Designing mimics of membrane active proteins

Accounts of Chemical Research

Volumn 46, Issue 12, 2013, Pages 2977-2987

  Sgolastra, Federica ^a   Deronde, Brittany M ^a   Sarapas, Joel M ^a   Som, Abhigyan ^a   Tew, Gregory N ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; MEMBRANE PROTEIN;

ARTICLE; BIOMIMETICS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DESIGN; SYNTHESIS;

ANTIMICROBIAL CATIONIC PEPTIDES; BIOMIMETICS; DRUG DESIGN; MEMBRANE PROTEINS; MOLECULAR STRUCTURE;

EID: 84890624112     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400066v     Document Type: Article

References (68)

1. Zasloff, M. Antimicrobial peptides of multicellular organisms Nature 2002, 415, 389-395 (Pubitemid 34100944)
2. Wender, P. A.; Cooley, C. B.; Geihe, E. I. Beyond Cell Penetrating Peptides: Designed Molecular Transporters Drug Discovery Today: Technol. 2012, 9, e49-e55
3. Takeshima, K.; Chikushi, A.; Lee, K. K.; Yonehara, S.; Matsuzaki, K. Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes J. Biol. Chem. 2003, 278, 1310-1315 (Pubitemid 36790815)
4. Henriques, S. T.; Melo, M. N.; Castanho, M. A. R. B. Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem. J. 2006, 399, 1-7 (Pubitemid 44505401)
5. 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, 6720-6727
6. Brogden, K. A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 2005, 3, 238-250 (Pubitemid 40298223)
7. Yeaman, M. R.; Yount, N. Y. Mechanisms of antimicrobial peptide action and resistance Pharmacol. Rev. 2003, 55, 27-55 (Pubitemid 36268398)
8. Yang, L. H.; Gordon, V. D.; Trinkle, D. R.; Schmidt, N. W.; Davis, M. A.; DeVries, C.; Som, A.; Cronan, J. E.; 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
9. Gabriel, G. J.; Som, A.; Madkour, A. E.; Eren, T.; Tew, G. N. Infectious disease: Connecting innate immunity to biocidal polymers Mater. Sci. Eng., R 2007, 57, 28-64 (Pubitemid 47042367)
10. Som, A.; Vemparala, S.; Ivanov, I.; Tew, G. N. Synthetic mimics of antimicrobial peptides Biopolymers 2008, 90, 83-93
11. Lienkamp, K.; Tew, G. N. Synthetic Mimics of Antimicrobial Peptides-A Versatile Ring-Opening Metathesis Polymerization Based Platform for the Synthesis of Selective Antibacterial and Cell-Penetrating Polymers Chem.-Eur. J. 2009, 15, 11784-11800
12. Hamuro, Y.; Schneider, J. P.; DeGrado, W. F. De novo design of antibacterial beta-peptides J. Am. Chem. Soc. 1999, 121, 12200-12201
13. Porter, E. A.; Weisblum, B.; Gellman, S. H. Mimicry of host-defense peptides by unnatural oligomers: Antimicrobial beta-peptides J. Am. Chem. Soc. 2002, 124, 7324-7330 (Pubitemid 34670441)
14. Seebach, D.; Beck, A. K.; Bierbaum, D. J. The world of beta- and gamma-peptides comprised of homologated proteinogenic amino acids and other components Chem. Biodivers. 2004, 1, 1111-1239
15. Tew, G. N.; Liu, D. H.; 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, 5110-5114 (Pubitemid 34411511)
16. Arnt, L.; Tew, G. N. New poly(phenyleneethynylene)s with cationic, facially amphiphilic structures J. Am. Chem. Soc. 2002, 124, 7664-7665 (Pubitemid 34733772)
17. Arnt, L.; Nusslein, K.; Tew, G. N. Nonhemolytic abiogenic polymers as antimicrobial peptide mimics J. Polym. Sci., Polym. Chem. 2004, 42, 3860-3864
