Cytostatic and cytotoxic effects of activated macrophages and nitric oxide donors on Brugia malayi

Infection and Immunity

Volumn 65, Issue 7, 1997, Pages 2732-2739

  Thomas, G Ruth ^a   McCrossan, Maria ^b   Selkirk, Murray E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE;

ANIMAL CELL; ARTICLE; BRUGIA MALAYI; CYTOTOXICITY; HOST PARASITE INTERACTION; INFECTION SENSITIVITY; MACROPHAGE ACTIVATION; MICROFILARIASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 0030951301     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.65.7.2732-2739.1997     Document Type: Article

References (53)

1. Ahmed, S. F., I. P. Oswald, P. Caspar, S. Hieny, L. Reefer, A. Sher, and S. L. James. 1997. Developmental differences determine larval susceptibility to nitric oxide-medinted killing in a murine model of vaccination against Schistosoma mansoni. Infect. Immun. 65:219-226.
2. Amano, F., and Y. Akamatsu. 1991. A lipopofysaccharide (LPS)-resistant mutant isolated from a macrophage-like cell line. J774.1, exhibits an altered activated macrophage phenotype in response to LPS. Infect. Immun. 59: 2166-2174.
3. Assreuy, J., F. Q. Cunha, M. Epperlein, A. Noronha-Dutra, C. A. O'Donnell, F. Y. Lien, and S. Moncada. 1994. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur. J. Immunol. 24:672-676.
4. Baldwin, C. I., F. de Medeiros, and D. A. Denham. 1993. IgE responses in cats infected with Brugia pahangi. Parasite Immunol. 15:291-296.
5. Bancroft, A, J., R. K. Grencis, K. J. Else, and K. Devaney. 1994. The role of CD4 cells in protective immunity to Brugia pahangi. Parasite Immunol. 16:385-387.
6. Beckman, J. S., T. W. Beckman, J. Chen, P. M. Marshall, and B. A. Freeman. 1990. Apparent hydroxyl radical production by peroxynitritc: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87:1621-1624.
7. Brunelli, L., J. P. Crow, and J. S. Beckman. 1995. The comparative toxicity of nitric oxide and peroxynitrite to Esherichia coli. Arch. Biochem. Biophys. 316:327-334.
8. Carreras, M. C., G. A. Pargamnent, S. D. Catz, J. J. Poderoso, and A. Boveris. 1994. Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Lett. 341:65-68.
9. Castro, L., M. Rodriguez, and R. Radi. 1994. Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide. J. Biol. Chem. 269: 29409-29415.
10. Comley, J. C. W., S. Townson, M. J. Rees, and A. Dobinson. 1989. The further application of MTT-formazon colorimetry to studies on filarial worm viability. Trop. Med. Parasitol. 40:311-316.
11. Cookson, E., M. L. Blaxter, and M. E. Selkirk. 1992. Identification of the major soluble cuticular glycoprotein of lymphatic filarial nematode parsites (gp29) as a secretory homolog of glutathione peroxidase. Proc. Nail. Acad. Sci. USA 89:5837-5841.
12. Denham, D. A., P. B. McGreevy, R. R. Suswillo, and R. Rogers. 1983. The resistance to re-infection of cats repeatedly inoculated with infective larvae of Brugia pahangi. Parasitology 86:11-18.
13. Denicolla, A., H. Rubbo, D. Rodriguez, and R. Radl. 1993. Peroxynitritemadiated cytotoxicity of T. cruzi. Arch. Biochem. Biophys. 304:279-286.
14. Dimock, K. A., M. L. Eberhard, and P. J. Lammie. 1996. Th1-like antifilarial immune responses predominate in antigen-negative persons. Infect. Immun. 64:2962-2967.
15. Granger, D. L., and J. B. Hibbs, Jr. 1981. Recovery from injury incurred by leukemia cells in contact with activated macrophages. Fed. Proc. 40:761.
16. Granger, D. L., and A. L. Lehninger. 1982. Sites of inhibition of mitochondrial electron transport in macrophage-injured neoplastic cells. J. Cell Biol. 95:527-535.
