Enhanced leishmanicidal activity of cryptopeptide chimeras from the active N1 domain of bovine lactoferrin

Amino Acids

Volumn 43, Issue 6, 2012, Pages 2265-2277

  Silva, Tania ^a   Abengózar, Maria Angeles ^b   Fernandez Reyes, Maria ^b   Andreu, David ^c   Nazmi, Kamran ^b,d   Bolscher, Jan G M ^b,d   Bastos, Margarida ^a   Rivas, Luis ^b  

^a UNIVERSITY OF PORTO   (Portugal)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Antimicrobial peptides; Lactoferrampin; Lactoferricin; Leishmania; Leishmanicidal activity; LFchimera; Membrane permeabilization

Indexed keywords

LACTOFERRAMPIN; LACTOFERRICIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

AMASTIGOTE; ANTIPROTOZOAL ACTIVITY; ARTICLE; BIOENERGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOFLUOROMETRY; DRUG ACTIVITY; DRUG STRUCTURE; LEISHMANIA DONOVANI; LEISHMANIA PIFANOI; LEISHMANICIDAL ACTIVITY; LUMINESCENCE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN SYNTHESIS; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANTIPROTOZOAL AGENTS; CATTLE; DOSE-RESPONSE RELATIONSHIP, DRUG; LACTOFERRIN; LEISHMANIA DONOVANI; MODELS, MOLECULAR; PARASITIC SENSITIVITY TESTS; PEPTIDE FRAGMENTS; STRUCTURE-ACTIVITY RELATIONSHIP;

BOVINAE; LEISHMANIA DONOVANI; LEISHMANIA PIFANOI; PROTOZOA;

EID: 84872683954     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-012-1304-0     Document Type: Article

References (68)

