Role of arginine and lysine in the antimicrobial mechanism of histone-derived antimicrobial peptides

FEBS Letters

Volumn 589, Issue 24, 2015, Pages 3915-3920

  Cutrona, Kara J ^a,b   Kaufman, Bethany A ^a   Figueroa, Dania M ^a   Elmore, Donald E ^a  

^a WELLESLEY COLLEGE   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

Arginine; Buforin; Histone derived antimicrobial peptide; Membrane permeabilization; Membrane translocation; Parasin

Indexed keywords

ANTIMICROBIAL PEPTIDE DESHDAP1; ARGININE; BUFORIN II; LYSINE; PARASIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; HISTONE;

ALPHA HELIX; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL MEMBRANE; CELL PERMEABILIZATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; ESCHERICHIA COLI; LIPID MEMBRANE; LIPID VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DNA BINDING; PROTEIN SECONDARY STRUCTURE; AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; ARGININE; CELL MEMBRANE; HISTONES; LYSINE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84959477848     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.11.002     Document Type: Article

References (49)

1. D.W. Hoskin, A. Ramamoorthy, Studies on anticancer activities of antimicrobial peptides. BBA-Biomembranes, 1778, (2008), 357-375.
2. H. Jenssen, P. Hamill, R.E.W. Hancock, Peptide antimicrobial agents. Clin. Microbiol. Rev., 19, (2006), 491-511.
3. R.E.W. Hancock, H.G. Sahl, Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol., 24, (2006), 1551-1557.
4. O. Toke, Antimicrobial peptides: new candidates in the fight against bacterial infections. Biopolymers, 80, (2005), 717-735.
5. M. Zasloff, Antimicrobial peptides of multicellular organisms. Nature, 415, (2002), 389-395.
6. M.R. Yeaman, N.Y. Yount, Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev., 55, (2003), 27-55.
7. J.D. Hale, R.E. Hancock, Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev. Anti-Infective, 5, (2007), 951-959.
8. C.B. Park, H.S. Kim, S.C. Kim, Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun., 244, (1998), 253-257.
9. C.B. Park, K.S. Yi, K. Matsuzaki, M.S. Kim, S.C. Kim, Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl. Acad. Sci. U.S.A., 97, (2000), 8245-8250.
10. Y. Xie, E. Fleming, J.L. Chen, D.E. Elmore, Effect of proline position on the antimicrobial mechanism of buforin II. Peptides, 32, (2011), 677-682.
11. K. Hristova, W.C. Wimley, A look at arginine in membranes. J. Membr. Biol., 239, (2011), 49-56.
12. J. Svenson, R. Karstad, G.E. Flaten, B.O. Brandsdal, M. Brandl, J.S. Svendsen, Altered activity and physicochemical properties of short cationic antimicrobial peptides by incorporation of arginine analogues. Mol. Pharmaceut., 6, (2009), 996-1005.
13. K. Andreev, C. Bianchi, J.S. Laursen, L. Citterio, L. Hein-Kristensen, L. Gram, I. Kuzmenko, C.A. Olsen, D. Gidalevitz, Guanidino groups greatly enhance the action of antimicrobial peptidomimetics against bacterial cytoplasmic membranes. Biochim. Biophys. Acta, 1838, (2014), 2492-2502.
14. J.S. Bahnsen, H. Franzyk, A. Sandberg-Schaal, H.M. Nielsen, Antimicrobial and cell-penetrating properties of penetratin analogs: effect of sequence and secondary structure. Biochim. Biophys. Acta, 1828, (2013), 223-232.
15. G.J. Gabriel, A.E. Madkour, J.M. Dabkowski, C.F. Nelson, K. Nusslein, G.N. Tew, Synthetic mimic of antimicrobial peptide with nonmembrane-disrupting antibacterial properties. Biomacromolecules, 9, (2008), 2980-2983.
