Indolicidin action on membrane permeability: Carrier mechanism versus pore formation

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 1, 2011, Pages 91-97

  Rokitskaya, Tatyana I ^a   Kolodkin, Nikolay I ^b   Kotova, Elena A ^a   Antonenko, Yuri N ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b Institute for Highly Pure Biopreparations   (Russian Federation)

Author keywords

Antimicrobial peptide; Arginine; Bilayer lipid membrane; Fluorescence; Leakage; Liposome

Indexed keywords

ARGININE; CALCEIN; CARBOXYFLUORESCEIN; FLUORESCENT DYE; INDOLICIDIN; LIPOSOME; ORGANIC ANION TRANSPORTER; PHOSPHATIDYLCHOLINE; SULFORHODAMINE B;

ARTICLE; CELL PERMEABILIZATION; COMPLEX FORMATION; CONTROLLED STUDY; DRUG ACTIVITY; ERYTHROCYTE MEMBRANE; HEMOLYSIS; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; MEMBRANE PERMEABILITY; OSMOSIS; PH; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CATIONS; CELL MEMBRANE; COLORING AGENTS; FLUORESCEINS; LIPID BILAYERS; MOLECULAR SEQUENCE DATA; OSMOSIS; PEPTIDES; PERMEABILITY; PHOSPHATIDYLCHOLINES; RHODAMINES;

EID: 78649798989     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.09.005     Document Type: Article

References (56)

