Long hydrophilic-and-cationic polymers: A different pathway toward preferential activity against bacterial over mammalian membranes

Biomacromolecules

Volumn 15, Issue 9, 2014, Pages 3267-3277

  Yang, Xin ^a   Hu, Kan ^a   Hu, Guantai ^a   Shi, Danyao ^a   Jiang, Yunjiang ^a,b   Hui, Liwei ^a   Zhu, Rui ^a   Xie, Yuntao ^a   Yang, Lihua ^a  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; HYDROPHILICITY; HYDROPHOBICITY; MAMMALS; MEMBRANES; TOXICITY;

ANTI-BACTERIAL ACTIVITY; ANTIMICROBIAL PEPTIDE; CATIONIC POLYMERS; HOST CELLS; HYDROPHOBIC MOIETIES; MAMMALIAN MEMBRANES; MEMBRANE ACTIVITY; TOXICITY REDUCTION;

POLYMERS;

ANTIINFECTIVE AGENT; COPOLYMER; METHACRYLIC ACID; POLYMER; POLYPEPTIDE ANTIBIOTIC AGENT; SYNTHETIC MIMICS OF ANTIMICROBIAL PEPTIDE; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; BIOMIMETIC MATERIAL; POLYMETHACRYLIC ACID; POLYMETHACRYLIC ACID DERIVATIVE;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HYDROPHOBICITY; MAMMAL CELL; MOLECULAR WEIGHT; NONHUMAN; ANIMAL; BACTERIUM; CHEMICAL PHENOMENA; CHEMISTRY; DRUG EFFECTS; ERYTHROCYTE MEMBRANE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MOUSE; SYNTHESIS;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; BIOMIMETIC MATERIALS; ERYTHROCYTE MEMBRANE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MICROBIAL VIABILITY; POLYMETHACRYLIC ACIDS;

EID: 84907558039     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm5006596     Document Type: Article

References (80)