16. K.E. Locock, T.D. Michl, J.D. Valentin, K. Vasilev, J.D. Hayball, Y. Qu, A. Traven, H.J. Griesser, L. Meagher, M. Haeussler, Guanylated polymethacrylates: a class of potent antimicrobial polymers with low hemolytic activity. Biomacromolecules, 14, (2013), 4021-4031.
17. L. Vedel, G. Bonke, C. Foged, H. Ziegler, H. Franzyk, J.W. Jaroszewski, C.A. Olsen, Antiplasmodial and prehemolytic activities of alpha-peptide-beta-peptoid chimeras. Chembiochem, 8, (2007), 1781-1784.
18. N.W. Schmidt, K.P. Tai, K. Kamdar, A. Mishra, G.H. Lai, K. Zhao, A.J. Ouellette, G.C. Wong, Arginine in alpha-defensins: differential effects on bactericidal activity correspond to geometry of membrane curvature generation and peptide-lipid phase behavior. J. Biol. Chem., 287, (2012), 21866-21872.
19. P.W. Chen, C.L. Shyu, F.C. Mao, Antibacterial activity of short hydrophobic and basic-rich peptides. Am. J. Vet. Res., 64, (2003), 1088-1092.
20. L.T. Nguyen, L. de Boer, S.A. Zaat, H.J. Vogel, Investigating the cationic side chains of the antimicrobial peptide tritrpticin: hydrogen bonding properties govern its membrane-disruptive activities. Biochim. Biophys. Acta, 1808, (2011), 2297-2303.
21. D.J. Schibli, L.T. Nguyen, S.D. Kernaghan, O. Rekdal, H.J. Vogel, Structure-function analysis of tritrpticin analogs: potential relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures. Biophys. J., 91, (2006), 4413-4426.
22. M.B. Strom, B.E. Haug, M.L. Skar, W. Stensen, T. Stiberg, J.S. Svendsen, The pharmacophore of short cationic antibacterial peptides. J. Med. Chem., 46, (2003), 1567-1570.
23. I. Nakase, S. Okumura, S. Katayama, H. Hirose, S. Pujals, H. Yamaguchi, S. Arakawa, S. Shimizu, S. Futaki, Transformation of an antimicrobial peptide into a plasma membrane-permeable, mitochondria-targeted peptide via the substitution of lysine with arginine. Chem. Commun., 48, (2012), 11097-11099.
24. D.J. Mitchell, D.T. Kim, L. Steinman, C.G. Fathman, J.B. Rothbard, Polyarginine enters cells more efficiently than other polycationic homopolymers. J. Pept. Res., 56, (2000), 318-325.
25. E.G. Stanzl, B.M. Trantow, J.R. Vargas, P.A. Wender, Fifteen years of cell-penetrating, guanidinium-rich molecular transporters: basic science, research tools, and clinical applications. Accounts Chem. Res., 46, (2013), 2944-2954.
26. S.A. Ouvry-Patat, K.L. Schey, Characterization of antimicrobial histone sequences and posttranslational modifications by mass spectrometry. J. Mass Spectrom., 42, (2007), 664-674.
27. S. Kobayashi, K. Takeshima, C.B. Park, S.C. Kim, K. Matsuzaki, Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor. Biochemistry-US, 39, (2000), 8648-8654.
28. H.S. Tsao, S.A. Spinella, A.T. Lee, D.E. Elmore, Design of novel histone-derived antimicrobial peptides. Peptides, 30, (2009), 2168-2173.
29. E.T. Uyterhoeven, C.H. Butler, D. Ko, D.E. Elmore, Investigating the nucleic acid interactions and antimicrobial mechanism of buforin II. FEBS Lett., 582, (2008), 1715-1718.
30. Y.S. Koo, J.M. Kim, I.Y. Park, B.J. Yu, S.A. Jang, K.S. Kim, C.B. Park, J.H. Cho, S.C. Kim, Structure-activity relations of parasin I, a histone H2A-derived antimicrobial peptide. Peptides, 29, (2008), 1102-1108.