1. Y. Shai Mode of action of membrane active antimicrobial peptides Biopolymers 66 2002 236 248
2. Y. Agawa, S. Lee, S. Ono, H. Aoyagi, M. Ohno, T. Taniguchi, K. Anzai, and Y. Kirino Interaction with phospholipid bilayers, ion channel formation, and antimicrobial activity of basic amphipathic alpha-helical model peptides of various chain lengths J. Biol. Chem. 266 1991 20218 20222
3. S. Cociancich, A. Ghazi, C. Hetru, J.A. Hoffmann, and L. Letellier Insect defensin, an inducible antibacterial peptide, forms voltage-dependent channels in Micrococcus luteus J. Biol. Chem. 268 1993 19239 19245
4. M. Zasloff Antimicrobial peptides of multicellular organisms Nature 415 2002 389 395
5. K. Matsuzaki, O. Murase, N. Fujii, and K. Miyajima An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation Biochemistry 35 1996 11361 11368
6. S.J. Ludtke, K. He, W.T. Heller, T.A. Harroun, L. Yang, and H.W. Huang Membrane pores induced by magainin Biochemistry 35 1996 13723 13728
7. A. Pokorny, and P.F. Almeida Kinetics of dye efflux and lipid flip-flop induced by delta-lysin in phosphatidylcholine vesicles and the mechanism of graded release by amphipathic, alpha-helical peptides Biochemistry 43 2004 8846 8857
8. G. Baumann, and P. Mueller A molecular model of membrane excitability J. Supramol. Struct. 2 1974 538 557
9. M.S. Sansom The biophysics of peptide models of ion channels Prog. Biophys. Mol. Biol. 55 1991 139 235
10. Y. Shai Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides Biochim. Biophys. Acta 1462 1999 55 70
11. J.M. Ruysschaert, E. Goormaghtigh, F. Homble, M. Andersson, E. Liepinsh, and G. Otting Lipid membrane binding of NK-lysin FEBS Lett. 425 1998 341 344
12. M. Miteva, M. Andersson, A. Karshikoff, and G. Otting Molecular electroporation: a unifying concept for the description of membrane pore formation by antibacterial peptides, exemplified with NK-lysin FEBS Lett. 462 1999 155 158
13. D. Derossi, S. Calvet, A. Trembleau, A. Brunissen, G. Chassaing, and A. Prochiantz Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent J. Biol. Chem. 271 1996 18188 18193
14. R.M. Epand, and R.F. Epand Lipid domains in bacterial membranes and the action of antimicrobial agents Biochim. Biophys. Acta 1788 2009 289 294
15. N. Sakai, and S. Matile Anion-mediated transfer of polyarginine across liquid and bilayer membranes J. Am. Chem. Soc. 125 2003 14348 14356
16. A. Hennig, G.J. Gabriel, G.N. Tew, and S. Matile Stimuli-responsive polyguanidino-oxanorbornene membrane transporters as multicomponent sensors in complex matrices J. Am. Chem. Soc. 130 2008 10338 10344
17. L. Zhang, A. Rozek, and R.E. Hancock Interaction of cationic antimicrobial peptides with model membranes J. Biol. Chem. 276 2001 35714 35722
18. S. Kobayashi, A. Chikushi, S. Tougu, Y. Imura, M. Nishida, Y. Yano, and K. Matsuzaki Membrane translocation mechanism of the antimicrobial peptide buforin 2 Biochemistry 43 2004 15610 15616
19. K. Takeshima, A. Chikushi, K.K. Lee, S. Yonehara, and K. Matsuzaki Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes J. Biol. Chem. 278 2003 1310 1315
20. M.C. Morris, J. Depollier, J. Mery, F. Heitz, and G. Divita A peptide carrier for the delivery of biologically active proteins into mammalian cells Nat. Biotechnol. 19 2001 1173 1176
21. M. Lindgren, M. Hallbrink, A. Prochiantz, and U. Langel Cell-penetrating peptides Trends Pharmacol. Sci. 21 2000 99 103
22. M. Tang, A.J. Waring, and M. Hong Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR J. Am. Chem. Soc. 129 2007 11438 11446
23. M.E. Selsted, M.J. Novotny, W.L. Morris, Y.Q. Tang, W. Smith, and J.S. Cullor Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils J. Biol. Chem. 267 1992 4292 4295
24. A. Giacometti, O. Cirioni, G. Greganti, M. Quarta, and G. Scalise In vitro activities of membrane-active peptides against gram-positive and gram-negative aerobic bacteria Antimicrob. Agents Chemother. 42 1998 3320 3324
25. I. Ahmad, W.R. Perkins, D.M. Lupan, M.E. Selsted, and A.S. Janoff Liposomal entrapment of the neutrophil-derived peptide indolicidin endows it with in vivo antifungal activity Biochim. Biophys. Acta 1237 1995 109 114
26. D.G. Lee, H.K. Kim, S.A. Kim, Y. Park, S.C. Park, S.H. Jang, and K.S. Hahm Fungicidal effect of indolicidin and its interaction with phospholipid membranes Biochem. Biophys. Res. Commun. 305 2003 305 310
27. W.E. Robinson Jr., B. McDougall, D. Tran, and M.E. Selsted Anti-HIV-1 activity of indolicidin, an antimicrobial peptide from neutrophils J. Leukoc. Biol. 63 1998 94 100
28. T.J. Falla, D.N. Karunaratne, and R.E. Hancock Mode of action of the antimicrobial peptide indolicidin J. Biol. Chem. 271 1996 19298 19303
29. A.S. Ladokhin, M.E. Selsted, and S.H. White Bilayer interactions of indolicidin, a small antimicrobial peptide rich in tryptophan, proline, and basic amino acids Biophys. J. 72 1997 794 805
30. J.E. Shaw, R.F. Epand, J.C. Hsu, G.C. Mo, R.M. Epand, and C.M. Yip Cationic peptide-induced remodelling of model membranes: direct visualization by in situ atomic force microscopy J. Struct. Biol. 162 2008 121 138