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 (5887) 356-361
3. McKenna, M. Antibiotic resistance: The last resort Nature 2013, 499, 394-396
4. Zasloff, M. Antimicrobial Peptides of Multicellular Organisms Nature 2002, 415, 389-395
5. Hancock, R. E. W.; Lehrer, R. Cationic Peptides: A New Source of Antibiotics Trends Biotechnol. 1998, 16 (2) 82-88
6. Fjell, C. D.; Hiss, J. A.; Hancock, R. E. W.; Schneider, G. Designing antimicrobial peptides: Form follows function Nat. Rev. Drug. Discovery 2012, 11 (1) 37-51
7. Boman, H. G. Antibacterial peptides: Basic facts and emerging concepts J. Int. Med. 2003, 254 (3) 197-215
8. Hancock, R. E. W.; Sahl, H.-G. Antimicrobial and Host-Defense Peptides As New Anti-Infective Therapeutic Strategies Nat. Biotechnol. 2006, 24 (12) 1551-1557
9. Shai, Y. From Innate Immunity to de-Novo Designed Antimicrobial Peptides Curr. Pharm. Des. 2002, 8 (9) 715-725
10. Brogden, K. A. Antimicrobial Peptides: Pore Formers or Metabolic Inhibitors in Bacteria? Nat. Rev. Microbiol. 2005, 3 (3) 238-250
11. 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.; Selsted, M. E.; Wong, G. C. L. Criterion for Amino Acid Composition of Defensins and Antimicrobial Peptides Based on Geometry of Membrane Destabilization J. Am. Chem. Soc. 2011, 133 (17) 6720-6727
12. Wimley, W. C. Describing the Mechanism of Antimicrobial Peptide Action with the Interfacial Activity Model ACS Chem. Biol. 2010, 5 (10) 905-917
13. Yeaman, M. R.; Yount, N. Y. Mechanisms of Antimicrobial Peptide Action and Resistance Pharmacol. Rev. 2003, 55 (1) 27-55
14. 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
15. Oren, Z.; Shai, Y. Selective Lysis of Bacteria but Not Mammalian Cells by Diastereomers of Melittin: Structure-Function Study Biochemistry 1997, 36 (7) 1826-1835
16. Chen, Y.; Mant, C. T.; Farmer, S. W.; Hancock, R. E. W.; Vasil, M. L.; Hodges, R. S. Rational Design of a-Helical Antimicrobial Peptides with Enhanced Activities and Specificity/Therapeutic Index J. Biol. Chem. 2005, 280 (13) 12316-12329
17. Won, H.-S.; Jung, S.-J.; Kim, H. E.; Seo, M.-D.; Lee, B.-J. Systematic Peptide Engineering and Structural Characterization to Search for the Shortest Antimicrobial Peptide Analogue of Gaegurin 5 J. Biol. Chem. 2004, 279 (15) 14784-14791
18. Fernandez-Lopez, S.; Kim, H.-S.; Choi, E. C.; Delgado, M.; Granja, J. R.; Khasanov, A.; Kraehenbuehl, K.; Long, G.; Weinberger, D. A.; Wilcoxen, K. M.; Ghadiri, M. R. Antibacterial Agents Based on the Cyclic d, l -[α]-Peptide Architecture Nature 2001, 412 (6845) 452-455
19. Hamuro, Y.; Schneider, J. P.; DeGrado, W. F. De Novo Design of Antibacterial β-Peptides J. Am. Chem. Soc. 1999, 121 (51) 12200-12201
20. Porter, E. A.; Wang, X.; Lee, H.-S.; Weisblum, B.; Gellman, S. H. Antibiotics: Non-haemolytic β-Amino-Acid Oligomers Nature 2000, 404, 565-565
21. Liu, D.; DeGrado, W. F. De Novo Design, Synthesis, and Characterization of Antimicrobial β-Peptides J. Am. Chem. Soc. 2001, 123 (31) 7553-7559
22. Porter, E. A.; Weisblum, B.; Gellman, S. H. Mimicry of Host-Defense Peptides by Unnatural Oligomers: Antimicrobial β-Peptides J. Am. Chem. Soc. 2002, 124 (25) 7324-7330
23. Hayouka, Z.; Chakraborty, S.; Liu, R.; Boersma, M. D.; Weisblum, B.; Gellman, S. H. Interplay among Subunit Identity, Subunit Proportion, Chain Length, and Stereochemistry in the Activity Profile of Sequence-Random Peptide Mixtures J. Am. Chem. Soc. 2013, 135 (32) 11748-11751