18. Ishitsuka, Y.; Arnt, L.; Majewski, J.; Frey, S.; Ratajczek, M.; Kjaer, K.; Tew, G. N.; Lee, K. Y. C. Amphiphilic poly(phenyleneethynylene)s can mimic antimicrobial peptide membrane disordering effect by membrane insertion J. Am. Chem. Soc. 2006, 128, 13123-13129 (Pubitemid 44527682)
19. 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
20. Yang, L. H.; Gordon, V. D.; Mishra, A.; Sorn, 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 (Pubitemid 47556850)
21. Som, A.; Yang, L. H.; Wong, G. C. L.; Tew, G. N. Divalent Metal Ion Triggered Activity of a Synthetic Antimicrobial in Cardiolipin Membranes J. Am. Chem. Soc. 2009, 131, 15102-+
22. Chen, J. M.; Hessler, J. A.; Putchakayala, K.; Panama, B. K.; Khan, D. P.; Hong, S.; Mullen, D. G.; DiMaggio, S. C.; Som, A.; Tew, G. N.; Lopatin, A. N.; Baker, J. R.; Holl, M. M. B.; Orr, B. G. Cationic Nanoparticles Induce Nanoscale Disruption in Living Cell Plasma Membranes J. Phys. Chem. B 2009, 113, 11179-11185
23. Hu, W. G.; Som, A.; Tew, G. N. Interaction between Lipids and Antimicrobial Oligomers Studied by Solid-State NMR J. Phys. Chem. B 2011, 115, 8474-8480
24. Tang, H.; Doerksen, R. J.; Jones, T. V.; Klein, M. L.; Tew, G. N. Biomimetic facially amphiphilic antibacterial oligomers with conformationally stiff backbones Chem. Biol. 2006, 13, 427-435
25. Choi, S.; Isaacs, A.; Clements, D.; Liu, D. H.; 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, 6968-6973
26. Liu, D. H.; 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, 1158-1162 (Pubitemid 39257984)
27. Chen, X. Y.; Tang, H. Z.; Even, M. A.; Wang, J.; Tew, G. N.; Chen, Z. Observing a molecular knife at work J. Am. Chem. Soc. 2006, 128, 2711-2714 (Pubitemid 43327949)
28. Tang, H. Z.; Doerksen, R. J.; Tew, G. N. Synthesis of urea oligomers and their antibacterial activity Chem. Commun. 2005, 1537-1539 (Pubitemid 40543538)
29. Thaker, H. D.; Sgolastra, F.; Clements, D.; Scott, R. W.; Tew, G. N. Synthetic Mimics of Antimicrobial Peptides from Triaryl Scaffolds J. Med. Chem. 2011, 54, 2241-2254
30. Thaker, H. D.; Som, A.; Ayaz, F.; Lui, D. H.; Pan, W. X.; Scott, R. W.; Anguita, J.; Tew, G. N. Synthetic Mimics of Antimicrobial Peptides with Immunomodulatory Responses J. Am. Chem. Soc. 2012, 134, 11088-11091
31. Hancock, R. E. W.; Sahl, H. G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies Nat. Biotechnol. 2006, 24, 1551-1557 (Pubitemid 44967479)
32. Som, A.; Navasa, N.; Percher, A.; Scott, R. W.; Tew, G. N.; Anguita, J. Identification of Synthetic Host Defense Peptide Mimics That Exert Dual Antimicrobial and Anti-Inflammatory Activities Clin. Vaccine Immunol. 2012, 19, 1784-1791
33. Ilker, M. F.; Nusslein, K.; Tew, G. N.; Coughlin, E. B. Tuning the hemolytic and antibacterial activities of amphiphilic polynorbornene derivatives J. Am. Chem. Soc. 2004, 126, 15870-15875 (Pubitemid 39602444)
34. Al-Badri, Z. M.; Som, A.; Lyon, S.; Nelson, C. F.; Nusslein, K.; Tew, G. N. Investigating the Effect of Increasing Charge Density on the Hemolytic Activity of Synthetic Antimicrobial Polymers Biomacromolecules 2008, 9, 2805-2810
35. Colak, S.; Nelson, C. F.; Nusslein, K.; Tew, G. N. Hydrophilic Modifications of an Amphiphilic Polynorbornene and the Effects on its Hemolytic and Antibacterial Activity Biomacromolecules 2009, 10, 353-359
