Human defensin α-1 causes Trypanosoma cruzi membrane pore formation and induces DNA fragmentation, which leads to trypanosome destruction

Infection and Immunity

Volumn 75, Issue 10, 2007, Pages 4780-4791

  Madison, M Nia ^a   Kleshchenko, Yuliya Y ^a   Nde, Pius N ^a   Simmons, Kaneatra J ^a   Lima, Maria F ^a   Villalta, Fernando ^a  

^a MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS DNA; DEFENSIN; DEFENSIN ALPHA 1; DNA FRAGMENT; IMMUNOGLOBULIN G; MITOCHONDRIAL DNA; UNCLASSIFIED DRUG;

AMASTIGOTE; ARTICLE; CELL DAMAGE; CELL VACUOLE; CHAGAS DISEASE; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; EXPOSURE; FLAGELLUM; HUMAN; HUMAN CELL; INNATE IMMUNITY; MEMBRANE DEPOLARIZATION; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

ALPHA-DEFENSINS; ANIMALS; CELL MEMBRANE; CYTOPLASM; DNA FRAGMENTATION; EPITHELIAL CELLS; HELA CELLS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; TRYPANOSOMA CRUZI; VACUOLES;

EID: 34848855400     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00557-07     Document Type: Article

References (48)

1. Agerberth, B., J. Charo, J. Werr, B. Olsson, F. Idali, L. Lindbom, R. Kiessling, H. Jornvall, H. Wigzell, and G. H. Gudmundsson. 2000. The human antimicrobial and chemotactic peptides LL-37 and alpha-defensins are expressed by specific lymphocyte and monocyte populations. Blood 96: 3086-3093.
2. Aley, S. B., M. Zimmerman, M. Hetsko, M. E. Selsted, and F. D. Gillin. 1994. Killing of Giardia lamblia by cryptdins and cationic neutrophil peptides. Infect. Immun. 62:5397-5403.
3. Ashitani, J., M. Nakazato, H. Mukae, H. Taniguchi, Y. Date, and S. Matsukara. 2000. Recombinant granulocyte colony-stimulating factor induces production of human neutrophil peptides in lung cancer patients with neutropenia. Regul. Pept. 95:87-92.
4. Bouley, R., S. Breton, T. Sun, M. McLaughin, N. N. Nsumu, H. Y. Lin, D. A. Ausiello, and D. Brown. 2000. Nitric oxide and atrial natriuretic factor stimulate cGMP-dependent membrane insertion of aquaporin 2 in renal epithelial cells. J. Clin. Investig. 10:1115-1126.
5. Castro, J. A., M. M. de Mecca, and L. C. Bartel. 2006. Toxic side effects of drugs used to treat Chagas' disease (American trypanosomiasis). Hum. Exp. Toxicol. 225:471-479.
6. Daher, K. A., R. I. Lehrer, T. Ganz, and M. Kronenberg. 1988. Isolation and characterization of human defensin cDNA clones. Proc. Natl. Acad. Sci. USA 85:7327-7331.
7. Deschesnes, R. G., J. Huot, K. Valerie, and J. Landry. 2001. Involvement of p38 in apoptosis-associated membrane blebbing and nuclear condensation. Mol. Biol. Cell 12:1569-1582.
8. Fischer, E., M. A. Ouaissi, P. Velge, J. Cornette, and M. D. Kazatchkine. 1988. gp 58168, a parasite component that contributes to the escape of the trypomastigote form of T. cruzi from damage by the human alternative complement pathway. Immunology 65:299-303.
9. Ganz, T. 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3:710-720.
10. Ganz, T., M. E. Selsted, D. Szklarek, S. S. L. Harwig, K. Daher, D. F. Bainton, and R. I. Lehrer. 1985. Defensins. Natural peptide antibiotics of human neutrophils. J. Clin. Investig. 76:1427-1435.
11. Garg, N., and V. Bhatia. 2005. Current status and future prospects for a vaccine against American trypanosomiasis. Exp. Rev. Vaccines 4:867-880.