24. Rapireddy, S.; Nhon, L.; Meehan, R. E.; Franks, J.; Stolz, D. B.; Tran, D.; Selsted, M. E.; Ly, D. H. RTD-1Mimic Containing γPNA Scaffold Exhibits Broad-Spectrum Antibacterial Activities J. Am. Chem. Soc. 2012, 134 (9) 4041-4044
25. Patch, J. A.; Barron, A. E. Helical Peptoid Mimics of Magainin-2 Amide J. Am. Chem. Soc. 2003, 125 (40) 12092-12093
26. Tew, G. N.; Liu, D.; Chen, B.; Doerksen, R. J.; Kaplan, J.; Carroll, P. J.; Klein, M. L.; DeGrado, W. F. De Novo Design of Biomimetic Antimicrobial Polymers Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (8) 5110-5114
27. Liu, D.; Choi, S.; Chen, B.; Doerksen, R. J.; Clements, D. J.; Winkler, J. D.; Klein, M. L.; DeGrado, W. F. Nontoxic Membrane-Active Antimicrobial Arylamide Oligomers Angew. Chem., Int. Ed. 2004, 43 (9) 1158-1162
28. Tew, G. N.; Clements, D.; Tang, H.; Arnt, L.; Scott, R. W. Antimicrobial Activity of an Abiotic Host Defense Peptide Mimic Biochim. Biophys. Acta, Biomembr. 2006, 1758 (9) 1387-1392
29. Choi, S.; Isaacs, A.; Clements, D.; Liu, D.; Kim, H.; Scott, R. W.; Winkler, J. D.; DeGrado, W. F. De Novo Design and in Vivo Activity of Conformationally Restrained Antimicrobial Arylamide Foldamers Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (17) 6968-6973
30. Radzishevsky, I. S.; Rotem, S.; Bourdetsky, D.; Navon-Venezia, S.; Carmeli, Y.; Mor, A. Improved Antimicrobial Peptides Based on Acyl-Lysine Oligomers Nat. Biotechnol. 2007, 25 (6) 657-659
31. Thaker, H. D.; Cankaya, A.; Scott, R. W.; Tew, G. N. Role of Amphiphilicity in the Design of Synthetic Mimics of Antimicrobial Peptides with Gram-Negative Activity ACS Med. Chem. Lett. 2013, 4 (5) 481-485
32. 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 (40) 12141-12147
33. Arnt, L.; Nüsslein, K.; Tew, G. N. Nonhemolytic Abiogenic Polymers as Antimicrobial Peptide Mimics J. Polym. Sci. A, Polym. Chem. 2004, 42 (15) 3860-3864
34. Kuroda, K.; DeGrado, W. F. Amphiphilic Polymethacrylate Derivatives as Antimicrobial Agents J. Am. Chem. Soc. 2005, 127 (12) 4128-4129
35. Palermo, E. F.; Sovadinova, I.; Kuroda, K. Structural Determinants of Antimicrobial Activity and Biocompatibility in Membrane-Disrupting Methacrylamide Random Copolymers Biomacromolecules 2009, 10 (11) 3098-3107
36. Lienkamp, K.; Madkour, A. E.; Musante, A.; Nelson, C. F.; Nüsslein, K.; Tew, G. N. Antimicrobial Polymers Prepared by ROMP with Unprecedented Selectivity: A Molecular Construction Kit Approach J. Am. Chem. Soc. 2008, 130 (30) 9836-9843
37. Ilker, M. F.; Nüsslein, K.; Tew, G. N.; Coughlin, E. B. Tuning the Hemolytic and Antibacterial Activities of Amphiphilic Polynorbornene Derivatives J. Am. Chem. Soc. 2004, 126 (48) 15870-15875
38. Mowery, B. P.; Lee, S. E.; Kissounko, D. A.; Epand, R. F.; Epand, R. M.; Weisblum, B.; Stahl, S. S.; Gellman, S. H. Mimicry of Antimicrobial Host-Defense Peptides by Random Copolymers J. Am. Chem. Soc. 2007, 129 (50) 15474-15476
39. Mowery, B. P.; Lindner, A. H.; Weisblum, B.; Stahl, S. S.; Gellman, S. H. Structure-Activity Relationships among Random Nylon-3 Copolymers That Mimic Antibacterial Host-Defense Peptides J. Am. Chem. Soc. 2009, 131 (28) 9735-9745
40. Sambhy, V.; Peterson, B. R.; Sen, A. Antibacterial and Hemolytic Activities of Pyridinium Polymers as a Function of the Spatial Relationship between the Positive Charge and the Pendant Alkyl Tail Angew. Chem., Int. Ed. 2008, 47 (7) 1250-1254
41. Oda, Y.; Kanaoka, S.; Sato, T.; Aoshima, S.; Kuroda, K. Block versus Random Amphiphilic Copolymers as Antibacterial Agents Biomacromolecules 2011, 12 (10) 3581-3591