36. Lienkamp, K.; Madkour, A. E.; Musante, A.; Nelson, C. F.; Nusslein, K.; Tew, G. N. Antimicrobial polymers prepared by ROMP with unprecedented selectivity: A molecular construction kit approach J. Am. Chem. Soc. 2008, 130, 9836-9843
37. Lienkamp, K.; Kumar, K. N.; Som, A.; Nusslein, K.; Tew, G. N. "Doubly Selective" Antimicrobial Polymers: How Do They Differentiate between Bacteria? Chem.-Eur. J. 2009, 15, 11710-11714
38. Lienkamp, K.; Madkour, A. E.; Kumar, K. N.; Nusslein, K.; Tew, G. N. Antimicrobial Polymers Prepared by Ring-Opening Metathesis Polymerization: Manipulating Antimicrobial Properties by Organic Counterion and Charge Density Variation Chem.-Eur. J. 2009, 15, 11715-11722
39. Pavia, K. E.; Spinella, S. A.; Elmore, D. E. Novel histone-derived antimicrobial peptides use different antimicrobial mechanisms Biochim. Biophys. Acta, Biomembr. 2012, 1818, 869-876
40. Gabriel, G. J.; Madkour, A. E.; Dabkowski, J. M.; Nelson, C. F.; Nusslein, K.; Tew, G. N. Synthetic Mimic of Antimicrobial Peptide with Nonmembrane-Disrupting Antibacterial Properties Biomacromolecules 2008, 9, 2980-2983
41. Hennig, A.; Gabriel, G. J.; Tew, G. N.; Matile, S. Stimuli-responsive polyguanidino-oxanorbornene membrane transporters as multicomponent sensors in complex matrices J. Am. Chem. Soc. 2008, 130, 10338-10344
42. 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, 19207-19216
43. Mitchell, D. J.; Kim, D. T.; Steinman, L.; Fathman, C. G.; Rothbard, J. B. Polyarginine enters cells more efficiently than other polycationic homopolymers J. Pept. Res. 2000, 56, 318-325
44. Wender, P. A.; Galliher, W. C.; Goun, E. A.; Jones, L. R.; Pillow, T. H. The design of guanidinium-rich transporters and their internalization mechanisms Adv. Drug Delivery Rev. 2008, 60, 452-472
45. Kawamoto, S.; Takasu, M.; Miyakawa, T.; Morikawa, R.; Oda, T.; Futaki, S.; Nagao, H. Binding of Tat peptides on DOPC and DOPG lipid bilayer membrane studied by molecular dynamics simulations Mol. Simul. 2012, 38, 366-368
46. Kawamoto, S.; Miyakawa, T.; Takasu, M.; Morikawa, R.; Oda, T.; Saito, H.; Futaki, S.; Nagao, H. Cell-Penetrating Peptide Induces Various Deformations of Lipid Bilayer Membrane: Inverted Micelle, Double Bilayer, and Transmembrane Int. J. Quantum Chem. 2012, 112, 178-183
47. Hirose, H.; Takeuchi, T.; Osakada, H.; Pujals, S.; Katayama, S.; Nakase, I.; Kobayashi, S.; Haraguchi, T.; Futaki, S. Transient Focal Membrane Deformation Induced by Arginine-rich Peptides Leads to Their Direct Penetration into Cells Mol. Ther. 2012, 20, 984-993
48. Marschall, A. L. J.; Frenzel, A.; Schirrmann, T.; Schungel, M.; Dubel, S. Targeting antibodies to the cytoplasm MAbs 2011, 3, 3-16
49. Kawamoto, S.; Takasu, M.; Miyakawa, T.; Morikawa, R.; Oda, T.; Futaki, S.; Nagao, H.: Inverted micelle formation of cell-penetrating peptide studied by coarse-grained simulation: Importance of attractive force between cell-penetrating peptides and lipid head group. J. Chem. Phys. 2011, 134.
50. Green, M.; Loewenstein, P. M. Autonomous Functional Domains of Chemically Synthesized Human Immunodeficiency Virus Tat Trans-Activator Protein Cell 1988, 55, 1179-1188 (Pubitemid 19020070)
51. Frankel, A. D.; Pabo, C. O. Cellular Uptake of the Tat Protein from Human Immunodeficiency Virus Cell 1988, 55, 1189-1193 (Pubitemid 19020071)
52. Vives, E.; Brodin, P.; Lebleu, B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus J. Biol. Chem. 1997, 272, 16010-16017 (Pubitemid 27265584)
