Antimicrobial peptide killing of African trypanosomes

Parasite Immunology

Volumn 33, Issue 8, 2011, Pages 461-469

  Harrington, J M ^a  

^a University of Georgia ^*  (United States)

Author keywords

African trypanosomiasis; Antimicrobial peptides; Human sleeping sickness; Tsetse

Indexed keywords

ADRENOMEDULLIN; ALAMETHICIN; ATTACIN; BETA DEFENSIN 1; BETA DEFENSIN 2; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CECROPIN; CORTICOTROPIN RELEASING FACTOR; CRYPTIN 4; DEFENSIN; DIPTERICIN; GHRELIN; INDOLICIDIN; LEUCINOSTATIN A; LEUCINOSTATIN B; NONAMER; NONAMER PEPTIDE A; NONAMER PEPTIDE B; NONAMER PEPTIDE C; NONAMER PEPTIDE D; NONAMER PEPTIDE E; NOVISPIRIN; OVISPIRIN; PLEUROCIDIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEGRIN 1; SMAP 29; STOMOXYN; UNCLASSIFIED DRUG; UNINDEXED DRUG; UROCORTIN;

AFRICAN TRYPANOSOME; ANTIPROTOZOAL ACTIVITY; DRUG EFFICACY; HUMAN; IMMUNITY; INFECTION SENSITIVITY; INNATE IMMUNITY; NAGANA; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRYPANOSOMA;

ALAMETHICIN; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; HUMANS; LIPOPEPTIDES; PEPTIDES; TRYPANOCIDAL AGENTS; TRYPANOSOMA; TSETSE FLIES;

GLOSSINA (GENUS); TRYPANOSOMA;

EID: 79960394032     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2011.01294.x     Document Type: Review

References (72)