1. Adao R, Nazmi K, Bolscher JG, Bastos M (2011) C-And N-truncated antimicrobial peptides from LFampin 265-284: biophysical versus microbiology results. J Pharm Bioallied Sci 3:60-69. doi:10.4103/0975-7406.76467
2. Aguilera O, Ostolaza H, Quiros LM, Fierro JF (1999) Permeabilizing action of an antimicrobial lactoferricin-derived peptide on bacterial and artificial membranes. FEBS Lett 462:273-277. doi:10.1016/S0014-5793(99)01545-8
3. Bastos M, Bai G, Gomes P, Andreu D, Goormaghtigh E, Prieto M (2008) Energetics and partition of two cecropin-melittin hybrid peptides to model membranes of different composition. Biophys J 94:2128-2141. doi:10.1529/ biophysj.107.119032
4. BolscherJG,AdaoR,Nazmi K, van den KeybusPA, van'tHofW,Nieuw Amerongen AV, Bastos M, Veerman EC (2009) Bactericidal activity of LFchimera is stronger and less sensitive to ionic strength than its constituent lactoferricin and lactoferrampin peptides. Biochimie 91:123-132. doi:10.1016/j.biochi.2008.05.019
5. Bolscher JG, Oudhoff MJ, Nazmi K, Antos JM, Guimaraes CP, Spooner E, Haney EF, Vallejo JJ, Vogel HJ, van't Hof W, Ploegh HL, Veerman EC (2011) Sortase A as a tool for highyield histatin cyclization. FASEB J 25:2650-2658. doi: 10.1096/fj.11-182212
6. Bolscher J, Nazmi K, van Marle J, van't Hof W, Veerman E (2012) Chimerization of lactoferricin and lactoferrampin peptides strongly potentiates the killing activity against Candida albicans. Biochem Cell Biol. doi:10.1139/o11-085
7. Boman HG, Wade D, Boman IA, Wahlin B, Merrifield RB (1989) Antibacterial and antimalarial properties of peptides that are cecropin-melittin hybrids. FEBS Lett 259:103-106. doi: 10.1016/0014-5793(89)81505-4 (Pubitemid 20009957)
8. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238-250. doi: 10.1038/nrmicro1098 (Pubitemid 40298223)
9. Castanho MARB (ed) (2010) Membrane-Active peptides: methods and results on structure and function, vol 9. IUL biotechnology series. International University Line
10. La Jolla Chan DI, Prenner EJ, Vogel HJ (2006) Tryptophan-And arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim Biophys Acta 1758:1184-1202. doi:10.1016/j.bbamem. 2006.04.006 (Pubitemid 44444830)
11. Chicharro C, Granata C, Lozano R, Andreu D, 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. doi:10.1128/AAC.45.9.2441-2449.2001 (Pubitemid 32801893)
12. Cho JH, Sung BH, Kim SC (2009) Buforins: histone H2A-derived antimicrobial peptides from toad stomach. Biochim Biophys Acta 1788:1564-1569. doi:10.1016/j.bbamem.2008.10.025
13. Cobb SL, Denny PW (2010) Antimicrobial peptides for leishmaniasis. Curr Opin Investig Drugs 11:868-875
14. Fernandez-Reyes M, D?az D, de la Torre BG, Cabrales-Rico A, Valles-Miret M, Jimenez-Barbero J, Andreu D, Rivas L (2010) Lysine Ne-trimethylation, a tool for improving the selectivity of antimicrobial peptides. J Med Chem 53:5587-5596. doi:10.1021/jm100261r
15. Fink J, Merrifield RB, Boman A, Boman HG (1989) The chemical synthesis of cecropin D and an analog with enhanced antibacterial activity. J Biol Chem 264:6260-6267 (Pubitemid 19106701)
16. Fjell CD, Hiss JA, Hancock RE, Schneider G (2011) Designing antimicrobial peptides: form follows function. Nat Rev Drug Discov 11:37-51. doi:10.1038/nrd3591
17. Flores-Villasenor H, Canizalez-Roman A, Reyes-Lopez M, Nazmi K, de la Garza M, Zazueta-Beltran J, Leon-Sicairos N, Bolscher JG (2010) Bactericidal effect of bovine lactoferrin, LFcin, LFampin and LFchimera on antibiotic-resistant Staphylococcus aureus and Escherichia coli. Biometals 23:569-578. doi:10.1007/s10534-010-9306-4
18. Gifford JL, Hunter HN, Vogel HJ (2005) Lactoferricin: A lactoferrinderived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol Life Sci 62:2588-2598. doi: 10.1007/s00018-005-5373-z (Pubitemid 41721232)
