi, S.; Hidaka, H.; Knowland, J. Chemical Oxidation and DNA Damage Catalysed by Inorganic Sunscreen Ingredients FEBS Lett. 1997, 418, 87-90
66. Pandey, R. C.; Cook, J. C.; Rinehart, K. L. High Resolution and Field Desorption Mass Spectrometry Studies and Revised Structures of Alamethicins I and II J. Am. Chem. Soc. 1977, 99, 8469-8483
67. He, K.; Ludtke, S. J.; Worcester, D. L.; Huang, H. W. Neutron Scattering in the Plane of Membranes: Structure of Alamethicin Pores Biophys. J. 1996, 70, 2659-2666
68. Lai, R.; Zheng, Y. T.; Shen, J. H.; Liu, G. J.; Liu, H.; Lee, W. H.; Tang, S. Z.; Zhang, Y. Antimicrobial Peptides from Skin Secretions of Chinese Red Belly Toad Bombina Maxima Peptides 2002, 23, 427-435