31. C.W. Tsai, N.Y. Hsu, C.H. Wang, C.Y. Lu, Y. Chang, H.H. Tsai, and R.C. Ruaan Coupling molecular dynamics simulations with experiments for the rational design of indolicidin-analogous antimicrobial peptides J. Mol. Biol. 392 2009 837 854
32. C. Subbalakshmi, V. Krishnakumari, N. Sitaram, and R. Nagaraj Interaction of indolicidin, a 13-residue peptide rich in tryptophan and proline and its analogues with model membranes J. Biosci. 23 1998 9 13
33. D.J. Schibli, L.T. Nguyen, S.D. Kernaghan, O. Rekdal, and 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
34. V.V. Andrushchenko, M.H. Aarabi, L.T. Nguyen, E.J. Prenner, and H.J. Vogel Thermodynamics of the interactions of tryptophan-rich cathelicidin antimicrobial peptides with model and natural membranes Biochim. Biophys. Acta 1778 2008 1004 1014
35. H.J. Askou, R.N. Jakobsen, and P. Fojan An atomic force microscopy study of the interactions between indolicidin and supported planar bilayers J. Nanosci. Nanotechnol. 8 2008 4360 4369
36. K.H. Park, Y.H. Nan, Y. Park, J.I. Kim, I.S. Park, K.S. Hahm, and S.Y. Shin Cell specificity, anti-inflammatory activity, and plausible bactericidal mechanism of designed Trp-rich model antimicrobial peptides Biochim. Biophys. Acta 1788 2009 1193 1203
37. S.M. Kim, J.M. Kim, B.P. Joshi, H. Cho, and K.H. Lee Indolicidin-derived antimicrobial peptide analogs with greater bacterial selectivity and requirements for antibacterial and hemolytic activities Biochim. Biophys. Acta 1794 2009 185 192
38. D.J. Schibli, R.F. Epand, H.J. Vogel, and R.M. Epand Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions Biochem. Cell Biol. 80 2002 667 677
39. M.P. Smirnova, V.G. Afonin, V.M. Shpen', I. Tiagotin, and N.I. Kolodkin Structure-function relationship between analogues of the antibacterial peptide indolicidin. I. Synthesis and biological activity of analogues with increased amphipathicity and elevated net positive charge of the molecule Russ. J. Bioorg. Chem. 30 2004 409 416
40. V.Y. Erukova, O.O. Krylova, Y.N. Antonenko, and N.S. Melik-Nubarov Effect of ethylene oxide and propylene oxide block copolymers on the permeability of bilayer lipid membranes to small solutes including doxorubicin Biochim. Biophys. Acta 1468 2000 73 86
41. J.A. Haxby, O. Gotze, H.J. Muller-Eberhard, and S.C. Kinsky Release of trapped marker from liposomes by the action of purified complement components Proc. Natl Acad. Sci. USA 64 1969 290 295
42. J.M. Gonzalez-Manas, J.H. Lakey, and F. Pattus Brominated phospholipids as a tool for monitoring the membrane insertion of colicin A Biochemistry 31 1992 7294 7300
43. H. Zhao, J.P. Mattila, J.M. Holopainen, and P.K. Kinnunen Comparison of the membrane association of two antimicrobial peptides, magainin 2 and indolicidin Biophys. J. 81 2001 2979 2991
44. P. Guterstam, F. Madani, H. Hirose, T. Takeuchi, S. Futaki, S. El Andaloussi, A. Graslund, and U. Langel Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate Biochim. Biophys. Acta 1788 2009 2509 2517
45. M. Nishihara, F. Perret, T. Takeuchi, S. Futaki, A.N. Lazar, A.W. Coleman, N. Sakai, and S. Matile Arginine magic with new counterions up the sleeve Org. Biomol. Chem. 3 2005 1659 1669
46. F. Perret, M. Nishihara, T. Takeuchi, S. Futaki, A.N. Lazar, A.W. Coleman, N. Sakai, and S. Matile Anionic fullerenes, calixarenes, coronenes, and pyrenes as activators of oligo/polyarginines in model membranes and live cells J. Am. Chem. Soc. 127 2005 1114 1115
47. J. Bramhall, J. Hofmann, R. DeGuzman, S. Montestruque, and R. Schell Temperature dependence of membrane ion conductance analyzed by using the amphiphilic anion 5/6-carboxyfluorescein Biochemistry 26 1987 6330 6340
48. 15N NMR Biochemistry 34 1995 13196 13202
49. + and calcein release from liposomes and the determination of pore size formed in a membrane Anal. Sci. 23 2007 517 522
50. P. Staubitz, A. Peschel, W.F. Nieuwenhuizen, M. Otto, F. Gotz, G. Jung, and R.W. Jack Structure-function relationships in the tryptophan-rich, antimicrobial peptide indolicidin J. Pept. Sci. 7 2001 552 564
51. T.S. Ryge, X. Doisy, D. Ifrah, J.E. Olsen, and P.R. Hansen New indolicidin analogues with potent antibacterial activity J. Pept. Res. 64 2004 171 185
52. C. Subbalakshmi, V. Krishnakumari, R. Nagaraj, and N. Sitaram Requirements for antibacterial and hemolytic activities in the bovine neutrophil derived 13-residue peptide indolicidin FEBS Lett. 395 1996 48 52
53. C. Subbalakshmi, E. Bikshapathy, N. Sitaram, and R. Nagaraj Antibacterial and hemolytic activities of single tryptophan analogs of indolicidin Biochem. Biophys. Res. Commun. 274 2000 714 716
54. S. Ando, K. Mitsuyasu, Y. Soeda, M. Hidaka, Y. Ito, K. Matsubara, M. Shindo, Y. Uchida, and H. Aoyagi Structure-activity relationship of indolicidin, a Trp-rich antibacterial peptide J. Pept. Sci. 16 2010 171 177
55. A.P. Podorieszach, and H.E. Huttunen-Hennelly The effects of tryptophan and hydrophobicity on the structure and bioactivity of novel indolicidin derivatives with promising pharmaceutical potential Org. Biomol. Chem. 8 2010 1679 1687
56. A. Merckx, G. Bouyer, S.L. Thomas, G. Langsley, and S. Egee Anion channels in Plasmodium-falciparum-infected erythrocytes and protein kinase A Trends Parasitol. 25 2009 139 144