19. Groenink J, Walgreen-Weterings E, van't Hof W, Veerman EC, Nieuw Amerongen AV (1999) Cationic amphipathic peptides, derived from bovine and human lactoferrins, with antimicrobial activity against oral pathogens. FEMS Microbiol Lett 179: 217-222. doi:10.1111/j.1574-6968.1999.tb08730.x (Pubitemid 29461640)
20. Guerrero E, Saugar JM, Matsuzaki K, Rivas L (2004) Role of positional hydrophobicity in the leishmanicidal activity of magainin 2. Antimicrob Agents Chemother 48:2980-2986. doi:10.1128/AAC.48.8.2980-2986.2004 (Pubitemid 38989164)
21. Hancock RE, Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24:1551-1557. doi:10.1038/nbt1267 (Pubitemid 44967479)
22. Haney EF, Nazmi K, Lau F, Bolscher JG, Vogel HJ (2009) Novel lactoferrampin antimicrobial peptides derived from human lactoferrin. Biochimie 91:141-154. doi:10.1016/j.biochi.2008. 04.013
23. Haney EF, Nazmi K, Bolscher JG, Vogel HJ (2012) Structural and biophysical characterization of an antimicrobial peptide chimera comprised of lactoferricin and lactoferrampin. Biochim Biophys Acta 1818:762-775. doi:10.1016/j.bbamem.2011.11.023
24. Haukland HH, Ulvatne H, Sandvik K, Vorland LH (2001) The antimicrobial peptides lactoferricin B and magainin 2 cross over the bacterial cytoplasmic membrane and reside in the cytoplasm. FEBS Lett 508:389-393. doi:10.1016/S0014-5793(01)03100-3 (Pubitemid 33135477)
25. Henriques ST, Melo MN, Castanho MA (2006) Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem J 399:1-7. doi:10.1042/BJ20061100 (Pubitemid 44505401)
26. Ibrahim HR, Aoki T, Pellegrini A (2002) Strategies for new antimicrobial proteins and peptides: lysozyme and aprotinin as model molecules. Curr Pharm Des 8:671-693. doi:10.2174/1381612023395349 (Pubitemid 34498558)
27. Ilgoutz SC, McConville MJ (2001) Function and assembly of the Leishmania surface coat. Int J Parasitol 31:899-908. doi: 10.1016/s0020-7519(01)00197-7 (Pubitemid 32530624)
28. Jenssen H, Hancock RE (2009) Antimicrobial properties of lactoferrin. Biochimie 91:19-29. doi:10.1016/j.biochi.2008.05.015
29. Kima PE (2007) The amastigote forms of Leishmania are experts at exploiting host cell processes to establish infection and persist. Int J Parasitol 37:1087-1096. doi:10.1016/j.ijpara.2007.04.007 (Pubitemid 47042032)
30. Kuwata H, Yip TT, Tomita M, Hutchens TW (1998) Direct evidence of the generation in human stomach of an antimicrobial peptide domain (lactoferricin) from ingested lactoferrin. Biochim Biophys Acta 1429:129-141. doi:10.1016/S0167-4838(98)00224-6 (Pubitemid 29052216)
31. Landon C, Barbault F, Legrain M, Guenneugues M, Vovelle F (2008) Rational design of peptides active against the gram positive bacteria Staphylococcus aureus. Proteins 72:229-239. doi: 10.1002/prot.21912 (Pubitemid 351809161)
32. Leon-Sicairos N, Reyes-Lopez M, Ordaz-Pichardo C, de la Garza M (2006) Microbicidal action of lactoferrin and lactoferricin and their synergistic effect with metronidazole in Entamoeba histolytica. Biochem Cell Biol 84:327-336. doi:10.1139/o06-060 (Pubitemid 44341307)
33. Leon-Sicairos N, Canizalez-Roman A, de la Garza M, Reyes-Lopez M, Zazueta-Beltran J, Nazmi K, Gomez-Gil B, Bolscher JG (2009) Bactericidal effect of lactoferrin and lactoferrin chimera against halophilic Vibrio parahaemolyticus. Biochimie 91:133-140. doi: 10.1016/j.biochi.2008.06.009
34. Lohner K (2009) New strategies for novel antibiotics: peptides targeting bacterial cell membranes. Gen Physiol Biophys 28:105-116. doi:10.4149/gpb-2009- 02-105
35. Lohner K, Blondelle SE (2005) Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics. Comb Chem High Throughput Screen 8:241-256 (Pubitemid 40488604)
