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Macrophages in the development of protective immunity against experimental Brugia malayi infection

Published online by Cambridge University Press:  23 August 2004

R. GUPTA ,
P. BAJPAI ,
L. M. TRIPATHI ,
V. M. L. SRIVASTAVA ,
S. K. JAIN  and
S. MISRA-BHATTACHARYA
R. GUPTA
Affiliation:
Division of Parasitology, Central Drug Research Institute, Post Box No. 173, Lucknow-226001, India
P. BAJPAI
Affiliation:
Division of Parasitology, Central Drug Research Institute, Post Box No. 173, Lucknow-226001, India
L. M. TRIPATHI
Affiliation:
Division of Parasitology, Central Drug Research Institute, Post Box No. 173, Lucknow-226001, India
V. M. L. SRIVASTAVA
Affiliation:
Division of Parasitology, Central Drug Research Institute, Post Box No. 173, Lucknow-226001, India
S. K. JAIN
Affiliation:
Faculty of Science, Department of Biotechnology, Jamia Hamdard University, Hamdard Nagar, New Delhi-110062, India
S. MISRA-BHATTACHARYA
Affiliation:
Division of Parasitology, Central Drug Research Institute, Post Box No. 173, Lucknow-226001, India
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Abstract

The present report compares the macrophage function in rodent hosts susceptible and resistant to the human lymphatic filariid Brugia malayi. Macrophages from both mastomys (resistant) and gerbil (susceptible) infected intraperitoneally (i.p.) with the infective larvae (L3) of B. malayi were isolated from peritoneal lavage at different time-intervals and formation rate of NO, H2O2, O2−, TNF-α, glutathione peroxidase and reductase was assayed. NO release was found to be significantly increased in resistant mastomys as compared to gerbils and the release was markedly suppressed by i.p. administration of the NOS inhibitor aminoguanidine (AG). The AG-treated mastomys also demonstrated significantly greater establishment of larvae which correlated well with suppressed formation of NO. Nitric oxide synergizes with superoxide to form peroxynitrite radical (potent oxidant), which is known to be more toxic per se than NO. Results indicate the possible involvement of peroxynitrite in the rapid killing of larvae in the peritoneal cavity of mastomys. In contrast, the production of H2O2 was found to be enhanced in both species indicating that B. malayi L3 could withstand the toxic effects of H2O2. The higher level of glutathione peroxidase and reductase, as observed in mastomys compared with the gerbil after larval introduction, possibly protects the cell against the injurious effect of H2O2. The TNF-α level remained virtually unchanged in both the hosts, suggesting an insignificant role for this cytokine in parasite establishment.

