Multifunctional host defense peptides: Intracellular-targeting antimicrobial peptides

FEBS Journal

Volumn 276, Issue 22, 2009, Pages 6483-6496

  Nicolas, Pierre ^a  

^a SORBONNE UNIVERSITÉ   (France)

Author keywords

Antimicrobial peptides; Cell penetrating peptides; Dermaseptin; Intracellular target; Membrane translocation

Indexed keywords

APIDAECIN; BACTENECIN 7; BUFORIN 2; CELL PENETRATING PEPTIDE; CRYPTDIN 4; DERMASEPTIN; HISTATIN 5; INDOLICIDIN; MAGAININ 2; PLEUROCIDIN; POLYPEPTIDE ANTIBIOTIC AGENT; POLYPHEMUSIN 1; PYRRHOCORICIN; TACHYPLESIN; TACHYPLESIN 1; TRITRPTICIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; BACTERIAL MEMBRANE; CELL DEATH; CELL FRACTIONATION; CELL KILLING; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DNA SYNTHESIS INHIBITION; DRUG MECHANISM; DRUG POTENCY; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROPHOBICITY; LIPID COMPOSITION; MEMBRANE DAMAGE; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; SHORT SURVEY; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BIOLOGICAL TRANSPORT; CELL MEMBRANE; HUMANS; PEPTIDES;

MAMMALIA;

EID: 70350435548     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07359.x     Document Type: Short Survey

References (78)

