Effect of BMAP-28 antimicrobial peptides on Leishmania major promastigote and amastigote growth: Role of leishmanolysin in parasite survival

PLoS Neglected Tropical Diseases

Volumn 5, Issue 5, 2011, Pages

  Lynn, Miriam A ^a   Kindrachuk, Jason ^b   Marr, Alexandra K ^a   Jenssen, Håvard ^b,c   Panté, Nelly ^b   Elliott, Melissa R ^b   Napper, Scott ^d,e   Hancock, Robert E ^b   McMaster, W Robert ^a  

^a VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c ROSKILDE UNIVERSITY   (Denmark)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

^e UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE MYELOID ANTIMICROBIAL PEPTIDE 28; DEXTRO BOVINE MYELOID ANTIMICROBIAL PEPTIDE 28; LEISHMANOLYSIN; MEMBRANE PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; RETRO INVERSO BOVINE MYELOID ANTIMICROBIAL PEPTIDE 28; UNCLASSIFIED DRUG; ANTIPROTOZOAL AGENT; BMAP 28; BMAP-28; GLYCOPROTEIN GP63, LEISHMANIA; METALLOPROTEINASE; PROTEIN;

AMASTIGOTE; ANIMAL CELL; ANIMAL TISSUE; ANTIPROTOZOAL ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL DISRUPTION; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CONTROLLED STUDY; CYTOLYSIS; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG SCREENING; IMMUNOMODULATION; IN VITRO STUDY; LEISHMANIA MAJOR; MOUSE; NONHUMAN; OSMOSIS; PARASITE SURVIVAL; PROMASTIGOTE; PROTEIN FUNCTION; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; ISOMERISM; MACROPHAGE; METABOLISM; MICROBIAL VIABILITY; PARASITOLOGY; PHYSIOLOGY;

ANIMALS; ANTIPROTOZOAL AGENTS; APOPTOSIS; HUMANS; ISOMERISM; LEISHMANIA MAJOR; MACROPHAGES; METALLOENDOPEPTIDASES; MICE; MICE, INBRED BALB C; MICROBIAL VIABILITY; PROTEINS;

EID: 79958002329     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001141     Document Type: Article

References (60)