12. Heibein, J. A., M. Barry, B. Motyka, and R. C. Bleackley. 1999. Granzyme B-induced loss of mitochondrial inner membrane potential (Delta Psi m) and cytochrome c release are caspase independent. J. Immunol. 163:4683-4693.
13. Horne, R. W., A. D. Bangham, and V. P. Whittaker. 1963. Negatively stained lipoprotein membranes. Nature 200:1340.
14. Ihi, T., M. Nakazato, H. Mukae, and S. Matsukura. 1997. Elevated concentrations of human neutrophil peptides in plasma, blood, and body fluids from patients with infections. Clin. Infect. Dis. 25:1134-1140.
15. Kirchhoff, L. V. 1989. Is Trypanosoma cruzi a new threat to our blood supply? Ann. Intern. Med. 111:773-775.
16. Kleshchenko, Y. Y., T. N. Moody, V. A. Furtak, J. Ochieng, M. F. Lima, and F. Villalta. 2004. Human galectin-3 promotes Trypanosoma cruzi adhesion to human coronary artery smooth muscle cells. Infect. Immun. 72:6717-6721.
17. Klotman, M. E., and T. L. Chang. 2006. Defensins in innate antiviral immunity. Nat. Rev. Immunol. 6:447-456.
18. Lehrer, R. I. 2007. Multispecific myeloid defensins. Curr. Opin. Hematol. 14:16-21.
19. Lehrer, R. I., A. K. Lichtenstein, and T. Ganz. 1993. Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu. Rev. Immunol. 11:105-128.
20. Lima, M. F., and F. Villalta. 1989. Trypanosoma cruzi trypomastigote clones differentially express a parasite cell adhesion molecule. Mol. Biochem. Parasitol. 33:159-170.
21. McCarthy, M. 2003. American Red Cross to screen blood for Chagas' disease. Lancet 362:1988.
22. McGwire, B. S., C. L. Olson, B. F. Tack, and D. M. Engman. 2003. Killing of African trypanosomes by antimicrobial peptides. J. Infect. Dis. 188:146-152.
23. Mukae, H., H. Iboshi, M. Nakazato, M. Hiratsuka, K. Tokojima, J. Abe, J. Ashitani, S. Kadota, S. Matsukara, and S. Kohno. 2002. Raised plasma concentrations of α defensins in patients with idiopathic pulmonary fibrosis. Thorax 57:623-628.
24. Nde, P. N., K. J. Simmons, Y. Y. Kleshchenko, S. Pratap, M. F. Lima, and F. Villalta. 2006. Silencing of the laminin gamma-1 gene blocks Trypanosoma cruzi infection. Infect. Immun. 74:1643-1648.
25. Nickerson, P., P. Orr, M. L. Schroeder, L. Sekla, and J. B. Johnston. 1989. Transfusion-associated Trypanosoma cruzi infection in a non-endemic area. Ann. Intern. Med. 111:851-853.
26. Panyutich, A. V., E. A. Panyutich, V. A. Krapivin, E. A. Baturevich, and T. Ganz. 1993. Plasma defensin concentrations are elevated in patients with septicemia or bacterial meningitis. J. Lab. Clin. Med. 122:202-207.
27. Rosemberg, S., C. J. Chaves, M. L. Higuchi, M. B. Lopes, H. L. Castro, and L. R. Machado. 1992. Fatal meningoencephalitis caused by reactivation of Trypanosoma cruzi infection in a patient with AIDS. Neurology 42:640-642.
28. Sahl, H. G., U. Pag, S. Bonness, S. Wagner, N. Antcheva, and A. Tossi. 2005. Mammalian defensins: structures and mechanism of antibiotic activity. J. Leukoc. Biol. 77:466-475.
29. Samejima, K., and W. C. Earnshaw. 2005. Trashing the genome: the roles of nucleases during apoptosis. Nat. Rev. Mol. Cell. Biol. 6:677-688.
30. Selsted, M. E., S. S. Harwig, T. Ganz, J. W. Schilling, and R. I. Lehrer. 1985. Primary structures of three human neutrophil defensins. J. Clin. Investig. 76:1436-1439.
31. Selsted, M. E., and A. J. Ouellette. 2005. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 6:551-557.
32. Shafer, W. M., X. Qu, A. J. Waring, and R. I. Lehrer. 1998. Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc. Natl. Acad. Sci. USA 95:1829-1833.