1. Hancock RE Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24, 1551 1557.
2. Yeaman MR Yount NY (2007) Unifying themes in host defence effector polypeptides. Nat Rev Microbiol 9, 727 740.
3. Hölzl MA, Hofer J, Steinberger P, Pfistershammer K Zlabinger GJ (2008) Host antimicrobial proteins as endogenous immunomodulators. Immunol Lett 119, 4 11.
4. Lai Y Gallo RL (2009) AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 3, 131 141.
5. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3, 238 250.
6. Otvos L Jr. (2005) Antibacterial peptides and proteins with multiple cellular targets. J Pept Sci 11, 697 706.
7. Hale JD Hancock RE (2007) Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev Anti Infect Ther 6, 951 959.
8. Henriques ST, Melo MN Castanho MA (2006) Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem J 399, 1 7.
9. Yang ST, Shin SY, Hahm KS Kim JI (2006) Different modes in antibiotic action of tritrpticin analogs, cathelicidin-derived Trp-rich and Pro/Arg-rich peptides. Biochim Biophys Acta 1758, 1580 1586.
10. Galanth C, Abbassi F, Lequin O, Ayala-Sanmartin J, Ladram A, Nicolas P Amiche M (2009) Mechanism of antibacterial action of dermaseptin B2: interplay between helix-hinge-helix structure and membrane curvature strain. Biochemistry 48, 313 327.
11. Nicolas P El Amri C (2009) The dermaseptin superfamily: a gene-based combinatorial library of antimicrobial peptides. Biochim Biophys Acta 1788, 1537 1550.
12. Zhang L, Dhillon P, Yan H, Farmer S Hancock RE (2000) Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrob Agents Chemother 44, 3317 3321.
13. Yount NY, Bayer AS, Xiong YQ Yeaman MR (2006) Advances in antimicrobial peptide immunobiology. Biopolymers 84, 435 458.
14. Koo SP, Bayer AS Yeaman MR (2001) Diversity in antistaphylococcal mechanisms among membrane-targeting antimicrobial peptides. Infect Immun 69, 4916 4922.
15. Tossi A, Tarantino C Romeo D (1997) Design of synthetic antimicrobial peptides based on sequence analogy and amphipathicity. Eur J Biochem 250, 549 558.
16. El Amri C, Bruston F, Joanne P, Lacombe C Nicolas P (2007) Intrinsic flexibility and structural adaptability of plasticins membrane-damaging peptides as a strategy for functional versatility. Eur Biophys J 36, 901 909.
17. El Amri C Nicolas P (2008) Plasticins: membrane-damaging peptides with 'chameleon-like' properties. Cell Mol Life Sci 65, 895 909.
18. Mangoni ML, Papo N, Barra D, Simmaco M, Bozzi A, Di Giulio A Rinaldi AC (2004) Effects of the antimicrobial peptide temporin L on cell morphology, membrane permeability and viability of Escherichia coli. Biochem J 380, 859 865.
19. Bhattacharjya S Ramamoorthy A (2009) Multifunctional host defense peptides: functional and mechanistic insights from NMR structures of potent antimicrobial peptides. FEBS J 276, doi :.
20. Sevcsik E, Pabst G, Richter W, Danner S, Amenitsch H Lohner K (2008) Interaction of LL-37 with model membrane systems of different complexity: influence of the lipid matrix. Biophys J 94, 4688 4699.
21. Zhang L, Rozek A Hancock RE (2001) Interaction of cationic antimicrobial peptides with model membranes. J Biol Chem 276, 35714 35722.
22. Pag U, Oedenkoven M, Sass V, Shai Y, Shamova O, Antcheva N, Tossi A Sahl HG (2008) Analysis of in vitro activities and modes of action of synthetic antimicrobial peptides derived from an alpha-helical 'sequence template'. J Antimicrob Chemother 61, 341 352.
23. Strahilevitz J, Mor A, Nicolas P Shai Y (1994) Spectrum of antimicrobial activity and assembly of dermaseptin-b and its precursor form in phospholipid membranes. Biochemistry 33, 10951 10960.
24. Matsuzaki K (1998) Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim Biophys Acta 1376, 391 400.
25. Shai Y (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66, 236 248.
26. Huang HW, Chen FY Lee MT (2004) Molecular mechanism of peptide-induced pores in membranes. Phys Rev Lett 92, 198304.
27. Uematsu N Matsuzaki K (2000) Polar angle as a determinant of amphipathic alpha-helix-lipid interactions: a model peptide study. Biophys J 79, 2075 2083.
28. Melo MN, Ferre R Castanho MA (2009) Antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 7, 245 250.
29. Jean-François F, Castano S, Desbat B, Odaert B, Roux M, Metz-Boutigue MH Dufourc EJ (2008) Aggregation of cateslytin beta-sheets on negatively charged lipids promotes rigid membrane domains. A new mode of action for antimicrobial peptides? Biochemistry 47, 6394 6402.
30. Epand RM Epand RF (2009) Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta 1788, 289 294.