36. Lopez-Soto F, Leon-Sicairos N, Nazmi K, Bolscher JG, de la Garza M (2010) Microbicidal effect of the lactoferrin peptides lactoferricin17-30, lactoferrampin265-284, and lactoferrin chimera on the parasite Entamoeba histolytica. Biometals 23:563-568. doi: 10.1007/s10534-010-9295-3
37. Luque-Ortega JR, Rivas L (2010) Characterization of the leishmanicidal activity of antimicrobial peptides. Methods Mol Biol 618:393-420. doi:10.1007/978-1-60761-594-1-25
38. Luque-Ortega JR, Saugar JM, Chiva C, Andreu D, Rivas L (2003) Identification of new leishmanicidal peptide lead structures by automated real-time monitoring of changes in intracellular ATP. Biochem J 375:221-230. doi:10.1042/bj20030544 (Pubitemid 37255399)
39. Luque-Ortega JR, van't Hof W, Veerman EC, Saugar JM, Rivas L (2008) Human antimicrobial peptide histatin 5 is a cellpenetrating peptide targeting mitochondrial ATP synthesis in Leishmania. FASEB J 22:1817-1828. doi:10.1096/fj.07-096081 (Pubitemid 351811459)
40. Mader JS, Richardson A, Salsman J, Top D, de Antueno R, Duncan R, Hoskin DW (2007) Bovine lactoferricin causes apoptosis in Jurkat T-leukemia cells by sequential permeabilization of the cell membrane and targeting of mitochondria. Exp Cell Res 313:2634-2650. doi:10.1016/j.yexcr.2007.05.015 (Pubitemid 46977347)
41. Mak P, Siwek M, Pohl J, Dubin A (2007) Menstrual hemocidin HbB115-146 is an acidophilic antibacterial peptide potentiating the activity of human defensins, cathelicidin and lysozyme. Am J Reprod Immunol 57:81-91. doi:10.1111/j.1600-0897.2006. 00456.x (Pubitemid 44911609)
42. McConville MJ, Ralton JE (1997) Developmentally regulated changes in the cell surface architecture of Leishmania parasites. Behring Inst Mitt (99):34-43
43. Merrifield RB, Merrifield EL, Juvvadi P, Andreu D, Boman HG (1994) Design and synthesis of antimicrobial peptides. Ciba Found Symp 186:5-20 (discussion 20-26)
44. Nguyen LT, Haney EF, Vogel HJ (2011) The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol 29:464-472. doi:10.1016/j.tibtech.2011.05.001
45. Omata Y, Satake M, Maeda R, Saito A, Shimazaki K, Yamauchi K, Uzuka Y, Tanabe S, Sarashina T, Mikami T (2001) Reduction of the infectivity of Toxoplasma gondii and Eimeria stiedai sporozoites by treatment with bovine lactoferricin. J Vet Med Sci 63:187-190. doi:10.1292/jvms.63.187 (Pubitemid 33674513)
46. Oo TZ, Cole N, Garthwaite L, Willcox MD, Zhu H (2010) Evaluation of synergistic activity of bovine lactoferricin with antibiotics in corneal infection. J Antimicrob Chemother 65:1243-1251. doi: 10.1093/jac/dkq106
47. Pellegrini A (2003) Antimicrobial peptides from food proteins. Curr Pharm Des 9:1225-1238 (Pubitemid 36592133)
48. Reddy KV, Yedery RD, Aranha C (2004) Antimicrobial peptides: premises and promises. Int J Antimicrob Agents 24:536-547. doi:10.1016/j.ijantimicag.2004. 09.005 (Pubitemid 39536106)
49. Rivas L, Luque-Ortega JR, Andreu D (2009) Amphibian antimicrobial peptides and protozoa: lessons from parasites. Biochim Biophys Acta 1788:1570-1581. doi:10.1016/j.bbamem.2008.11.002
50. Sanchez-Gomez S, Japelj B, Jerala R, Moriyon I, Fernandez Alonso M, Leiva J, Blondelle SE, Andra J, Brandenburg K, Lohner K, Mart?nez de Tejada G (2011) Structural features governing the activity of lactoferricin-derived peptides that act in synergy with antibiotics against Pseudomonas aeruginosa in vitro and in vivo. Antimicrob Agents Chemother 55:218-228. doi:10.1128/aac. 00904-10
51. Schmitt MA, Weisblum B, Gellman SH (2007) Interplay among folding, sequence, and lipophilicity in the antibacterial and hemolytic activities of a/b-peptides. J Am Chem Soc 129:417-428. doi:10.1021/ja0666553 (Pubitemid 46106642)
52. Shin SY, Kang JH, Lee MK, Kim SY, Kim Y, Hahm KS (1998) Cecropin A-magainin 2 hybrid peptides having potent antimicrobial activity with low hemolytic effect. Biochem Mol Biol Int 44:1119-1126. doi:10.1080/ 15216549800202192 (Pubitemid 28246144)
