Esculentin-1b(1-18) - A membrane-active antimicrobial peptide that synergizes with antibiotics and modifies the expression level of a limited number of proteins in Escherichia coli

FEBS Journal

Volumn 276, Issue 19, 2009, Pages 5647-5664

  Marcellini, Ludovica ^a   Borro, Marina ^a   Gentile, Giovanna ^a   Rinaldi, Andrea C ^b   Stella, Lorenzo ^c   Aimola, Pierpaolo ^d   Barra, Donatella ^a   Mangoni, Maria Luisa ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Frog skin antimicrobial peptides; Gram negative bacteria; Mode of action; Peptide membrane interaction; Proteomics

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN ESCULENTIN 1B(1-18); UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; ESCHERICHIA COLI; IN VIVO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEOMICS; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; AMPHIBIAN PROTEINS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE PERMEABILITY; DRUG SYNERGISM; ERYTHROMYCIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPOPOLYSACCHARIDES; LIPOSOMES; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEOME;

AMPHIBIA; ANURA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 70349238995     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07257.x     Document Type: Article

References (62)

1. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415, 389 395.
2. Brown KL Hancock RE (2006) Cationic host defense (antimicrobial) peptides. Curr Opin Immunol 18, 24 30.
3. Hancock RE Diamond G (2000) The role of cationic antimicrobial peptides in innate host defenses. Trends Microbiol 8, 402 410.
4. Peschel A Sahl HG (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4, 529 536.
5. Hancock RE Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24, 1551 1557.
6. Wenzel RP Edmond MB (2000) Managing antibiotic resistance. N Engl J Med 343, 1961 1963.
7. Jenssen H, Hamill P Hancock RE (2006) Peptide antimicrobial agents. Clin Microbiol Rev 19, 491 511.
8. Rossi LM, Rangasamy P, Zhang J, Qiu XQ Wu GY (2008) Research advances in the development of peptide antibiotics. J Pharm Sci 97, 1060 1070.
9. Shai Y (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66, 236 248.
10. Boman HG, Agerberth B Boman A (1993) Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect Immun 61, 2978 2984.
11. 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.
12. Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R Otvos L Jr. (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40, 3016 3026.
13. 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.
14. Simmaco M, Mignogna G Barra D (1998) Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers 47, 435 450.
15. Mangoni ML, Miele R, Renda TG, Barra D Simmaco M (2001) The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms. FASEB J 15, 1431 1432.
16. Barra D, Simmaco M Boman HG (1998) Gene-encoded peptide antibiotics and innate immunity. Do 'animalcules' have defense budgets? FEBS Lett 430, 130 134.
17. Boland MP Separovic F (2006) Membrane interactions of antimicrobial peptides from Australian tree frogs. Biochim Biophys Acta 1758, 1178 1183.
18. Mangoni ML, Papo N, Saugar JM, Barra D, Shai Y, Simmaco M Rivas L (2006) Effect of natural L- to D-amino acid conversion on the organization, membrane binding, and biological function of the antimicrobial peptides bombinins H. Biochemistry 45, 4266 4276.
19. Mangoni ML (2006) Temporins, anti-infective peptides with expanding properties. Cell Mol Life Sci 63, 1060 1069.
20. Mangoni ML, Maisetta G, Di Luca M, Gaddi LM, Esin S, Florio W, Brancatisano FL, Barra D, Campa M Batoni G (2008) Comparative analysis of the bactericidal activities of amphibian peptide analogues against multidrug-resistant nosocomial bacterial strains. Antimicrob Agents Chemother 52, 85 91.