Keywords

Brugia malayimacrophagesTNF-αnitric oxideglutathionemastomysgerbilprotective immunity
Type
Research Article
Information
Parasitology , Volume 129 , Issue 3 , September 2004 , pp. 311 - 323
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ADAMS, L. B., HIBBS, J., TAINTOR, R. R. & KRAHENBUHL, J. S. ( 1990). Microbiostatic effect of murine activated macrophages for Toxoplasma gondii. Journal of Immunology 144, 2726–2729.Google Scholar
ASH, L. R. & RILEY, J. M. ( 1970). Development of subperiodic Brugia malayi in the jird, Meriones unguiculatus with notes on infections in other rodents. Journal of Parasitology 56, 969–972.CrossRefGoogle Scholar
BAERMANN, G. ( 1917). Eine einfache Methode zur Auffindung von Ankylostomum (Nematoden) Larven in Erdproben. Geneesk Tijdschr Ned-Indie 57, 131–137.Google Scholar
BRUNELLI, L., CROW, J. P. & BECKMAN, J. S. ( 1995). The comparative toxicity of nitric oxide and peroxynitrite to E. coli. Archives of Biochemistry and Biophysics 316, 327–334.CrossRefGoogle Scholar
CALLAHAN, H. L., CROUCH, R. K. & JAMES, E. R. ( 1988). Helminth anti-oxidant enzymes: a protective mechanism against host oxidants? Parasitology Today 4, 218–225.Google Scholar
CALLAHAN, H. L., CROUCH, R. K. & JAMES, E. R. ( 1990). Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae. Parasitology 100, 407–415.CrossRefGoogle Scholar
CARRERAS, M. C., PARGAMENT, G. A., CATZ, S. D., PODEROSO, J. J. & BOVERIS, A. ( 1994). Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Letters 341, 65–68.CrossRefGoogle Scholar
CORBETT, J. A., TILTON, R. G., CHANG, K., HASAN, S., IDO, Y., WANG, L., SWEETLAND, L., LANCASTER, M. A., WILLIAMSON, J. R. & McDANIEL, M. L. ( 1992). Aminoguanidine, a novel inhibitor of nitric oxide formation, prevents diabetic vascular dysfunction. Diabetes 41, 552–556.CrossRefGoogle Scholar
DENICOLA, A., RUBBO, H., RODRIGUEZ, D. & RADI, R. ( 1993). Peroxynitrite mediated cytotoxicty of T. cruzi. Archives of Biochemistry and Biophysics 304, 279–286.CrossRefGoogle Scholar
GANLEY, L., BABU, S. & RAJAN, T. V. ( 2001). Course of Brugia malayi infection in C57BL/6J NOS2+/+ and −/− mice. Experimental Parasitology 98, 35–43.CrossRefGoogle Scholar
GREEN, L. C., WAGNER, D. A., GLOGOWSKI, J., SKIPPER, P. L., WISHNOK, J. S. & TANNENBAUM, S. A. ( 1982). Analysis of nitrate, nitrite and [15N] nitrate in biological fluids. Analytical Biochemistry 126, 131–138.CrossRefGoogle Scholar
GREEN, S. J., MELTZER, M. S., HIBBS, J. B. & NACY, C. A. ( 1990). Activated macrophages destroy intracellular Leishmania major amastigotes by an L-arginine dependent killing mechanism. Journal of Immunology 144, 278–283.Google Scholar
GUPTA, R., TYAGI, K., JAIN, S. K. & MISRA-BHATTACHARYA, S. ( 2003). Brugia malayi: establishment in inbred and outbred strains of mice. Experimental Parasitology 103, 57–60.CrossRefGoogle Scholar
ISCHIROPOULOUS, S. H., ZHU, L. & BECKMAN, J. S. ( 1992). Peroxynitrite formation from macrophage derived nitric oxide. Archives of Biochemistry and Biophysics 298, 446–451.CrossRefGoogle Scholar
JAMES, S. L. ( 1995). Role of nitric oxide in parasitic infections. Microbiology Review 59, 533–547.Google Scholar
JAMES, S. L. & GLAVEN, J. ( 1989). Macrophage cytotoxicity against schistosomula of Schistosoma mansoni involves arginine dependent production of reactive nitrogen intermediates. Journal of Immunology 143, 4208–4214.Google Scholar
JAMES, S. L., GLAVEN, J., GOLDENBERG, S., MELTZER, M. S. & PEARCE, E. ( 1992). Tumor necrosis factor (TNF) as a mediator of macrophage helminthotoxic activity. Parasite Immunology 12, 1–13.Google Scholar
JENKINS, P., SPIERS, S., DIXON, J. B., CARTER, S. D. & MAY, S. ( 1992). The effects of tumor necrosis factor on host–parasite relations in murine Mesocestoides corti (Cestoda) infection. Parasitology 105, 453–459.CrossRefGoogle Scholar
McCALL, J. W., MALONE, J. B., AH, H. S. & THOMPSON, P. E. ( 1973). Mongolian jirds (Meriones unguiculatus) infected with Brugia pahangi by the intraperitoneal route: a rich source of developing larvae, adult filariae and microfilariae. Journal of Parasitology 59, 436.CrossRefGoogle Scholar
MELLOUK, S., GREEN, S. J., NACY, C. A. & HOFFMAN, S. L. ( 1991). IFN-γ inhibits development of Plasmodium berghei exoerythrocytic stages in hepatocytes by an l-arginine dependent effector mechanism. Journal of Immunology 146, 3971–3976.Google Scholar
MICHAEL, E. ( 2000). The population dynamics and epidemiology of lymphatic filariasis. In Lymphatic Filariasis ( ed. Nutman, T. B.), Imperial College Press, London. 1, 41–82.CrossRef
MISRA, S., SINGH, D. P., MURTHY, P. K. & CHATTERJEE, R. K. ( 1990). Mode of action of antifilarials: modulation of immune adherence of cells to microfilariae in vitro. Tropical Medicine 32, 33–43.Google Scholar