33. Simmons, K. J., P. N. Nde, Y. Y. Kleshchenko, M. F. Lima, and F. Villalta. 2006. Stable RNA interference of host thrombospondin-1 blocks Trypanosoma cruzi infection. FEBS Lett. 580:2365-2370.
34. Sugiyama, T., M. Kobayashi, H. Kawamura, Q. Li, and D. G. Puro. 2004. Enhancement of P2X(7)-induced pore formation and apoptosis: an early effect of diabetes on the retinal microvasculature. Investig. Ophthalmol. Vis. Sci. 45:1026-1032.
35. Szyk, A., Z. Wu, K. Tucker, D. Yang, W. Lu, and J. Lubkowski. 2006. Crystal structures of human alpha-defensins HNP4, HD5, and HD6. Protein Sci. 15:2749-2760.
36. Tanaka, S., C. J. Edberg, C. Winn, G. Fassina, and R. Kimberley. 2003. FcγIIIb allele-sensitive release of α-defensins: anti-neutrophil cytoplasmic antibody-induced release of chemotaxins. J. Immunol. 171:6090-6096.
37. Tang, Y. Q., J. Yuan, G. Osapay, K. Osapay, D. Tran, C. J. Miller, A. J. Ouellette, and M. E. Selsted. 1999. A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated defensins. Science 286:498-502.
38. Tanowitz, H. B., L. V. Kirchhoff, D. Simon, S. A. Morris, L. M. Weiss, and M. Wittner. 1992. Chagas' disease. Clin. Microbiol. Rev. 5:400-419.
39. Tobler, L. H., P. Contestable, L. Pitina, H. Groth, S. Shaffer, G. R. Blackburn, H. Warren, S. R. Lee, and M. P. Busch. 2007. Evaluation of a new enzyme-linked immunosorbent assay for detection of Chagas antibody in US blood donors. Transfusion 47:90-96.
40. Valore, E. V., and T. Ganz. 1992. Posttranslational processing of defensins in immature human myeloid cells. Blood 79:1538-1544.
41. Villalta, F., and F. Kierszenbaum. 1982. Growth of isolated amastigotes of Trypanosoma cruzi in cell-free medium. J. Protozool. 129:570-576.
42. Villalta, F., and F. Kierszenbaum. 1983. Immunization against a challenge with insect vector, metacyclic forms of Trypanosoma cruzi simulating a natural infection. Am. J. Trop. Med. Hyg. 32:273-276.
43. Villalta, F., and F. Kierszenbaum. 1984. Role of inflammatory cells in Chagas' disease. I. Uptake and mechanism of destruction of intracellular (amastigote) forms of Trypanosoma cruzi by human eosinophils. J. Immunol. 132:2053-2058.
44. Villalta, F., and F. Kierszenbaum. 1984. Role of inflammatory cells in Chagas' disease. II. Interactions of mouse macrophages and human monocytes with intracellular forms of Trypanosoma cruzi: uptake and mechanism of destruction. J. Immunol. 133:3338-3343.
45. Villalta, F., Y. Zhang, K. E. Bibb, J. C. Kappes, and M. F. Lima. 1998. The cysteine-cysteine family of chemokines RANTES, MIP-1alpha, and MIP-1beta induce trypanocidal activity in human macrophages via nitric oxide. Infect. Immun. 66:4690-4695.
46. Wetering, S. V., S. P. G. Mannesse-Lazeroms, J. H. Dikjman, and P. S. Hiemstra. 1997. Effect of neutrophil serine proteinases and defensins on lung epithelial cells: modulation of cytotoxicity and IL-8 production. J. Leukoc. Biol. 62:217-226.
47. Wimley, W. C., M. E. Selsted, and S. H. White. 1994. Interactions between human defensins and lipid bilayers: evidence for formation of multimeric pores. Protein Sci. 3:1362-1373.
48. Zhang, C., Y. Xu, J. Gu, and S. F. Schlossman. 1998. A cell surface receptor defined by a mAb mediates a unique type of cell death similar to oncosis. Proc. Natl. Acad. Sci. USA 95:6290-6295.