Effect of natural L- to D-amino acid conversion on the organization, membrane binding, and biological function of the antimicrobial peptides bombinins H

Biochemistry

Volumn 45, Issue 13, 2006, Pages 4266-4276

  Mangoni, Maria Luisa ^a   Papo, Niv ^b   Saugar, José M ^c   Barra, Donatella ^a   Shai, Yechiel ^b   Simmaco, Maurizio ^a   Rivas, Luis ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; BINDING ENERGY; BIOLOGICAL MEMBRANES; BIOLOGICAL ORGANS; MICROORGANISMS; PARAMETER ESTIMATION;

ANTIMICROBIAL PEPTIDES (AMPS); ANTIMICROBIAL PEPTIDES BOMBININS H; INNATE IMMUNITY; MEMBRANE BINDING;

PROTEINS;

AMINO ACID; BOMBININ; BOMBININ H2; BOMBININ H4; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANTIPROTOZOAL ACTIVITY; ARTICLE; BINDING AFFINITY; BOMBINA VARIEGATA; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTRON MICROSCOPY; EPIMERIZATION; FROG; INNATE IMMUNITY; ISOMERIZATION; LEISHMANIA; MEMBRANE DEPOLARIZATION; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; ANTIPROTOZOAL AGENTS; ANURA; CELL MEMBRANE PERMEABILITY; CIRCULAR DICHROISM; LEISHMANIA DONOVANI; LIPID BILAYERS; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; ORGANIC CHEMICALS; PEPTIDES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STEREOISOMERISM; SURFACE PLASMON RESONANCE;

ANIMALIA; ANURA; BACTERIA (MICROORGANISMS); BOMBINA VARIEGATA; MAMMALIA; PROTOZOA;

EID: 33645538062     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052150y     Document Type: Article

References (70)