1. Barrett MP, Burchmore RJ, Stich A, et al. The trypanosomiases. Lancet 2003; 362: 1469-1480.
2. Jones TW & Davila AM. Trypanosoma vivax- out of Africa. Trends Parasitol 2001; 17: 99-101.
3. Cross GA. Antigenic variation in trypanosomes. Am J Trop Med Hyg 1977; 26: 240-244.
4. Fenn K & Matthews KR. The cell biology of Trypanosoma brucei differentiation. Curr Opin Microbiol 2007; 10: 539-546.
5. Ferguson MA, Haldar K & Cross GA. Trypanosoma brucei variant surface glycoprotein has a sn-1, 2-dimyristyl glycerol membrane anchor at its COOH terminus. J Biol Chem 1985; 260: 4963-4968.
6. Field MC, Menon AK & Cross GA. A glycosylphosphatidylinositol protein anchor from procyclic stage Trypanosoma brucei: lipid structure and biosynthesis. EMBO J 1991; 10: 2731-2739.
7. Morgan GW, Allen CL, Jeffries TR, Hollinshead M & Field MC. Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei. J Cell Sci 2001; 114: 2605-2615.
8. Rodriguez JA, Lopez MA, Thayer MC, et al. Propulsion of African trypanosomes is driven by bihelical waves with alternating chirality separated by kinks. Proc Natl Acad Sci U S A 2009; 106: 19322-19327.
9. Vickerman K. Polymorphism and mitochondrial activity in sleeping sickness trypanosomes. Nature 1965; 208: 762-766.
10. Zhang X, Cui J, Nilsson D, et al. The Trypanosoma brucei MitoCarta and its regulation and splicing pattern during development. Nucleic Acids Res 2010; 38: 7378-7387.
11. Michael R & Yeaman NYY. Mechanisms of antimicrobial peptides and resistance. Pharmacol Rev 2003; 55: 27-55.
12. McGwire BS, Olson CL, Tack BF & Engman DM. Killing of African trypanosomes by antimicrobial peptides. J Infect Dis 2003; 188: 146-152.
13. Hao Z, Kasumba I, Lehane MJ, Gibson WC, Kwon J & Aksoy S. Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proc Natl Acad Sci U S A 2001; 98: 12648-12653.
14. Hao Z, Kasumba I & Aksoy S. Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochem Mol Biol 2003; 33: 1155-1164.
15. Hu Y & Aksoy S. An antimicrobial peptide with trypanocidal activity characterized from Glossina morsitans morsitans. Insect Biochem Mol Biol 2005; 35: 105-115.
16. Hu C & Aksoy S. Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans. Mol Microbiol 2006; 60: 1194-1204.
17. Nayduch D & Aksoy S. Refractoriness in tsetse flies (Diptera: Glossinidae) may be a matter of timing. J Med Entomol 2007; 44: 660-665.
18. Wang J, Hu C, Wu Y, et al. Characterization of the antimicrobial peptide attacin loci from Glossina morsitans. Insect Mol Biol 2008; 17: 293-302.
19. Boulanger N, Brun R, Ehret-Sabatier L, Kunz C & Bulet P. Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Insect Biochem Mol Biol 2002; 32: 369-375.
20. Ishiyama A, Otoguro K, Iwatsuki M, et al. In vitro and in vivo antitrypanosomal activities of three peptide antibiotics: leucinostatin A and B, alamethicin I and tsushimycin. J Antibiot 2009; 62: 303-308.
21. Yamage M, Yoshiyama M, Grab DJ, et al. Characteristics of novel insect defensin-based membrane-disrupting trypanocidal peptides. Biosci Biotechnol Biochem 2009; 73: 1520-1526.
22. Kitani H, Naessens J, Kubo M, et al. Synthetic nonamer peptides derived from insect defensin mediate the killing of African trypanosomes in axenic culture. Parasitol Res 2009; 105: 217-225.
23. Delgado M, Anderson P, Garcia-Salcedo JA, Caro M & Gonzalez-Rey E. Neuropeptides kill African trypanosomes by targeting intracellular compartments and inducing autophagic-like cell death. Cell Death Differ 2009; 16: 406-416.
24. Harrington JM, Widener J, Stephens N, et al. The plasma membrane of bloodstream-form African trypanosomes confers susceptibility and specificity to killing by hydrophobic peptides. J Biol Chem 2010; 285: 28659-28666.
25. McGwire BS & Kulkarni MM. Interactions of antimicrobial peptides with Leishmania and trypanosomes and their functional role in host parasitism. Exp Parasitol 2010; 126: 397-405.