1. McConville MJ, Handman E, (2007) The molecular basis of Leishmania pathogenesis. Int J Parasitol 37: 1047-1051.
2. Marsden PD, (1986) Mucosal leishmaniasis ("espundia" Escomel, 1911). Trans R Soc Trop Med Hyg 80: 859-876.
3. Sacks D, Anderson C, (2004) Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol Rev 201: 225-238.
4. Besteiro S, Williams RA, Coombs GH, Mottram JC, (2007) Protein turnover and differentiation in Leishmania. Int J Parasitol 37: 1063-1075.
5. Chakravarty J, Sundar S, (2010) Drug Resistance in Leishmaniasis. J Glob Infect Dis 2: 167-176.
6. Kuckelhaus SA, Leite JR, Muniz-Junqueira MI, Sampaio RN, Bloch C Jr, et al. (2009) Antiplasmodial and antileishmanial activities of phylloseptin-1, an antimicrobial peptide from the skin secretion of Phyllomedusa azurea (Amphibia). Exp Parasitol 123: 11-16.
7. Croft SL, Yardley V, (2002) Chemotherapy of leishmaniasis. Curr Pharm Des 8: 319-342.
8. Subbalakshmi C, Sitaram N, (1998) Mechanism of antimicrobial action of indolicidin. FEMS Microbiol Lett 160: 91-96.
9. 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.
10. Otvos L Jr, O I, Rogers ME, Consolvo PJ, Condie BA, et al. (2000) Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 39: 14150-14159.
11. Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R, et al. (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40: 3016-3026.
12. 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.
13. Bowdish DM, Davidson DJ, Scott MG, Hancock RE, (2005) Immunomodulatory activities of small host defense peptides. Antimicrob Agents Chemother 49: 1727-1732.
14. Heilborn JD, Nilsson MF, Kratz G, Weber G, Sorensen O, et al. (2003) The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol 120: 379-389.
15. Rehaume LM, Hancock RE, (2008) Neutrophil-derived defensins as modulators of innate immune function. Crit Rev Immunol 28: 185-200.
16. Mookherjee N, Hancock RE, (2007) Cationic host defence peptides: innate immune regulatory peptides as a novel approach for treating infections. Cell Mol Life Sci 64: 922-933.
17. Mookherjee N, Wilson HL, Doria S, Popowych Y, Falsafi R, et al. (2006) Bovine and human cathelicidin cationic host defense peptides similarly suppress transcriptional responses to bacterial lipopolysaccharide. J Leukoc Biol 80: 1563-1574.
18. Cirioni O, Giacometti A, Ghiselli R, Bergnach C, Orlando F, et al. (2006) LL-37 protects rats against lethal sepsis caused by gram-negative bacteria. Antimicrob Agents Chemother 50: 1672-1679.
19. Haines LR, Thomas JM, Jackson AM, Eyford BA, Razavi M, et al. (2009) Killing of trypanosomatid parasites by a modified bovine host defense peptide, BMAP-18. PLoS Negl Trop Dis 3: e373.
20. Kulkarni MM, McMaster WR, Kamysz E, Kamysz W, Engman DM, et al. (2006) The major surface-metalloprotease of the parasitic protozoan, Leishmania, protects against antimicrobial peptide-induced apoptotic killing. Mol Microbiol 62: 1484-1497.
21. Kulkarni MM, McMaster WR, Kamysz W, McGwire BS, (2009) Antimicrobial peptide-induced apoptotic death of leishmania results from calcium-de pend ent, caspase-independent mitochondrial toxicity. J Biol Chem 284: 15496-15504.
22. McGwire BS, Olson CL, Tack BF, Engman DM, (2003) Killing of African trypanosomes by antimicrobial peptides. J Infect Dis 188: 146-152.
23. Benincasa M, Skerlavaj B, Gennaro R, Pellegrini A, Zanetti M, (2003) In vitro and in vivo antimicrobial activity of two alpha-helical cathelicidin peptides and of their synthetic analogs. Peptides 24: 1723-1731.
24. Giacometti A, Cirioni O, Ghiselli R, Bergnach C, Orlando F, et al. (2004) The antimicrobial peptide BMAP-28 reduces lethality in mouse models of staphylococcal sepsis. Crit Care Med 32: 2485-2490.
25. Risso A, Braidot E, Sordano MC, Vianello A, Macri F, et al. (2002) BMAP-28, an antibiotic peptide of innate immunity, induces cell death through opening of the mitochondrial permeability transition pore. Mol Cell Biol 22: 1926-1935.
26. Kindrachuk J, Scruten E, Attah-Poku S, Bell K, Potter A, et al. Stability, toxicity and biological activity of host defense peptide BMAP28 and its inversed and retro-inversed isomers. Biopolymers.
27. Papo N, 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.
28. Oren Z, Hong J, Shai Y, (1997) A repertoire of novel antibacterial diastereomeric peptides with selective cytolytic activity. J Biol Chem 272: 14643-14649.
29. Oren Z, Shai Y, (1997) Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study. Biochemistry 36: 1826-1835.
30. Joshi PB, Kelly BL, Kamhawi S, Sacks DL, McMaster WR, (2002) Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Mol Biochem Parasitol 120: 33-40.
31. Allison DC, Ridolpho P, (1980) Use of a trypan blue assay to measure the deoxyribonucleic acid content and radioactive labeling of viable cells. J Histochem Cytochem 28: 700-703.
32. Moore RA, Bates NC, Hancock RE, (1986) Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin. Antimicrob Agents Chemother 29: 496-500.