21. Conlon JM (2008) Reflections on a systematic nomenclature for antimicrobial peptides from the skins of frogs of the family Ranidae. Peptides 29, 1815 1819.
22. Sal-Man N, Oren Z Shai Y (2002) Preassembly of membrane-active peptides is an important factor in their selectivity toward target cells. Biochemistry 41, 11921 11930.
23. Mangoni ML Shai Y (2009) Temporins and their synergism against Gram-negative bacteria and in lipopolysaccharide detoxification. Biochim Biophys Acta 1788, 1610 1619.
24. Maisetta G, Batoni G, Esin S, Florio W, Bottai D, Favilli F Campa M (2006) In vitro bactericidal activity of human beta-defensin 3 against multidrug-resistant nosocomial strains. Antimicrob Agents Chemother 50, 806 809.
25. Oren Z, Hong J Shai Y (1997) A repertoire of novel antibacterial diastereomeric peptides with selective cytolytic activity. J Biol Chem 272, 14643 14649.
26. Park CB, Kim HS Kim SC (1998) 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, 253 257.
27. Hancock RE Bell A (1988) Antibiotic uptake into gram-negative bacteria. Eur J Clin Microbiol Infect Dis 7, 713 720.
28. Gutsmann T, Hagge SO, Larrick JW, Seydel U Wiese A (2001) Interaction of CAP18-derived peptides with membranes made from endotoxins or phospholipids. Biophys J 80, 2935 2945.
29. Clausell A, Garcia-Subirats M, Pujol M, Busquets MA, Rabanal F Cajal Y (2007) Gram-negative outer and inner membrane models: insertion of cyclic cationic lipopeptides. J Phys Chem B 111, 551 563.
30. Giacometti A, Cirioni O, Ghiselli R, Mocchegiani F, Orlando F, Silvestri C, Bozzi A, Di Giulio A, Luzi C, Mangoni ML et al. (2006) Interaction of antimicrobial peptide temporin L with lipopolysaccharide in vitro and in experimental rat models of septic shock caused by gram-negative bacteria. Antimicrob Agents Chemother 50, 2478 2486.
31. Bebrone C, Moali C, Mahy F, Rival S, Docquier JD, Rossolini GM, Fastrez J, Pratt RF, Frere JM Galleni M (2001) CENTA as a chromogenic substrate for studying beta-lactamases. Antimicrob Agents Chemother 45, 1868 1871.
32. Rosenfeld Y, Barra D, Simmaco M, Shai Y Mangoni ML (2006) A synergism between temporins toward Gram-negative bacteria overcomes resistance imposed by the lipopolysaccharide protective layer. J Biol Chem 281, 28565 28574.
33. Johansson E, Majka J Burgers PM (2001) Structure of DNA polymerase delta from Saccharomyces cerevisiae. J Biol Chem 276, 43824 43828.
34. Scudamore RA, Beveridge TJ Goldner M (1979) Outer-membrane penetration barriers as components of intrinsic resistance to beta-lactam and other antibiotics in Escherichia coli K-12. Antimicrob Agents Chemother 15, 182 189.
35. Breukink E, van Kraaij C, Demel RA, Siezen RJ, Kuipers OP de Kruijff B (1997) The C-terminal region of nisin is responsible for the initial interaction of nisin with the target membrane. Biochemistry 36, 6968 6976.
36. Steffen H, Rieg S, Wiedemann I, Kalbacher H, Deeg M, Sahl HG, Peschel A, Gotz F, Garbe C Schittek B (2006) Naturally processed dermcidin-derived peptides do not permeabilize bacterial membranes and kill microorganisms irrespective of their charge. Antimicrob Agents Chemother 50, 2608 2620.
37. Rinaldi AC, Mangoni ML, Rufo A, Luzi C, Barra D, Zhao H, Kinnunen PK, Bozzi A, Di Giulio A Simmaco M (2002) Temporin L: antimicrobial, haemolytic and cytotoxic activities, and effects on membrane permeabilization in lipid vesicles. Biochem J 368, 91 100.
38. Stella L, Mazzuca C, Venanzi M, Palleschi A, Didone M, Formaggio F, Toniolo C Pispisa B (2004) Aggregation and water-membrane partition as major determinants of the activity of the antibiotic peptide trichogin GA IV. Biophys J 86, 936 945.
39. Ladokhin AS, Selsted ME White SH (1997) Sizing membrane pores in lipid vesicles by leakage of co-encapsulated markers: pore formation by melittin. Biophys J 72, 1762 1766.