42. Qiao, Y.; Yang, C.; Coady, D. J.; Ong, Z. Y.; Hedrick, J. L.; Yang, Y.-Y. Highly Dynamic Biodegradable Micelles Capable of Lysing Gram-Positive and Gram-Negative Bacterial Membrane Biomaterials 2012, 33 (4) 1146-1153
43. Jiang, Y.; Yang, X.; Zhu, R.; Hu, K.; Lan, W.-W.; Wu, F.; Yang, L. Acid-Activated Antimicrobial Random Copolymers: A Mechanism-Guided Design of Antimicrobial Peptide Mimics Macromolecules 2013, 46 (10) 3959-3964
44. Lienkamp, K.; Kumar, K.-N.; Som, A.; Nüsslein, K.; Tew, G. N. "Doubly Selective" Antimicrobial Polymers: How Do They Differentiate between Bacteria? Chem.-Eur. J. 2009, 15 (43) 11710-11714
45. Kuroda, K.; Caputo, G. A.; DeGrado, W. F. The Role of Hydrophobicity in the Antimicrobial and Hemolytic Activities of Polymethacrylate Derivatives Chem.-Eur. J. 2009, 15 (5) 1123-1133
46. Chen, Y.; Guarnieri, M. T.; Vasil, A. I.; Vasil, M. L.; Mant, C. T.; Hodges, R. S. Role of Peptide Hydrophobicity in the Mechanism of Action of α-Helical Antimicrobial Peptides Antimicrob. Agents Chemother. 2007, 51 (4) 1398-1406
47. Sgolastra, F.; deRonde, B. M.; Sarapas, J. M.; Som, A.; Tew, G. N. Designing Mimics of Membrane Active Proteins Acc. Chem. Res. 2013, 46 (12) 2977-2987
48. Thaker, H. D.; Cankaya, A.; Scott, R. W.; Tew, G. N. Role of Amphiphilicity in the Design of Synthetic Mimics of Antimicrobial Peptides with Gram-Negative Activity ACS Med. Chem. Lett. 2013, 4 (5) 481-485
49. Porter, E. A.; Weisblum, B.; Gellman, S. H. Mimicry of Host-Defense Peptides by Unnatural Oligomers: Antimicrobial β-Peptides J. Am. Chem. Soc. 2002, 124 (25) 7324-7330
50. Wieprecht, T.; Dathe, M.; Krause, E.; Beyermann, M.; Maloy, W. L.; MacDonald, D. L.; Bienert, M. Modulation of Membrane Activity of Amphipathic, Antibacterial Peptides by Slight Modifications of the Hydrophobic Moment FEBS Lett. 1997, 417 (1) 135-140
51. Fernández-Vidal, M.; Jayasinghe, S.; Ladokhin, A. S.; White, S. H. Folding Amphipathic Helices Into Membranes: Amphiphilicity Trumps Hydrophobicity J. Mol. Biol. 2007, 370 (3) 459-470
52. 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 (5) 1908-1915
53. Kondejewski, L. H.; Jelokhani-Niaraki, M.; Farmer, S. W.; Lix, B.; Kay, C. M.; Sykes, B. D.; Hancock, R. E. W.; Hodges, R. S. Dissociation of Antimicrobial and Hemolytic Activities in Cyclic Peptide Diastereomers by Systematic Alterations in Amphipathicity J. Biol. Chem. 1999, 274 (19) 13181-13192
54. Colville, K.; Tompkins, N.; Rutenberg, A. D.; Jericho, M. H. Effects of Poly(l -lysine) Substrates on Attached Escherichia coli Bacteria Langmuir 2009, 26 (4) 2639-2644
55. Yoshida, T.; Nagasawa, T. ε-Poly- l -lysine: Microbial Production, Biodegradation and Application Potential Appl. Microbiol. Biotechnol. 2003, 62 (1) 21-26
56. Gabriel, G. J.; Madkour, A. E.; Dabkowski, J. M.; Nelson, C. F.; Nüsslein, K.; Tew, G. N. Synthetic Mimic of Antimicrobial Peptide with Nonmembrane-Disrupting Antibacterial Properties Biomacromolecules 2008, 9 (11) 2980-2983
57. Tossi, A.; Sandri, L.; Giangaspero, A. Amphipathic, α-Helical Antimicrobial Peptides Pept. Sci. 2000, 55 (1) 4-30
58. http://aps.unmc.edu/AP/main.php.
59. Schmidt, N. W.; Lis, M.; Zhao, K.; Lai, G. H.; Alexandrova, A. N.; Tew, G. N.; Wong, G. C. L. Molecular Basis for Nanoscopic Membrane Curvature Generation from Quantum Mechanical Models and Synthetic Transporter Sequences J. Am. Chem. Soc. 2012, 134 (46) 19207-19216
60. Mishra, A.; Lai, G. H.; Schmidt, N. W.; Sun, V. Z.; Rodriguez, A. R.; Tong, R.; Tang, L.; Cheng, J.; Deming, T. J.; Kamei, D. T.; Wong, G. C. L. Translocation of HIV TAT Peptide and Analogues Induced by Multiplexed Membrane and Cytoskeletal Interactions Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (41) 16883-16888