1. Boman, H. G. (1995) Peptide antibiotics and their role in innate immunity, Annu. Rev. Immun. 13, 61-92.
2. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms, Nature 415, 389-395.
3. Hancock, R. E. W., and Scott, M. G. (2000) The role of antimicrobial peptides in animal defenses, Proc. Natl. Acad. Sci. U.S.A. 97, 8856-8861.
4. Brogden, K. A. (2005) Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250.
5. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides, Biopolymers 66, 236-248.
6. Cudic, M., and Otvos, L., Jr. (2002) Intracellular targets of antibacterial peptides, Curr. Drug Targets 3, 101-106.
7. Avrahami, D., and Shai, Y. (2002) Conjugation of a magainin analogue with lipophilic acids controls hydrophobicity, solution assembly, and cell selectivity, Biochemistry 41, 2254-2263.
8. Chicharro, C., Granata, C., Lozano, R., Andreu, D., and Rivas, L. (2001) N-Terminal fatty acid substitution increases the leishmanicidal activity of CA(1-7)M(2-9), a cecropin-melittin hybrid peptide, Antimicrob. Agents Chemother. 45, 2441-2449.
9. Feder, R., Dagan, A., and Mor, A. (2000) Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerization on selective cytotoxicity, J. Biol. Chem. 275, 4230-4238.
10. Guerrero, E., Saugar, J. M., Matsuzaki, K., and Rivas, L. (2004) Role of positional hydrophobicity in the leishmanicidal activity of magainin 2, Antimicrob. Agents Chemother. 48, 2980-2986.
11. Sal-Man, N., Oren, Z., and Shai, Y. (2002) Preassembly of membrane-active peptides is an important factor in their selectivity toward target cells, Biochemistry 41, 11921-11930.
12. Barra, D., and Simmaco, M. (1995) Amphibian skin: A promising resource for antimicrobial peptides, Trends Biotechnol. 13, 205-209.
13. Bevins, C. L., and Zasloff, M. (1990) Peptides from frog skin, Annu. Rev. Biochem. 59, 395-414.
14. Nicolas, P., and Mor, A. (1995) Peptides as weapons against microorganisms in the chemical defense system of vertebrates, Annu. Rev. Microbiol. 49, 277-304.
15. Mangoni, M. L., Miele, R., Renda, T. G., Barra, D., and Simmaco, M. (2001) The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms, FASEB J. 15, 1431-1432
16. Gibson, B. W., Tang, D. Z., Mandrell, R., Kelly, M., and Spindel, E. R. (1991) Bombinin-like peptides with antimicrobial activity from skin scretions of the Asian toad, Bombina orientalis, J. Biol. Chem. 266, 23103-23111.
17. Simmaco, M., Barra, D., Chiarini, F., Noviello, L., Melchiorri, P., Kreil, G., and Richter, K. (1991) A family of bombinin-related peptides from the skin of Bombina variegata, Eur. J. Biochem. 199, 217-222.
18. Mignogna, G., Simmaco, M., Kreil, G., and Barra, D. (1993) Antibacterial and haemolytic peptides containing D-alloisoleucine from the skin of Bombina variegata, EMBO J. 12, 4829-4832.
19. Kreil, G. (1997) D-Amino acids in animal peptides, Annu. Rev. Biochem. 66, 337-345.
20. Mor, A., Amiche, M., and Nicolas, P. (1992) Enter a new posttranslational modification: D-Amino acids in gene-encoded peptides, Trends Biochem. Sci. 17, 481-485.
21. Jilek, A., Mollay, C., Tippelt, C., Grassi, J., Mignogna, G., Mullegger, J., Sander, V., Fehrer, C., Barra, D., and Kreil, G. (2005) Biosynthesis of a D-amino acid in peptide linkage by an enzyme from frog skin secretions, Proc. Natl. Acad. Sci. U.S.A. 102, 4235-4239.
22. Mangoni, M. L., Grovale, N., Giorgi, A., Mignogna, G., Simmaco, M., and Barra, D. (2000) Structure-function relationships in bombinins H, antimicrobial peptides from Bombina skin secretions, Peptides 21, 1673-1679.
23. Berman, J. (2005) Recent developments in leishmaniasis: Epidemiology, diagnosis, and treatment, Curr. Infect. Dis. Rep. 7, 33-38.
24. Croft, S. L., and Coombs, G. H. (2003) Leishmaniasis: Current chemotherapy and recent advances in the search for novel drugs, Trends Parasitol. 19, 502-558.
25. Guerin, P. J., Olliaro, P., Sundar, S., Boelaert, M., Croft, S. L., Desjeux, P., Wasunna, M. K., and Bryceson, A. D. (2002) Visceral leishmaniasis: Current status of control, diagnosis, and treatment, and a proposed research and development agenda, Lancet Infect. Dis. 2, 494-501.
26. Gull, K. (1999) The cytoskeleton of trypanosomatid parasites, Annu. Rev. Microbiol. 53, 629-655.
27. McConville, M. J., Mullin, K. A., Ilgoutz, S. C., and Teasdale, R. D. (2002) Secretory pathway of trypanosomatid parasites, Microbiol. Mol. Biol. Rev. 66, 122-154.
28. Ilgoutz, S. C., and McConville, M. J. (2001) Function and assembly of the Leishmania surface coat, Int. J. Parasitol. 31, 899-908.