17. Granner, D. L., R. R. Taintor, J. L. Cook, and J. B. Hibbs, Jr. 1980. Injury of neoplastic cells by murine macrophages leads to inhibition of mitochondrial respiration. J. Clin. Invest. 65:357-370.
18. Gusmǎo. R. D'A., A. M. Stanley, and E. A. Ottesen. 1981. Brugia pahangi: immunologic evaluation of the differential susceptibility to filarial infection in inbred Lewis cais. Exp. Parasitol. 52:147-159.
19. Hogg, N., M. Darley-Usmar, M. T. Wilson, and S. Moneada. 1992. Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem. J. 281:419-424.
20. Ischiropoulos, H., L. Zhu, and J. S. Beckman. 1992. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 298:446-451.
21. King, C. L., S. Mahangty, V. Kumaraswami, J. S. Abrams, J. Regunathan, K. Jayaraman, K. A. Otteson, and T. B. Nutman. 1993. Cytokine control of parasite-specific anergy in human lymphatic filariasis: preferential induction of a regulatory T helper type 2 subset. J. Clin. Invest. 92:1667-1673.
22. Kurniawan, A., M. Yazdanbakhsh, R. van Ree, R. Aalberse, M. E. Selkirk, F. Partono, and R. M. Maizels. 1993. Differential expression of IgE and IgG4 specific antibody responses in asymptomatic and chronic human filariasis J. Immunol. 150:3941-3950.
23. Lammie, P. J., A. W. Hightower, F. O. Richards, Jr., R. T. Bryan, H. C. Spencer, D. F. McNeeley, M. B. McNeeley, and M. L. Eberhard. 1992. Alterations in filarial antigen-specific immunologic reactivity following treatment with ivcrmectin and diethylcarbamazime. Am. J. Trop. Med. Hyg. 46:292-295.
24. Lawrence, R. A. 1996. Lymphatic filariasis: what mice can tell us. Parasitol. Today 12:267-271.
25. Lipton, S. A., Y. B. Choi, Z. H. Pan, S. Z. Lei, H. S. V. Chen, N. J. Sucher, J. Losalzo, D. J. Singel, and J. S. Stamler. 1993. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso- compounds. Nature 364:626-632.
26. Maizels, R. M., D. A. P. Bundy, M. E. Selkirk, D. F. Smith, and R. M. Anderson. 1993. Immunological modulation and evasion by helminth parasites in human populations. Nature 365:797-805.
27. Mabels, R. M., E, Sartono, A. Kurniawan, F. Portono, M, E. Selkirk, and M. Yazdanbakhsh. 1995. T cell activation and the balance of antibody isotypes in human lymphatic filariasis. Parasitol. Today 11:50-56.
28. McLaren, D. J., and S. L. James. 1985. Ultrastructural studies of the killing of schistosomula of Schistosoma mansoni by activated macrophages in vitro. Parasite Immunol. 7:315-331.
29. Mendis, A. H. W., and S. Townson. 1985. Evidence for the occurrence of respiratory electron transport in adult Brugia pahangi and Diptalonema viteae. Mol. Biochem. Parasitol. 14:337-354.
30. Middleton, K. R., and H. J. Saz. 1979. Comparative utilization of pyruvatc by Brugia pahangi, Dipetalonema viteae, and Litomosides carinii. J. Parasitol. 65:1-7.
31. Mosmann,T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63.
32. Ottesen, E. A. 1992. Infection and disease in lymphatic filariasis: an immunological perspective, Parasitology 104:S71-S79.
33. Ou, X., L. Tang, M. McCrossan, K. Henkle-Duhrsen, and M. E. Selkirk. 1995. Brugia pahangi: localisation and differential expression of extracellular and cytoplasmic CuZn superoxide dismutases in adults and microfilariae. Exp. Parasitol. 80:515-529.
34. Ou, X., G. R. Thomas, M. R. Chacón, L. Tang, and M. E. Selkirk. 1995. Brugia pahangi: differential susceptibility to and metabolism of hydrogen peroxide in adults and microfilariae. Exp. Parasitol. 80:530-540.
35. Pearco, E. J., and S. L. James. 1986. Post lung-stage schistosomula of Schistosoma mansoni exhibit transient susceptibility to macrophage-mediated cytotoxicity in vitro that may relate to late phase killing in vivo. Parasite Immunol. 8:513-527.