31. Leontiadou H, Mark AE Marrink SJ (2006) Antimicrobial peptides in action. J Am Chem Soc 128, 12156 12161.
32. Jean-François F, Elezgaray J, Berson P, Vacher P Dufourc EJ (2008) Pore formation induced by an antimicrobial peptide: electrostatic effects. Biophys J 95, 5748 5756.
33. Sengupta D, Leontiadou H, Mark AE Marrink SJ (2008) Toroidal pores formed by antimicrobial peptides show significant disorder. Biochim Biophys Acta 1778, 2308 2317.
34. Mason AJ, Moussaoui W, Abdelrahman T, Boukhari A, Bertani P, Marquette A, Shooshtarizaheh P, Moulay G, Boehm N, Guerold B et al. (2009) Structural determinants of antimicrobial and antiplasmodial activity and selectivity in histidine-rich amphipathic cationic peptides. J Biol Chem 284, 119 133.
35. Herce HD Garcia AE (2007) Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proc Natl Acad Sci USA 104, 20805 20810.
36. Otvos L Jr. (2002) The short proline-rich antibacterial peptide family. Cell Mol Life Sci 59, 1138 1150.
37. Kragol G, Hoffmann R, Chattergoon MA, Lovas S, Cudic M, Bulet P, Condie BA, Rosengren KJ, Montaner LJ Otvos L Jr. (2002) Identification of crucial residues for the antibacterial activity of the proline-rich peptide, pyrrhocoricin. Eur J Biochem 269, 4226 4237. (Pubitemid 35026009)
38. Otvos L, Snyder C, Condie B, Bulet P Wade JD (2005) Chimeric antimicrobial peptides exhibit multiple modes of action. Int J Pept Res Ther 11, 29 42.
39. Li WF, Ma GX Zhou XX (2006) Apidaecin-type peptides: biodiversity, structure-function relationships and mode of action. Peptides 27, 2350 2359.
40. Podda E, Benincasa M, Pacor S, Micali F, Mattiuzzo M, Gennaro R Scocchi M (2006) Dual mode of action of Bac7, a proline-rich antibacterial peptide. Biochim Biophys Acta 1760, 1732 1740.
41. Luque-Ortega JR, van't Hof W, Veerman EC, Saugar JM Rivas L (2008) Human antimicrobial peptide histatin 5 is a cell-penetrating peptide targeting mitochondrial ATP synthesis in Leishmania. FASEB J 22, 1817 1828.
42. Mochon AB Liu H (2008) The antimicrobial peptide histatin-5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm. PLoS Pathog 4, e1000190.
43. Cho JH, Sung BH Kim SC (2009) Buforins: histone H2A-derived antimicrobial peptides from toad stomach. Biochim Biophys Acta 1788, 1564 1569.
44. Takeshima K, Chikushi A, Lee KK, Yonehara S Matsuzaki K (2003) Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J Biol Chem 278, 1310 1315.
45. Fleming E, Maharaj NP, Chen JL, Nelson RB Elmore DE (2008) Effect of lipid composition on buforin II structure and membrane entry. Proteins 73, 480 491.
46. Kobayashi S, Chikushi A, Tougu S, Imura Y, Nishida M, Yano Y Matsuzaki K (2004) Membrane translocation mechanism of the antimicrobial peptide buforin 2. Biochemistry 43, 15610 15616.
47. Uyterhoeven ET, Butler CH, Ko D Elmore DE (2008) Investigating the nucleic acid interactions and antimicrobial mechanism of buforin II. FEBS Lett 582, 1715 1718.
48. Park KH, Park Y, Park IS, Hahm KS Shin SY (2008) Bacterial selectivity and plausible mode of antibacterial action of designed Pro-rich short model antimicrobial peptides. J Pept Sci 14, 876 882.
49. Hsu CH, Chen C, Jou ML, Lee AY, Lin YC, Yu YP, Huang WT Wu SH (2005) Structural and DNA-binding studies on the bovine antimicrobial peptide, indolicidin: evidence for multiple conformations involved in binding to membranes and DNA. Nucleic Acids Res 33, 4053 4064.
50. Nan YH, Park KH, Park Y, Jeon YJ, Kim Y, Park IS, Hahm KS Shin SY (2009) Investigating the effects of positive charge and hydrophobicity on the cell selectivity, mechanism of action and anti-inflammatory activity of a Trp-rich antimicrobial peptide indolicidin. FEMS Microbiol Lett 292, 134 140.
51. Imura Y, Choda N Matsuzaki K (2008) Magainin 2 in action: distinct modes of membrane permeabilization in living bacterial and mammalian cells. Biophys J 95, 5757 5765.
52. Powers JP, Tan A, Ramamoorthy A Hancock RE (2005) Solution structure and interaction of the antimicrobial polyphemusins with lipid membranes. Biochemistry 44, 15504 15513.
53. Powers JP, Rozek A Hancock RE (2004) Structure-activity relationships for the beta-hairpin cationic antimicrobial peptide polyphemusin I. Biochim Biophys Acta 1698, 239 250.
54. Powers JP, Martin MM, Goosney DL Hancock RE (2006) The antimicrobial peptide polyphemusin localizes to the cytoplasm of Escherichia coli following treatment. Antimicrob Agents Chemother 50, 1522 1524.
55. Doherty T, Waring AJ Hong M (2006) Membrane-bound conformation and topology of the antimicrobial peptide tachyplesin I by solid-state NMR. Biochemistry 45, 13323 13330.