61. Kyte, J.; Doolittle, R. F. A simple Method for Displaying the Hydropathic Character of a Protein J. Mol. Biol. 1982, 157 (1) 105-132
62. Eisenberg, D.; Weiss, R. M.; Terwilliger, T. C.; Wilcox, W. Hydrophobic Moments and Protein Structure Faraday Symp. Chem. Soc. 1982, 17 (0) 109-120
63. Hessa, T.; Kim, H.; Bihlmaier, K.; Lundin, C.; Boekel, J.; Andersson, H.; Nilsson, I.; White, S. H.; von Heijne, G. Recognition of Transmembrane Helices by the Endoplasmic Reticulum Translocon Nature 2005, 433 (7024) 377-381
64. Fujisawa, S.; Masuhara, E. Determination of Partition Coefficients of Acrylates, Methacrylates, and Vinyl Monomers Using High Performance Liquid Chromatography (HPLC) J. Biomed. Mater. Res. 1981, 15 (6) 787-793
65. Kim, A.; Szoka, F., Jr. Amino Acid Side-Chain Contributions to Free Energy of Transfer of Tripeptides from Water to Octanol Pharm. Res. 1992, 9 (4) 504-514
66. Ananthapadmanabhan, K. P.; Goddard, E. D.; Turro, N. J.; Kuo, P. L. Fluorescence Probes for Critical Micelle Concentration Determination Langmuir 1985, 1 (3) 352-355
67. Eisenberg, D.; Weiss, R. M.; Terwilliger, T. C.; Wilcox, W. Hydrophobic Moments and Protein Structure Faraday Symp. Chem. Soc. 1982, 17 (0) 109-120
68. Ludtke, S. J.; He, K.; Heller, W. T.; Harroun, T. A.; Yang, L.; Huang, H. W. Membrane Pores Induced by Magainin Biochemistry 1996, 35 (43) 13723-13728
69. Matsuzaki, K.; Murase, O.; Fujii, N.; Miyajima, K. An Antimicrobial Peptide, Magainin 2, Induced Rapid Flip-Flop of Phospholipids Coupled with Pore Formation and Peptide Translocation Biochemistry 1996, 35 (35) 11361-11368
70. Matsuzaki, K.; Murase, O.; Fujii, N.; Miyajima, K. Translocation of a Channel-Forming Antimicrobial Peptide, Magainin 2, across Lipid Bilayers by Forming a Pore Biochemistry 1995, 34 (19) 6521-6526
71. Matsuzaki, K.; Sugishita, K.-i.; Harada, M.; Fujii, N.; Miyajima, K. Interactions of an Antimicrobial Peptide, Magainin 2, with Outer and Inner Membranes of Gram-Negative Bacteria Biochim. Biophys. Acta, Biomembr. 1997, 1327 (1) 119-130
72. Matsuzaki, K.; Sugishita, K.-i.; 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 (34) 11856-11863
73. Zasloff, M.; 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. U.S.A. 1987, 84 (15) 5449-5453
74. Rathinakumar, R.; Walkenhorst, W. F.; Wimley, W. C. Broad-Spectrum Antimicrobial Peptides by Rational Combinatorial Design and High-Throughput Screening: The Importance of Interfacial Activity J. Am. Chem. Soc. 2009, 131 (22) 7609-7617
75. Fujisawa, S.; Masuhara, E. Determination of Partition Coefficients of Acrylates, Methacrylates, and Vinyl Monomers Using High Performance Liquid Chromatography (HPLC) J. Biomed. Mater. Res. 1981, 15 (6) 787-793
76. 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 (15) 2041-2061
77. Darveau, R. P.; Cunningham, M. D.; Seachord, C. L.; Cassiano-Clough, L.; Cosand, W. L.; Blake, J.; Watkins, C. S. Beta-Lactam Antibiotics Potentiate Magainin 2 Antimicrobial Activity in Vitro and in Vivo Antimicrob. Agents Chemother. 1991, 35 (6) 1153-1159
78. Hancock, R. E. W. Alterations in Outer Membrane Permeability Annu. Rev. Microbiol. 1984, 38 (1) 237-264
79. Klibanov, A. M. Permanently Microbicidal Materials Coatings J. Mater. Chem. 2007, 17 (24) 2479-2482
80. Raghuraman, H.; Chattopadhyay, A. Orientation and Dynamics of Melittin in Membranes of Varying Composition Utilizing NBD Fluorescence Biophys. J. 2007, 92 (4) 1271-1283