MOSIER, D. F. ( 1984). Separation of macrophages on plastic and glass surfaces. Methods in Enzymology 108, 294–299.CrossRefGoogle Scholar
NASSARE, C., KRAHENBUHL, J. L. & KLEI, T. R. ( 1998). Down regulation of macrophage activation in Brugia pahangi infected jird (Meriones unguiculatus). Infection and Immunity 66, 1063–1069.Google Scholar
NATHAN, C. F., MURRAY, H. W. & COHN, Z. A. ( 1980). Current concepts: the macrophage as an effector cell. New England Journal of Medicine 303, 622–626.CrossRefGoogle Scholar
NOSEWORTHY, J. Jr. & KARNOVSKY, M. L. ( 1972). Role of peroxide in the stimulation of the hexose monophosphate shunt during phagocytosis by polymorphonuclear leukocytes. Enzyme 13, 110–131.CrossRefGoogle Scholar
OLIVEIRA, O., FONSECA, S., ROMAO, P. R. T., FIGUEIREDO, F., FERREIRA, S. H. & CUHNA, F. Q. ( 1998). Microbial activity of eosinophils is associated with activation of the arginine-NO pathway. Parasite Immunology 20, 405–412.CrossRefGoogle Scholar
OTTESEN, E. A. ( 1992). Infection and disease in lymphatic filariasis: an immunological perspective. Parasitology 104, S71–S79.CrossRefGoogle Scholar
OU, X., THOMAS, G. R., CHACON, M. R., TANG, L. & SELKRIK, M. E. ( 1995). Brugia malayi: differential susceptibility to and metabolism of hydrogen peroxide in adults and microfilariae. Experimental Parasitology 80, 530–540.CrossRefGoogle Scholar
PAGLIA, D. E. & VALENTINE, W. N. ( 1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158–169.Google Scholar
PETRANYI, G., MIETH, H. & LEITNER, I. ( 1975). Mastomys natalensis as an experimental host for Brugia malayi sub periodic. South East Asian Journal of Tropical Medicine and Public Health 6, 328–332.Google Scholar
PICK, E. & MIZEL, D. ( 1981). Rapid micro assays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader. Journal of Immunological Methods 46, 211–219.CrossRefGoogle Scholar
RACKER, E. ( 1955). Glutathione reductase from Baker's yeast beef liver. Journal of Biological Chemistry 217, 855–865.Google Scholar
RADI, R., BECKMAN, J. S., BUSH, K. M. & FREEMAN, B. A. ( 1991). Peroxynitrite oxidation of sulphydryls. Journal of Biological Chemistry 266, 4244–4250.Google Scholar
RAJAN, T. V., GANLEY, L., PACIORKOWSKI, N., SPENCER, L., KLEI, T. R. & SHULTZ, L. D. ( 2002). Brugian infection in peritoneal cavities of laboratory mice: kinetics of infection and cellular responses. Experimental Parasitology 100, 235–247.CrossRefGoogle Scholar
RAJAN, T. V., PORTE, P., YATES, J. A., KEEFER, L. & SHULTZ, L. D. ( 1996). Role of nitric oxide in host defence against an extracellular metazoan parasite Brugia malayi. Infection and Immunity 64, 3351–3352.Google Scholar
RZEPCZYK, C. & BISHOP, C. J. ( 1984). Immunological and ultrastructural aspects of the cell mediated killing of Dirofilaria immitis microfilariae. Parasite Immunology 6, 443–457.CrossRefGoogle Scholar
SELKRIK, M. E., SMITH, V. P., THOMAS, G. R. & GOUNARIS, K. ( 1998). Resistance of filarial nematode parasites to oxidative stress. International Journal for Parasitology 28, 1315–1332.CrossRefGoogle Scholar
SINGH, U., MISRA, S., MURTHY, P. K., KATIYAR, J. C., AGARWAL, A. & SIRCAR, A. R. ( 1997). Immunoreactive molecules of Brugia malayi and their diagnostic potential. Serodiagnosis and Immunotherapy and Infectious Disease 8, 207–212.CrossRefGoogle Scholar
STRAUSS, R. R., PAUL, B. B., JACOBS, A. A. & SBARRA, A. J. ( 1969). The role of phagocytes in host parasite interactions. XIX. Leukocytic glutathione reductase and its involvement in phagocytosis. Archives of Biochemistry and Biophysics 135, 265–271.CrossRefGoogle Scholar
TAYLOR, M., CROSS, H. F., MOHAMMED, A. A., TREES, A. J. & BIANCO, A. E. ( 1996). Susceptibility of Brugia malayi and Onchocerca lienalis microfilariae to nitric oxide and hydrogen peroxide in cell free culture and from IFN-γ activated macrophages. Parasitology 112, 315–322.CrossRefGoogle Scholar
THOMAS, G. R., McCROSSAN, M. & SELKRIK, M. E. ( 1997). Cytostatic and cytotoxic effects of activated macrophages and nitric oxide donors on Brugia malayi. Infection and Immunity 65, 2732–2739.Google Scholar
VAZQUEZ-TORRES, A., JONES-CARSON, J. & BALISH, E. ( 1996). Peroxynitrite contributes to the candidacidal activity of nitric oxide producing macrophages. Infection and Immunity 64, 3127–3133.Google Scholar
WINKLER, S., MENYAWI, I. E., LINNAU, K. F. & GRANINGER, W. ( 1998). Total serum levels of the nitric oxide derivatives nitrite/nitrate during microfilarial clearance in human filarial disease. American Journal of Tropical Medicine and Hygiene 18, 523–525.CrossRefGoogle Scholar
XIE, Q. W., CHO, H. J., CALAYCAY, J., MUMFORD, R. A., SWIDERICK, K., LEE, T., DING, A., TROSO, T. & NATHAN, C. ( 1992). Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256, 225–228.CrossRefGoogle Scholar