53. Tachi T, Epand RF, Epand RM, Matsuzaki K (2002) Positiondependent hydrophobicity of the antimicrobial magainin peptide affects the mode of peptide-lipid interactions and selective toxicity. Biochemistry 41:10723-10731. doi:10.1021/bi0256983 (Pubitemid 34913333)
54. Teixeira V, Feio MJ, Rivas L, De la Torre BG, Andreu D, Coutinho A, Bastos M (2010) Influence of lysine Ne-trimethylation and lipid composition on the membrane activity of the cecropin a-melittin hybrid peptide CA(1-7)M(2-9). J Phys Chem B 114:16198-16208. doi:10.1021/jp106915c
55. Teixeira V, Feio MJ, Bastos M (2012) Role of lipids in the interaction of antimicrobial peptides with membranes. Prog Lipid Res 51:149-177. doi:10.1016/j.plipres.2011.12.005
56. Turchany JM, Aley SB, Gillin FD (1995) Giardicidal activity of lactoferrin and N-terminal peptides. Infect Immun 63:4550-4552
57. Ulvatne H, Haukland HH, Olsvik O, Vorland LH (2001) Lactoferricin B causes depolarization of the cytoplasmic membrane of Escherichia coli ATCC 25922 and fusion of negatively charged liposomes. FEBS Lett 492:62-65. doi:10.1016/S0014-5793 (01)02233-5 (Pubitemid 32206721)
58. van der Kraan MI, Groenink J, Nazmi K, Veerman EC, Bolscher JG, Nieuw Amerongen AV (2004) Lactoferrampin: A novel antimicrobial peptide in the N1-domain of bovine lactoferrin. Peptides 25:177-183. doi:10.1016/j.peptides. 2003.12.006 (Pubitemid 38520047)
59. van der Kraan MI, Nazmi K, Teeken A, Groenink J, van't Hof W, Veerman EC, Bolscher JG, Nieuw Amerongen AV (2005a) Lactoferrampin, an antimicrobial peptide of bovine lactoferrin, exerts its candidacidal activity by a cluster of positively charged residues at the C-terminus in combination with a helix-facilitating N-terminal part. Biol Chem 386:137-142. doi:10.1515/BC. 2005.017 (Pubitemid 40361439)
60. van der Kraan MI, van Marle J, Nazmi K, Groenink J, van't Hof W, Veerman EC, Bolscher JG, Nieuw Amerongen AV (2005b) Ultrastructural effects of antimicrobial peptides from bovine lactoferrin on the membranes of Candida albicans and Escherichia coli. Peptides 26:1537-1542. doi:10.1016/j.peptides. 2005.02.011 (Pubitemid 41169745)
61. van der Kraan MI, Nazmi K, van't Hof W, Amerongen AV, Veerman EC, Bolscher JG (2006) Distinct bactericidal activities of bovine lactoferrin peptides LFampin 268-284 and LFampin 265-284: Asp-Leu-Ile makes a difference. Biochem Cell Biol 84:358-362. doi:10.1139/o06-042 (Pubitemid 44341311)
62. Wade D, Flock JI, Edlund C, Lofving-Arvholm I, Sallberg M, Bergman T, Silveira A, Unson C, Rollins-Smith L, Silberring J, Richardson M, Kuusela P, Lankinen H (2002) Antibiotic properties of novel synthetic temporin A analogs and a cecropin A-temporin A hybrid peptide. Protein Pept Lett 9:533-543 (Pubitemid 36264203)
63. Wang Y, Chen Y, Xin L, Beverley SM, Carlsen ED, Popov V, Chang KP, Wang M, Soong L (2011) Differential microbicidal effects of human histone proteins H2A and H2B on Leishmania promastigotes and amastigotes. Infect Immun 79:1124-1133. doi:10.1128/IAI.00658-10
64. Wassef MK, Fioretti TB, Dwyer DM (1985) Lipid analyses of isolated surface membranes of Leishmania donovani promastigotes. Lipids 20:108-115. doi:10.1007/BF02534216
65. WHO (2010) Control of the leishmaniases: report of a meeting of the WHO Expert Committee on the control of leishmaniases, Geneva, 22-26 March 2010.
66. WHO Technical Report Series, No. 949. World Health Organization, Geneva
67. Yamauchi K, Tomita M, Giehl TJ, Ellison RT (1993) Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect Immun 61:719-728 (Pubitemid 23030865)
68. Yeung AT, Gellatly SL, Hancock RE (2011) Multifunctional cationic host defence peptides and their clinical applications. Cell Mol Life Sci 68:2161-2176. doi:10.1007/s00018-011-0710-x