36. Piessens W. F., S. Ratowayanto, P. W. Piessens, S. Tuti, P. B. McGreevy, F. Darwis, J. R. Palmieri, I. Koiman, and D. T. Dennis. 1981. Effect of treatment with diethylcarbamazine on immune responses to filarial antigens in patients infected with Brugia pahangi. Acta Trop. 38:227-234.
37. Radi, R., J. S. Beckman, K. M. Bush, and B. A. Freeman. 1991. Peroxynitrite oxidation of sulfhydryls. J. Biol. Chem. 266:4244-4250.
38. Kadi, R., J. S. Beckman, K. M. Bush, and B. A. Freeman. 1991. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288:481-487.
39. Radi, R., M. Rodriguez., L. Castro, and R. Telleri. 1994. Inhibition of mitochondrial electron transport by peroxynitrite. Arch. Biochem. Biophys. 308: 89-95.
40. Rajan, T. V., P. Porte, J. A. Yates, L. Keefer, and L. D. Shultz. 1996. Role of nitric oxide in host defence against an extracellular metazoan parasite, Brugia malayi. Infect. Immun. 64:3351-3353.
41. Rew, R. S., and H. J. Saz. 1977. The carbohydrate metabolism of Brugia pahangi microfiluriae. J. Parasitol. 63:123-129.
42. Sartono, E., Y. C. M. Kruize, A. Kurniawan, P. H. van der Meide, F. Partono, R. M. Maizels, and M. Yazdanbakhsh. 1995. Elevated cellular immune responses and interferon-γ release after long-term diethylcarbamazine treatment of patients with human lymphatic filariasis. J. Infect. Dis. 171:1683-1687.
43. Smith, V. P., et al. Unpublished data.
44. Smith, V. P., M. E. Selkirk, and K. Goumnaris. 1996. Identification and composition of lipid classes in surface and somatic preparations of adult Brugia malayi. Mol. Biochem. Parasitol. 78:105-116.
45. Suswillo, R. R., D. G. Owen, and D. A. Denham. 1980. Infections of Brugia pahanagi in conventional und nude (athymic) mice. Acta Trop, 37:327-335.
46. Szab́o, C., B. J. Day, und A. L. Sulzman. 1996. Evaluation of the relative contribution of nitric oxide and peroxynitrite to the suppression of mitochondrial respiration in immunostimulated macrophages using a manganese mesoporphyrin superoxide dismutase mimetic und peroxynitriie scavenger. FEBS Lett. 381:82-86.
47. Szab́o, C., and A. L. Salzman. 1995. Endogenous peroxynitrite is involved in the inhibition of mitochondrial respiration in immuno-stimulated J774.2 macrophages, Biochem. Biophys. Res. Commun. 209:739-743.
48. Taylor, M., H. F. Cross, A. A. Mohammed, A. J. Trees, and A. E. Blanco. 1996. Susceptibility of Brugia malayi and Onchocerca lienalis microfilariae to nitric oxide and hydrogen peroxide in cell-fee culture and from IFNγ-activated macrophages. Parasitology 112:315-322.
49. Vazquez-Torres, A., J. Jones-Corson, and E. Balish. 1996. Peroxynitrite contributes 10 the candidacidal activity of nitric oxide-producing macrophages. Infect. Immun. 64:3127-3133.
50. Vickery, A. C., A. L. Vincent, and W. A. Sodeman, Jr. 1983. Effect of immune reconstitution on resistance to Brugia pahangi in congentially athymic nude mice. J. Parasitol. 69:478-485.
51. Vincent, A. L., L. R. Ash, and S. P. Frommes. 1975. The ultrastructure of adult Brugia malayi (Brug, 1927) (Nematoda:Filaroidea). J. Parasitol. 61: 499-512.
52. Wang, E. J., and H. J. Saz. 1974. Comparative biochemical studies of Litomosoides carinii, Dipetalonema viteae, and Brugia pahangi adults. J. Parasitol. 60:316-321.
53. Zembala, M., M. Siedlar, J. Marcinkiewicz, and J. Pryjma. 1994. Human monocytes are stimulated for nitric oxide release in vitro by some tumour cells but not by cytokines and lipopolysaccharide. Eur. J. Immunol. 24:435-439.