26. Msangi AR, Whitaker CJ & Lehane MJ. Factors influencing the prevalence of trypanosome infection of Glossina pallidipes on the Ruvu flood plain of Eastern Tanzania. Acta Trop 1998; 70: 143-155.
27. Maudlin I & Welburn SC. Maturation of trypanosome infections in tsetse. Exp Parasitol 1994; 79: 202-205.
28. Gibson W & Bailey M. The development of Trypanosoma brucei within the tsetse fly midgut observed using green fluorescent trypanosomes. Kinetoplastid Biol Dis 2003; 2: 1.
29. Boulanger N, Munks RJ, Hamilton JV, et al. Epithelial innate immunity. A novel antimicrobial peptide with antiparasitic activity in the blood-sucking insect Stomoxys calcitrans. J Biol Chem 2002; 277: 49921-49926.
30. Beard CB, O'Neill SL, Mason P, et al. Genetic transformation and phylogeny of bacterial symbionts from tsetse. Insect Mol Biol 1993; 1: 123-131.
31. Cheng Q & Aksoy S. Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol 1999; 8: 125-132.
32. Aksoy S, Weiss B & Attardo G. Paratransgenesis applied for control of tsetse transmitted sleeping sickness. Adv Exp Med Biol 2008; 627: 35-48.
33. Lehrer RI. Primate defensins. Nat Rev Microbiol 2004; 2: 727-738.
34. Zanetti M. The role of cathelicidins in the innate host defenses of mammals. Curr Issues Mol Biol 2005; 7: 179-196.
35. Dorschner RA, Pestonjamasp VK, Tamakuwala S, et al. Cutaneous injury induces the release of cathelicidin anti-microbial peptides active against group A Streptococcus. J Invest Dermatol 2001; 117: 91-97.
36. Haines LR, Hancock RE & Pearson TW. Cationic antimicrobial peptide killing of African trypanosomes and Sodalis glossinidius, a bacterial symbiont of the insect vector of sleeping sickness. Vector Borne Zoonotic Dis 2003; 3: 175-186.
37. Ishiguro K & Arai T. Action of the peptide antibiotic leucinostatin. Antimicrob Agents Chemother 1976; 9: 893-898.
38. Shima A, Fukushima K, Arai T & Terada H. Dual inhibitory effects of the peptide antibiotics leucinostatins on oxidative phosphorylation in mitochondria. Cell Struct Funct 1990; 15: 53-58.
39. Mihajlovic M & Lazaridis T. Antimicrobial peptides in toroidal and cylindrical pores. Biochim Biophys Acta 2010; 1798: 1485-1493.
40. Packchanian A. Chemotherapy of African sleeping sickness. II. Chemotherapy of experimental Trypanosoma gambiense and Trypanosoma rhodesiense infections in mice (Mus musculus) with a new antibiotic, amphomycin. Antibiot Chemother 1956; 6: 684-691.
41. Morita YS, Paul KS & Englund PT. Specialized fatty acid synthesis in African trypanosomes: myristate for GPI anchors. Science 2000; 288: 140-143.
42. Arrighi RB, Ebikeme C, Jiang Y, et al. Cell-penetrating peptide TP10 shows broad-spectrum activity against both Plasmodium falciparum and Trypanosoma brucei brucei. Antimicrob Agents Chemother 2008; 52: 3414-3417.
43. Soomets U, Lindgren M, Gallet X, et al. Deletion analogues of transportan. Biochim Biophys Acta 2000; 1467: 165-176.
44. Haines LR, Thomas JM, Jackson AM, et al. Killing of trypanosomatid parasites by a modified bovine host defense peptide, BMAP-18. PLoS Negl Trop Dis 2009; 3: e373.
45. Hajduk SL, Moore DR, Vasudevacharya J, et al. Lysis of Trypanosoma brucei by a toxic subspecies of human high density lipoprotein. J Biol Chem 1989; 264: 5210-5217.
46. Drain J, Bishop JR & Hajduk SL. Haptoglobin-related protein mediates trypanosome lytic factor binding to trypanosomes. J Biol Chem 2001; 276: 30254-30260.
47. Vanhollebeke B, De Muylder G, Nielsen MJ, et al. A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 2008; 320: 677-681.
48. Harrington JM, Howell S & Hajduk SL. Membrane permeabilization by trypanosome lytic factor, a cytolytic human high-density lipoprotein. J Biol Chem 2009; 284: 13505-13512.
49. Smith AB, Esko JD & Hajduk SL. Killing of trypanosomes by the human haptoglobin-related protein. Science 1995; 268: 284-286.