53. Wender, P. A.; Mitchell, D. J.; Pattabiraman, K.; Pelkey, E. T.; Steinman, L.; Rothbard, J. B. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 13003-13008
54. Goun, E. A.; Pillow, T. H.; Jones, L. R.; Rothbard, J. B.; Wender, P. A. Molecular transporters: Synthesis of oligoguanidinium transporters and their application to drug delivery and real-time imaging ChemBioChem 2006, 7, 1497-1515 (Pubitemid 44555995)
55. Potocky, T. B.; Silvius, J.; Menon, A. K.; Gellman, S. H. HeLa cell entry by guanidinium-rich beta-peptides: Importance of specific cation-cell surface interactions ChemBioChem 2007, 8, 917-926 (Pubitemid 47194840)
56. Joliot, A.; Pernelle, C.; Deagostinibazin, H.; Prochiantz, A. Antennapedia Homeobox Peptide Regulates Neural Morphogenesis Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 1864-1868 (Pubitemid 21916327)
57. Derossi, D.; Joliot, A. H.; Chassaing, G.; Prochiantz, A. The 3rd Helix of the Antennapedia Homeodomain Translocates through Biological-Membranes J. Biol. Chem. 1994, 269, 10444-10450 (Pubitemid 24198241)
58. Derossi, D.; Chassaing, G.; Prochiantz, A. Trojan peptides: the penetratin system for intracellular delivery Trends Cell Biol. 1998, 8, 84-87 (Pubitemid 28056816)
59. Pooga, M.; Hallbrink, M.; Zorko, M.; Langel, U. Cell penetration by transportan FASEB J. 1998, 12, 67-77 (Pubitemid 28060272)
60. Morris, M. C.; Depollier, J.; Mery, J.; Heitz, F.; Divita, G. A peptide carrier for the delivery of biologically active proteins into mammalian cells Nat. Biotechnol. 2001, 19, 1173-1176 (Pubitemid 33115705)
61. Kolonko, E. M.; Kiessling, L. L. A polymeric domain that promotes cellular internalization J. Am. Chem. Soc. 2008, 130, 5626-5627 (Pubitemid 351600476)
62. Cooley, C. B.; Trantow, B. M.; Nederberg, F.; Kiesewetter, M. K.; Hedrick, J. L.; Waymouth, R. M.; Wender, P. A. Oligocarbonate Molecular Transporters: Oligomerization-Based Syntheses and Cell-Penetrating Studies J. Am. Chem. Soc. 2009, 131, 16401-16403
63. Geihe, E. I.; Cooley, C. B.; Simon, J. R.; Kiesewetter, M. K.; Edward, J. A.; Hickerson, R. P.; Kaspar, R. L.; Hedrick, J. L.; Waymouth, R. M.; Wender, P. A. Designed guanidinium-rich amphipathic oligocarbonate molecular transporters complex, deliver and release siRNA in cells Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 13171-13176
64. Som, A.; Tezgel, A. O.; Gabriel, G. J.; Tew, G. N. Self Activation in De Novo Designed Mimics of Cell Penetrating Peptides Angew. Chem., Int. Ed. 2011, 50, 6147-6150
65. Nishihara, M.; Perret, F.; Takeuchi, T.; Futaki, S.; Lazar, A. N.; Coleman, A. W.; Sakai, N.; Matile, S. Arginine magic with new counterions up the sleeve Org. Biomol. Chem. 2005, 3, 1659-1669 (Pubitemid 40683090)
66. Som, A.; Reuter, A.; Tew, G. N. Protein Transduction Domain Mimics: The Role of Aromatic Functionality Angew. Chem., Int. Ed. 2012, 51, 980-983
67. Tezgel, A. O.; Telfer, J. C.; Tew, G. N. De Novo Designed Protein Transduction Domain Mimics from Simple Synthetic Polymers Biomacromolecules 2011, 12, 3078-3083
68. Tezgel, A. O.; Gonzalez-Perez, G.; Telfer, J. C.; Osborne, B. A.; Minter, L. M.; Tew, G. N. Novel Protein Transduction Domain Mimics as Nonviral Delivery Vectors for siRNA Targeting NOTCH1 in Primary Human T cells Mol. Ther. 2013, 21, 201-209