29. Diaz-Achirica, P., Ubach, J., Guinea, A., Andreu, D., and Rivas, L. (1998) The plasma membrane of Leishmania donovani promastigotes is the main target for CA(1-8)M(1-18), a synthetic cecropin A-melittin hybrid peptide, Biochem. J. 330, 453-460.
30. Mangoni, M. L., Rinaldi, A. C., Di Giulio, A., Mignogna, G., Bozzi, A., Barra, D., and Simmaco, M. (2000) Structure-function relationships of temporins, small antimicrobial peptides from amphibian skin, Eur. J. Biochem. 267, 1447-1454.
31. Papo, N., and Shai, Y. (2003) Exploring peptide membrane interaction using surface plasmon resonance: Differentiation between pore formation versus membrane disruption by lytic peptides, Biochemistry 42, 458-466.
32. King, D. L., and Turco, S. J. (1988) A ricin agglutinin-resistant clone of Leishmania donovani deficient in lipophosphoglycan, Mol. Biochem. Parasitol. 28, 285-293.
33. Pan, A. A., McMahon-Pratt, D., and Honigberg, B. M. (1984) Leishmania mexicana pifanoi: Antigenic characterization of promastigote and amastigote stages by solid-phase radioimmunoassay, J. Parasitol. 70, 834-835.
34. Hanks, W. J. (1958) Determination of cell viability, Proc. Soc. Biol. Med. 98, 188-192.
35. Mangoni, M. L., Saugar, J. M., Dellisanti, M., Barra, D., Simmaco, M., and Rivas, L. (2005) Temporins, small antimicrobial peptides with leishmanicidal activity, J. Biol. Chem. 280, 984-990.
36. Oren, Z., and Shai, Y. (2000) Cyclization of a cytolytic amphipathic α-helical peptide and its diastereomer: Effect on structure, interaction with model membranes, and biological function, Biochemistry 39, 6103-6114.
37. Surewicz, W. K., Manisch, H. H., and Chapman, D. (1993) Determination of protein secondary structure by Fourier transform infrared spectroscopy: A critical assessment, Biochemistry 32, 389-394.
38. Harrick, N. J. (1967) Internal Reflection Spectroscopy, Interscience, New York.
39. Ishiguro, R., Kimura, N., and Takahashi, S. (1993) Orientation of fusion-active synthetic peptides in phospholipid bilayers: Determination by Fourier transform infrared spectroscopy, Biochemistry 32, 9792-9797.
40. Brumfeld, V., and Miller, I. R. (1988) Effect of membrane potential on the conformation of bacterorhodopsin reconstituted in lipid vesicles, Biophys. J. 54, 747-750.
41. Erb, E. M., Chen, X., Allen, S., Roberts, C. J., Tendler, S. J., Davies, M. C., and Forsen, S. (2000) Characterization of the surfaces generated by liposome binding to the modified dextran matrix of a surface plasmon resonance sensor chip, Anal. Biochem. 280, 29-35.
42. Cooper, M. A., Hansson, A., Lofas, S., and Williams, D. H. (2000) A vesicle capture sensor chip for kinetic analysis of interactions with membrane-bound receptors, Anal. Biochem. 277, 196-205.
43. Mozsolits, H., Wirth, H. J., Werkmeister, J., and Aguilar, M. I. (2001) Analysis of antimicrobial peptide interactions with hybrid bilayer membrane systems using surface plasmon resonance, Biochim. Biophys. Acta 1512, 64-76.
44. Morton, T. A., Myszka, D. G., and Chaiken, I. M. (1995) Interpreting complex binding kinetics from optical biosensors: A comparison of analysis by linearization, the integrated rate equation, and numerical integration, Anal. Biochem. 227, 176-185.
45. Turco, S. J., Hull, S. R., Orlandi, P. A., Jr., Shepherd, S. D., Homans, S. W., Dwek, R. A., and Rademacher, T. W. (1987) Structure of the major carbohydrate fragment of the Leishmania donovani lipophosphoglycan, Biochemistry 26, 6233-6238.
46. Wassef, M. K., Fioretti, T. B., and Dwyer, D. M. (1985) Lipid analyses of isolated surface membranes of Leishmania donovani promastigotes, Lipids 20, 108-115.
47. Byler, D. M., and Susi, H. (1986) Examination of the secondary structure of proteins by deconvolved Fourier transform infrared spectroscopy, Biopolymers 25, 469-487.
48. Jackson, M., and Manisch, H. H. (1995) The use and misuse of FTIR spectroscopy in the determination of protein structure, Crit. Rev. Biochem. Mol. Biol. 30, 95-120.
49. Frey, S., and Tamm, L. K. (1991) Orientation of melittin in phospholipid bilayers. A polarized attenuated total reflection infrared study, Biophys. J. 60, 922-930.
50. Pezolet, M., Bonenfant, S., Dousscau, F., and Papineau, Y. (1992) Conformation of wheat gluten proteins. Comparison between functional and solution states as determined by infrared spectroscopy, FEBS Lett. 299, 247-250.
51. Oren, Z., Hong, J., and Shai, Y. (1999) A comparative study on the structure and function of a cytolytic β-helical peptide and its antimicrobial β-sheet diastereomer, Eur. J. Biochem. 259, 360-369.