56. Matsuzaki K, Yoneyama S, Fujii N, Miyajima K, Yamada K, Kirino Y Anzai K (1997) Membrane permeabilization mechanisms of a cyclic antimicrobial peptide, tachyplesin I, and its linear analog. Biochemistry 36, 9799 9806.
57. Imura Y, Nishida M, Ogawa Y, Takakura Y Matsuzaki K (2007) Action mechanism of tachyplesin I and effects of PEGylation. Biochim Biophys Acta 1768, 1160 1169.
58. Yonezawa A, Kuwahara J, Fujii N Sugiura Y (1992) Binding of tachyplesin I to DNA revealed by footprinting analysis: significant contribution of secondary structure to DNA binding and implication for biological action. Biochemistry 31, 2998 3004.
59. Patrzykat A, Friedrich CL, Zhang L, Mendoza V Hancock RE (2002) Sublethal concentrations of pleurocidin-derived antimicrobial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob Agents Chemother 46, 605 614.
60. Mason AJ, Marquette A Bechinger B (2007) Zwitterionic phospholipids and sterols modulate antimicrobial peptide-induced membrane destabilization. Biophys J 93, 4289 4299.
61. Hadjicharalambous C, Sheynis T, Jelinek R, Shanahan MT, Ouellette AJ Gizeli E (2008) Mechanisms of alpha-defensin bactericidal action: comparative membrane disruption by cryptdin-4 and its disulfide-null analogue. Biochemistry 47, 12626 12634.
62. Schibli DJ, Nguyen LT, Kernaghan SD, Rekdal Ø Vogel HJ (2006) Structure-function analysis of tritrpticin analogs: potential relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures. Biophys J 91, 4413 4426.
63. Fischer R, Fotin-Mleczek M, Hufnagel H Brock R (2005) Break on through to the other side - biophysics and cell biology shed light on cell-penetrating peptides. Chembiochem 6, 2126 2142.
64. Hong RW, Shchepetov M, Weiser JN Axelsen PH (2003) Transcriptional profile of the Escherichia coli response to the antimicrobial insect peptide cecropin A. Antimicrob Agents Chemother 47, 1 6.
65. Morton CO, Hayes A, Wilson M, Rash BM, Oliver SG Coote P (2007) Global phenotype screening and transcript analysis outlines the inhibitory mode(s) of action of two amphibian-derived, alpha-helical, cationic peptides on Saccharomyces cerevisiae. Antimicrob Agents Chemother 51, 3948 3959.
66. Nekhotiaeva N, Elmquist A, Rajarao GK, Hällbrink M, Langel U Good L (2004) Cell entry and antimicrobial properties of eukaryotic cell-penetrating peptides. FASEB J 18, 394 396.
67. Arrighi RB, Ebikeme C, Jiang Y, Ranford-Cartwright L, Barrett MP, Langel U Faye I (2008) Cell-penetrating peptide TP10 shows broad-spectrum activity against both Plasmodium falciparum and Trypanosoma brucei brucei. Antimicrob Agents Chemother 52, 3414 3417.
68. Palm C, Jayamanne M, Kjellander M Hällbrink M (2007) Peptide degradation is a critical determinant for cell-penetrating peptide uptake. Biochim Biophys Acta 1768, 1769 1776.
69. Palm C, Netzereab S Hällbrink M (2006) Quantitatively determined uptake of cell-penetrating peptides in non-mammalian cells with an evaluation of degradation and antimicrobial effects. Peptides 27, 1710 1716.
70. Zhu WL Shin SY (2009) Antimicrobial and cytolytic activities and plausible mode of bactericidal action of the cell penetrating peptide penetratin and its lys-linked two-stranded peptide. Chem Biol Drug Des 73, 209 215.
71. Zhu WL Shin SY (2009) Effects of dimerization of the cell-penetrating peptide Tat analog on antimicrobial activity and mechanism of bactericidal action. J Pept Sci 15, 345 352.
72. Henriques ST Castanho MA (2008) Translocation or membrane disintegration? Implication of peptide-membrane interactions in pep-1 activity J Pept Sci 14, 482 487.
73. Henriques ST Castanho MA (2004) Consequences of nonlytic membrane perturbation to the translocation of the cell penetrating peptide pep-1 in lipidic vesicles. Biochemistry 43, 9716 9724.
74. Deshayes S, Heitz A, Morris MC, Charnet P, Divita G Heitz F (2004) Insight into the mechanism of internalization of the cell-penetrating carrier peptide Pep-1 through conformational analysis. Biochemistry 43, 1449 1457.
75. Palm-Apergi C, Lorents A, Padari K, Pooga M Hällbrink M (2009) The membrane repair response masks membrane disturbances caused by cell-penetrating peptide uptake. FASEB J 23, 214 223.
76. Hansen M, Kilk K Langel U (2008) Predicting cell-penetrating peptides. Adv Drug Deliv Rev 60, 572 579.
77. Mitchell DJ, Kim DT, Steinman L, Fathman CG Rothbard JB (2000) Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 56, 318 325.
78. Tang M, Waring AJ Hong M (2007) Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR. J Am Chem Soc 129, 11438 11446.