33. Ganguly S, Bandyopadhyay S, Sarkar A, Chatterjee M, (2006) Development of a semi-automated colorimetric assay for screening anti-leishmanial agents. J Microbiol Methods 66: 79-86.
34. Kolodziej H, Kiderlen AF, (2005) Antileishmanial activity and immune modulatory effects of tannins and related compounds on Leishmania parasitised RAW 264.7 cells. Phytochemistry 66: 2056-2071.
35. 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.
36. Mangoni ML, Papo N, Saugar JM, Barra D, Shai Y, et al. (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.
37. Gaidukov L, Fish A, Mor A, (2003) Analysis of membrane-binding properties of dermaseptin analogues: relationships between binding and cytotoxicity. Biochemistry 42: 12866-12874.
38. Mangoni ML, (2006) Temporins, anti-infective peptides with expanding properties. Cell Mol Life Sci 63: 1060-1069.
39. Diaz-Achirica P, Ubach J, Guinea A, Andreu D, 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 (Pt 1): 453-460.
40. Orlando F, Ghiselli R, Cirioni O, Minardi D, Tomasinsig L, et al. (2008) BMAP-28 improves the efficacy of vancomycin in rat models of gram-positive cocci ureteral stent infection. Peptides 29: 1118-1123.
41. Ghiselli R, Giacometti A, Cirioni O, Dell'Acqua G, Bergnach C, et al. (2006) RNAIII-inhibiting peptide in combination with the cathelicidin BMAP-28 reduces lethality in mouse models of staphylococcal sepsis. Shock 26: 296-301.
42. Hancock RE, Sahl HG, (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551-1557.
43. Alvarez-Bravo J, Kurata S, Natori S, (1994) Novel synthetic antimicrobial peptides effective against methicillin-resistant Staphylococcus aureus. Biochem J 302 (Pt 2): 535-538.
44. Santamaria C, Larios S, Quiros S, Pizarro-Cerda J, Gorvel JP, et al. (2005) Bactericidal and antiendotoxic properties of short cationic peptides derived from a snake venom Lys49 phospholipase A2. Antimicrob Agents Chemother 49: 1340-1345.
45. Chen Y, Vasil AI, Rehaume L, Mant CT, Burns JL, et al. (2006) Comparison of biophysical and biologic properties of alpha-helical enantiomeric antimicrobial peptides. Chem Biol Drug Des 67: 162-173.
46. Cirioni O, Giacometti A, Ghiselli R, Bergnach C, Orlando F, et al. (2006) Pre-treatment of central venous catheters with the cathelicidin BMAP-28 enhances the efficacy of antistaphylococcal agents in the treatment of experimental catheter-related infection. Peptides 27: 2104-2110.
47. Chang CS, Chang KP, (1986) Monoclonal antibody affinity purification of a Leishmania membrane glycoprotein and its inhibition of leishmania-macrophage binding. Proc Natl Acad Sci U S A 83: 100-104.
48. Etges R, Bouvier J, Bordier C, (1986) The major surface protein of Leishmania promastigotes is a protease. J Biol Chem 261: 9098-9101.
49. Wilson ME, Paetz KE, Ramamoorthy R, Donelson JE, (1993) The effect of ongoing protein synthesis on the steady state levels of Gp63 RNAs in Leishmania chagasi. J Biol Chem 268: 15731-15736.
50. Bouvier J, Schneider P, Etges R, Bordier C, (1990) Peptide substrate specificity of the membrane-bound metalloprotease of Leishmania. Biochemistry 29: 10113-10119.
51. Bouvier J, Bordier C, Vogel H, Reichelt R, Etges R, (1989) Characterization of the promastigote surface protease of Leishmania as a membrane-bound zinc endopeptidase. Mol Biochem Parasitol 37: 235-245.
52. Ip HS, Orn A, Russell DG, Cross GA, (1990) Leishmania mexicana mexicana gp63 is a site-specific neutral endopeptidase. Mol Biochem Parasitol 40: 163-172.
53. Tzinia AK, Soteriadou KP, (1991) Substrate-dependent pH optima of gp63 purified from seven strains of Leishmania. Mol Biochem Parasitol 47: 83-89.
54. Halle M, Gomez MA, Stuible M, Shimizu H, McMaster WR, et al. (2009) The Leishmania surface protease GP63 cleaves multiple intracellular proteins and actively participates in p38 mitogen-activated protein kinase inactivation. J Biol Chem 284: 6893-6908.
55. Montaraz JA, Winter AJ, (1986) Comparison of living and nonliving vaccines for Brucella abortus in BALB/c mice. Infect Immun 53: 245-251.
56. Kelly BL, Nelson TN, McMaster WR, (2001) Stage-specific expression in Leishmania conferred by 3′ untranslated regions of L. major leishmanolysin genes (GP63). Mol Biochem Parasitol 116: 101-104.
57. Kulkarni MM, Jones EA, McMaster WR, McGwire BS, (2008) Fibronectin binding and proteolytic degradation by Leishmania and effects on macrophage activation. Infect Immun 76: 1738-1747.
58. Lieke T, Nylen S, Eidsmo L, McMaster WR, Mohammadi AM, et al. (2008) Leishmania surface protein gp63 binds directly to human natural killer cells and inhibits proliferation. Clin Exp Immunol 153: 221-230.
59. Brittingham A, Morrison CJ, McMaster WR, McGwire BS, Chang KP, et al. (1995) Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J Immunol 155: 3102-3111.
60. Gomez MA, Contreras I, Halle M, Tremblay ML, McMaster RW, et al. (2009) Leishmania GP63 alters host signaling through cleavage-activated protein tyrosine phosphatases. Sci Signal 2: ra58.