52. Hong, J., Oren, Z., and Shai, Y. (1999) The structure and organization of hemolytic and nonhemolytic diastereomers of antimicrobial peptides in membranes, Biochemistry 38, 16963-16973.
53. Sharon, M., Oren, Z., Shai, Y., and Anglister, J. (1999) 2D-NMR and ATR-FTIR study of the structure of a cell-selective diastereomer of melittin and its orientation in phospholipids, Biochemistry 38, 15305-15316.
54. Montecucchi, P. C., de Castiglione, R., Piani, S., Gozzini, L., and Erspamer, V. (1981) Amino acid composition and sequence of dermorphin, a novel opiate-like peptide from the skin of Phyllomedusa sauvagei, Int. J. Pept. Protein Res. 17, 275-283.
55. Erspamer, V., Melchiorri, P., Falconieri-Erspamer, G., Negri, L., Corsi, R., Severini, C., Barra, D., Simmaco, M., and Kreil, G. (1989) Deltorphins: A family of naturally occurring peptides with high affinity and selectivity for delta opioid binding sites, Proc. Natl. Acad. Sci. U.S.A. 86, 5188-5192.
56. Kamatani, Y., Minakata, H., Kenny, P. T., Iwashita, T., Watanabe, K., Funase, K., Sun, X. P., Yongsiri, A., Kim, K. H., Novales-Li, P., et al. (1989) Achatin-I, an endogenous neuroexcitatory tetrapeptide from Achatina fulica Ferussac containing a D-amino acid residue, Biochem. Biophys. Res. Commun. 160, 1015-1020.
57. Buczek, O., Yoshikami, D., Bulaj, G., Jimenez, E. C., and Olivera, B. M. (2005) Post-translational amino acid isomerization: A functionally important D-amino acid in an excitatory peptide, J. Biol. Chem. 280, 4247-4253.
58. Kuwada, M., Teramoto, T., Kumagaye, K. Y., Nakajima, K., Watanabe, T., Kawai, T., Kawakami, Y., Niidome, T., Sawada, K., Nishizawa, Y., et al. (1994) ω-Agatoxin-TK containing D-serine at position 46, but not synthetic ω-[L-Ser46]agatoxin-TK, exerts blockade of P-type calcium channels in cerebellar Purkinje neurons, Mol. Pharmacol. 46, 587-593.
59. Torres, A. M., Menz, I., Alewood, P. F., Bansal, P., Lahnstein, J., Gallagher, C. H., and Kuchel, P. W. (2002) D-Amino acid residue in the C-type natriuretic peptide from the venom of the mammal, Ornithorhynchus anatinus, the Australian platypus, FEBS Lett. 524, 172-176.
60. Mignogna, G., Simmaco, M., and Barra, D. (1998) Occurrence and function of D-amino acid-containing peptides and proteins: Antimicrobial peptides, EXS 85, 29-36.
61. Hernandez, C., Mor, A., Dagger, F., Nicolas, P., Hernandez, A., Benedetti, E. L., and Dunia, I. (1992) Functional and structural damage in Leishmania mexicana exposed to the cationic peptide dermaseptin, Eur. J. Cell Biol. 59, 414-424.
62. Silva, P. I., Jr., Daffre, S., and Bulet, P. (2000) Isolation and characterization of gomesin, an 18-residue cysteine-rich defense peptide from the spider Acanthoscurria gomesiana hemocytes with sequence similarities to horseshoe crab antimicrobial peptides of the tachyplesin family, J. Biol. Chem. 275, 33464-33470.
63. Papo, N., Oren, Z., Pag, U., Sahl, H. G., and Shai, Y. (2002) The consequence of sequence alteration of an amphipathic α-helical antimicrobial peptide and its diastereomers, J. Biol. Chem. 277, 33913-33921.
64. Hong, S. Y., Oh, J. E., and Lee, K. H. (1999) Effect of D-amino acid substitution on the stability, the secondary structure, and the activity of membrane-active peptide, Biochem. Pharmacol. 58, 1775-1780.
65. Braunstein, A., Papo, N., and Shai, Y. (2004) In vitro activity and potency of an intravenously injected antimicrobial peptide and its DL amino acid analog in mice infected with bacteria, Antimicrob. Agents Chemother. 48, 3127-3129.
66. Mottram, J. C., Coombs, G. H., and Alexander, J. (2004) Cysteine peptidases as virulence factors of Leishmania, Curr. Opin. Microbiol. 7, 375-381.
67. Morty, R. E., and Morehead, J. (2002) Cloning and characterization of a leucyl aminopeptidase from three pathogenic Leishmania species, J. Biol. Chem. 277, 26057-26065.
68. Yao, C., Donelson, J. E., and Wilson, M. E. (2003) The major surface protease (MSP or GP63) of Leishmania sp. Biosynthesis, regulation of expression, and function, Mol. Biochem. Parasitol. 132, 1-16.
69. Holak, T. A., Engstrom, A., Kraulis, P. J., Lindeberg, G., Bennich, H., Jones, T. A., Gronenborn, A. M., and Clore, G. M. (1988) The solution conformation of the antibacterial peptide cecropin A: A nuclear magnetic resonance and dynamical simulated annealing study, Biochemistry 27, 7620-7629.
70. Tripathi, A., and Gupta, C. M. (2003) Transbilayer translocation of membrane phosphatidylserine and its role in macrophage invasion in Leishmania promastigotes, Mol. Biochem. Parasitol. 128, 1-9.