50. Shiflett AM, Bishop JR, Pahwa A & Hajduk SL. Human high density lipoproteins are platforms for the assembly of multi-component innate immune complexes. J Biol Chem 2005; 280: 32578-32585.
51. Vanhollebeke B, Nielsen MJ, Watanabe Y, et al. Distinct roles of haptoglobin-related protein and apolipoprotein L-I in trypanolysis by human serum. Proc Natl Acad Sci U S A 2007; 104: 4118-41123.
52. Engstler M, Pfohl T, Herminghaus S, et al. Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 2007; 131: 505-515.
53. Gunne H, Hellers M & Steiner H. Structure of preproattacin and its processing in insect cells infected with a recombinant baculovirus. Eur J Biochem 1990; 187: 699-703.
54. Cudic M, Bulet P, Hoffmann R, Craik DJ & Otvos L Jr. Chemical synthesis, antibacterial activity and conformation of diptericin, an 82-mer peptide originally isolated from insects. Eur J Biochem 1999; 266: 549-558.
55. Holak TA, Engstrom A, Kraulis PJ, et al. The solution conformation of the antibacterial peptide cecropin A: a nuclear magnetic resonance and dynamical simulated annealing study. Biochemistry 1988; 27: 7620-7629.
56. Hoover DM, Chertov O & Lubkowski J. The structure of human beta-defensin-1: new insights into structural properties of beta-defensins. J Biol Chem 2001; 276: 39021-39026.
57. Harder J, Bartels J, Christophers E & Schroder JM. A peptide antibiotic from human skin. Nature 1997; 387: 861.
58. Sawai MV, Jia HP, Liu L, et al. The NMR structure of human beta-defensin-2 reveals a novel alpha-helical segment. Biochemistry 2001; 40: 3810-3816.
59. Ouellette AJ & Selsted ME. Paneth cell defensins: endogenous peptide components of intestinal host defense. FASEB J 1996; 10: 1280-1289.
60. Jing W, Hunter HN, Tanabe H, Ouellette AJ & Vogel HJ. Solution structure of cryptdin-4, a mouse paneth cell alpha-defensin. Biochemistry 2004; 43: 15759-15766.
61. Larrick JW, Hirata M, Balint RF, Lee J, Zhong J & Wright SC. Human CAP18: a novel antimicrobial lipopolysaccharide-binding protein. Infect Immun 1995; 63: 1291-1297.
62. Oren Z, Lerman JC, Gudmundsson GH, Agerberth B & Shai Y. Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem J 1999; 341: 501-513.
63. Bagella L, Scocchi M & Zanetti M. cDNA sequences of three sheep myeloid cathelicidins. FEBS Lett 1995; 376: 225-228.
64. Skerlavaj B, Benincasa M, Risso A, Zanetti M & Gennaro R. SMAP-29: a potent antibacterial and antifungal peptide from sheep leukocytes. FEBS Lett 1999; 463: 58-62.
65. Steinstraesser L, Tack BF, Waring AJ, et al. Activity of novispirin G10 against Pseudomonas aeruginosa in vitro and in infected burns. Antimicrob Agents Chemother 2002; 46: 1837-1844.
66. Kokryakov VN, Harwig SS, Panyutich EA, et al. Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins. FEBS Lett 1993; 327: 231-236.
67. Fahrner RL, Dieckmann T, Harwig SS, Lehrer RI, Eisenberg D & Feigon J. Solution structure of protegrin-1, a broad-spectrum antimicrobial peptide from porcine leukocytes. Chem Biol 1996; 3: 543-550.
68. Selsted ME, Novotny MJ, Morris WL, Tang YQ, Smith W & Cullor JS. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J Biol Chem 1992; 267: 4292-4295.
69. Friedrich CL, Rozek A, Patrzykat A & Hancock RE. Structure and mechanism of action of an indolicidin peptide derivative with improved activity against gram-positive bacteria. J Biol Chem 2001; 276: 24015-24022.
70. Romeo D, Skerlavaj B, Bolognesi M & Gennaro R. Structure and bactericidal activity of an antibiotic dodecapeptide purified from bovine neutrophils. J Biol Chem 1988; 263: 9573-9575.
71. Skerlavaj B, Gennaro R, Bagella L, Merluzzi L, Risso A & Zanetti M. Biological characterization of two novel cathelicidin-derived peptides and identification of structural requirements for their antimicrobial and cell lytic activities. J Biol Chem 1996; 271: 28375-28381.
72. Briggs MS, Cornell DG, Dluhy RA & Gierasch LM. Conformations of signal peptides induced by lipids suggest initial steps in protein export. Science 1986; 233: 206-208.