31. G.A. Birkemo, D. Mantzilas, T. Luders, I.F. Nes, J. Nissen-Meyer, Identification and structural analysis of the antimicrobial domain in hipposin, a 51-mer antimicrobial peptide isolated from Atlantic halibut. BBA-Proteins Proteomics, 1699, (2004), 221-227.
32. R.I. Lehrer, M. Rosenman, S.S.S.L. Harwig, R. Jackson, P. Eisenhauer, Ultrasensitive assays for endogenous antimicrobial polypeptides. J. Immunol. Methods, 137, (1991), 167-173.
33. D.A. Steinberg, R.I. Lehrer, Designer assays for antimicrobial peptides. Disputing the "one-size-fits-all" theory. Methods Mol. Biol., 78, (1997), 169-186.
34. C.B. Park, K.S. Yi, K. Matsuzaki, M.S. Kim, S.C. Kim, Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc. Natl. Acad. Sci., 97, (2000), 8245-8250.
35. E. Fleming, N.P. Maharaj, J.L. Chen, R.B. Nelson, D.E. Elmore, Effect of lipid composition on buforin II structure and membrane entry. Proteins, 73, (2008), 480-491.
36. A.S. Ladokhin, S. Jayasinghe, S.H. White, How to measure and analyze tryptophane fluorescence in membrane properly, and why bother?. Anal. Biochem., 285, (2000), 235-245.
37. K.E. Pavia, S.A. Spinella, D.E. Elmore, Novel histone-derived antimicrobial peptides use different antimicrobial mechanisms. BBA-Biomembranes, 1818, (2012), 869-876.
38. S.A. Spinella, R.B. Nelson, D.E. Elmore, Measuring peptide translocation into large unilamellar vesicles. J. Visual. Exp., 59, (2012)
39. M.E. Bustillo, A.L. Fischer, M.A. LaBouyer, J.A. Klaips, A.C. Webb, D.E. Elmore, Modular analysis of hipposin, a histone-derived antimicrobial peptide consisting of membrane translocating and membrane permeabilizing fragments. Biochim. Biophys. Acta, 1838, (2014), 2228-2233.
40. D.E. Elmore, Insights into buforin II membrane translocation from molecular dynamics simulations. Peptides, 38, (2012), 357-362.
41. N.W. Schmidt, M. Lis, K. Zhao, G.H. Lai, A.N. Alexandrova, G.N. Tew, G.C. Wong, Molecular basis for nanoscopic membrane curvature generation from quantum mechanical models and synthetic transporter sequences. J. Am. Chem. Soc., 134, (2012), 19207-19216.
42. N.W. Schmidt, A. Mishra, G.H. Lai, M. Davis, L.K. Sanders, D. Tran, A. Garcia, K.P. Tai, P.B. McCray, A.J. Ouellette, M.E. Selsted, G.C. Wong, Criterion for amino acid composition of defensins and antimicrobial peptides based on geometry of membrane destabilization. J. Am. Chem. Soc., 133, (2011), 6720-6727.
43. C.P. Moon, K.G. Fleming, Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc. Natl. Acad. Sci. U.S.A., 108, (2011), 10174-10177.
44. M. Alami, D. Trescher, L.F. Wu, M. Muller, Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli. J. Biol. Chem., 277, (2002), 20499-20503.
45. K. Cline, Mechanistic aspects of folded protein transport by the twin arginine translocase (Tat). J. Biol. Chem., 290, (2015), 16530-16538.
46. S. Cristobal, J.W. de Gier, H. Nielsen, G. von Heijne, Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J., 18, (1999), 2982-2990.
47. F. Diez-Garcia, A. Chakrabartty, C. Gonzalez, D.V. Laurents, An Arg-rich putative prebiotic protein is as stable as its Lys-rich variant. Arch. Biochem. Biophys., 528, (2012), 118-126.
48. Y.X. Jiang, A. Lee, J.Y. Chen, M. Cadene, B.T. Chait, R. MacKinnon, The open pore conformation of potassium channels. Nature, 417, (2002), 523-526.
49. D. Schmidt, Q.X. Jiang, R. MacKinnon, Phospholipids and the origin of cationic gating charges in voltage sensors. Nature, 444, (2006), 775-779.