40. Lieber MR Steck TL (1982) A description of the holes in human erythrocyte membrane ghost J Biol Chem 257, 11651 11659.
41. 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.
42. Bolter B Soll J (2001) Ion channels in the outer membranes of chloroplasts and mitochondria: open doors or regulated gates? EMBO J 20, 935 940.
43. Hong H, Patel DR, Tamm LK van den Berg B (2006) The outer membrane protein OmpW forms an eight-stranded beta-barrel with a hydrophobic channel. J Biol Chem 281, 7568 7577.
44. Merz F, Boehringer D, Schaffitzel C, Preissler S, Hoffmann A, Maier T, Rutkowska A, Lozza J, Ban N, Bukau B et al. (2008) Molecular mechanism and structure of trigger factor bound to the translating ribosome. EMBO J 27, 1622 1632.
45. Hoffmann A, Merz F, Rutkowska A, Zachmann-Brand B, Deuerling E Bukau B (2006) Trigger factor forms a protective shield for nascent polypeptides at the ribosome. J Biol Chem 281, 6539 6545.
46. Vollmer W (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32, 287 306.
47. Jones DD Perham RN (2008) The role of loop and beta-turn residues as structural and functional determinants for the lipoyl domain from the Escherichia coli 2-oxoglutarate dehydrogenase complex. Biochem J 409, 357 366.
48. Mangoni ML, Fiocco D, Mignogna G, Barra D Simmaco M (2003) Functional characterisation of the 1-18 fragment of esculentin-1b, an antimicrobial peptide from Rana esculenta. Peptides 24, 1771 1777.
49. Simmaco M, Mignogna G, Barra D Bossa F (1994) Antimicrobial peptides from skin secretions of Rana esculenta. Molecular cloning of cDNAs encoding esculentin and brevinins and isolation of new active peptides. J Biol Chem 269, 11956 11961.
50. Ponti D, Mangoni ML, Mignogna G, Simmaco M Barra D (2003) An amphibian antimicrobial peptide variant expressed in Nicotiana tabacum confers resistance to phytopathogens. Biochem J 370, 121 127.
51. Hancock RE Rozek A (2002) Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol Lett 206, 143 149.
52. Giuliani A, Pirri G, Bozzi A, Di Giulio A, Aschi M Rinaldi AC (2008) Antimicrobial peptides: natural templates for synthetic membrane-active compounds. Cell Mol Life Sci 65, 2450 2460.
53. Lockhart DJ Winzeler EA (2000) Genomics, gene expression and DNA arrays. Nature 405, 827 836.
54. Bandow JE, Brotz H, Leichert LI, Labischinski H Hecker M (2003) Proteomic approach to understanding antibiotic action. Antimicrob Agents Chemother 47, 948 955.
55. Han MJ Lee SY (2006) The Escherichia coli proteome: past, present, and future prospects. Microbiol Mol Biol Rev 70, 362 439.
56. Chen FY, Lee MT Huang HW (2002) Sigmoidal concentration dependence of antimicrobial peptide activities: a case study on alamethicin. Biophys J 82, 908 914.
57. Gamberi T, Cavalieri D, Magherini F, Mangoni ML, De Filippo C, Borro M, Gentile G, Simmaco M Modesti A (2007) An integrated analysis of the effects of esculentin 1-21 on Saccharomyces cerevisiae. Biochim Biophys Acta 1774, 688 700.
58. Lewis RE, Diekema DJ, Messer SA, Pfaller MA Klepser ME (2002) Comparison of Etest, chequerboard dilution and time-kill studies for the detection of synergy or antagonism between antifungal agents tested against Candida species. J Antimicrob Chemother 49, 345 351.
59. Makovitzki A, Avrahami D Shai Y (2006) Ultrashort antibacterial and antifungal lipopeptides. Proc Natl Acad Sci USA 103, 15997 16002.
60. Matsuzaki K (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes. Biochim Biophys Acta 1462, 1 10.
61. Choi MJ, Kang SH, Kim S, Chang JS, Kim SS, Cho H Lee KH (2004) The interaction of an antimicrobial decapeptide with phospholipid vesicles. Peptides 25, 675 683.
62. Shangguan T, Alford D Bentz J (1996) Influenza-virus-liposome lipid mixing is leaky and largely insensitive to the material properties of the target membrane. Biochemistry 35, 4956 4965.