Synergism of Gamma Interferon and Interleukin-5 in the Control of Murine Filariasis

Infection and Immunity

Volumn 71, Issue 12, 2003, Pages 6978-6985

  Saeftel, Michael ^a,b   Arndt, Manuela ^a   Specht, Sabine ^a,b   Volkmann, Lars ^a   Hoerauf, Achim ^a,b  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 5; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; FILARIASIS; IMMUNE RESPONSE; KNOCKOUT MOUSE; LEUKOCYTE ACTIVATION; LITOMOSOIDES SIGMODONTIS; MACROPHAGE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TH1 CELL; TH2 CELL; WILD TYPE; WORM;

ANIMALS; DRUG SYNERGISM; FILARIASIS; FILARIOIDEA; INTERFERON TYPE II; INTERLEUKIN-5; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NEUTROPHILS; PHAGOCYTOSIS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0344851665     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.12.6978-6985.2003     Document Type: Article

References (47)

1. Alexander, J., A. R. Satoskar, and D. G. Russell. 1999. Leishmania species: models of intracellular parasitism. J. Cell Sci. 112:2993-3002.
2. Al-Qaoud, K. M., B. Fleischer, and A. Hoerauf. 1998. The Xid defect imparts susceptibility to experimental murine filariosis-association with a lack of antibody and IL-10 production by B cells in response to phosphorylcholine. Int. Immunol. 10:17-25.
3. Al-Qaoud, K. M., E. Pearlman, J. Klukowski, T. Hartung, B. Fleischer, and A. Hoerauf. 2000. A new mechanism for IL-5-dependent helminth control: neutrophil accumulation and neutrophil-mediated worm encapsulation in murine filariasis are abolished in the absence of IL-5. Int. Immunol. 12:899-908.
4. + T cells in controlling larval development. Infect. Immun. 65:2457-2461.
5. Babu, S., L. M. Ganley, T. R. Klei, L. D. Shultz, and T. V. Rajan. 2000. Role of gamma interferon and interleukin-4 in host defense against the human filarial parasite Brugia malayi Infect. Immun. 68:3034-3035.
6. Brattig, N., D. W. Büttner, and A. Hoerauf. 2001. Neutrophil accumulation around Onchocerca worms and chemotaxis of neutrophils are dependent on Wolbachia endobacteria. Microbes Infect. 3:439-446.
7. Braun, R. K., M. Franchini, F. Erard, S. Rihs, I. J. De Vries, K. Blaser, T. T. Hansel, and C. Walker. 1993. Human peripheral blood eosinophils produce and release interleukin-8 on stimulation with calcium ionophore. Eur. J. Immunol. 23:956-960.
8. Brunet, L. R., M. Beall, D. W. Dunne, and E. J. Pearce. 1997. IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J. Immunol. 159:777-785.
9. Brunet, L. R., M. Beall, D. W. Dunne, and E. J. Pearce. 1999. Nitric oxide and the Th2 response combine to prevent severe hepatic damage during Schistosoma mansoni infection. J. Immunol. 163:4976-4984.
10. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178:2243-2247.
11. Cooper, A. M., J. Magram, J. Ferrante, and I. M. Orme. 1997. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with Mycobacterium tuberculosis. J. Exp. Med. 186:39-45.
12. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742.
13. Doetze, A., J. Satoguina, G. Burchard, T. Rau, C. Löliger, B. Fleischer, and A. Hoerauf. 2000. Antigen-specific cellular hyporesponsiveness in generalized onchocerciasis is mediated by Th3/Tr1-type cytokines IL-10 and TGF-beta but not by a Th1 to Th2 shift. Int. Immunol. 12:623-630.
14. Etges, R., and I. Muller. 1998. Progressive disease or protective immunity to Leishmania major infection: the result of a network of stimulatory and inhibitory interactions. J. Mol. Med. 76:372-390.
15. Fallon, P. G., E. J. Richardson, G. J. McKenzie, and A. N. McKenzie. 2000. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164:2585-2591.
16. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249-2254.
17. Girard, D., R. Paquin, and A. D. Beaulieu. 1997. Responsiveness of human neutrophils to interleukin-4: induction of cytoskeletal rearrangements, de novo protein synthesis and delay of apoptosis. Biochem. J. 325:147-153.
18. Hartmann, S., A. Schönemeyer, B. Sonnenburg, B. Vray, and R. Lucius. 2002. Cystatins of filarial nematodes up-regulate the nitric oxide production of interferon-γ-activated murine macrophages. Parasite Immunol. 24:253-262.
19. Hoerauf, A., and N. Brattig. 2002. Resistance and susceptibility in human onchocerciasis-beyond Th1 vs. Th2. Trends Parasitol. 18:25-31.
20. Hoerauf, A., and B. Fleischer. 1997. Immune responses to filarial infection in laboratory mice. Med. Microbiol. Immunol. 185:207-215.
21. Johnson, E. H., M. Irvine, P. H. Kass, J. Browne, M. Abdullai, A. M. Prince, and S. Lustigman. 1994. Onchocerca volvulus: in vitro cytotoxic effects of human neutrophils and serum on third-stage larvae. Trop. Med. Parasitol. 45:331-335.
22. Johnson, E. H., S. Schynder-Candrian, T. V. Rajan, F. K. Nelson, S. Lustigman, and D. Abraham. 1998. Immune responses to third stage larvae of Onchocerca volvulus in interferon-gamma and interleukin-4 knockout mice. Parasite Immunol. 20:319-324.
23. Kobayashi, K., M. Kai, M. Gidoh, N. Nakata, M. Endoh, R. P. Singh, T. Kasama, and H. Saito. 1998. The possible role of interleukin (IL)-12 and interferon-gamma-inducing factor/IL-18 in protection against experimental Mycobacterium leprae infection in mice. Clin. Immunol. Immunopathol. 88:226-23l.
24. + B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4:15-24.
25. Lawrence, R. A. 1996. Lymphatic filariasis: what mice can tell us. Parasitol. Today 12:267-271.
26. Le Goff, L., T. J. Lamb, A. L. Graham, Y. Harcus, and J. E. Allen. 2002. IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. Int. J. Parasitol. 32:1277-1284.
27. Maclvor, D. M., S. D. Shapiro, C. T. Pham, A. Belaaouaj, S. N. Abraham, and T. J. Ley. 1999. Normal neutrophil function in cathepsin G-deficient mice. Blood 94:4282-4293.
28. Marechal, P., L. Goff, G. Petit, M. Diagne, D. W. Taylor, and O. Bain. 1996. The fate of the filaria Litomosoides Sigmodontis in susceptible and naturally resistant mice. Parasite 3:25-31.
29. Modlin, R. L. 1994. Th1-Th2 paradigm: insights from leprosy. J. Investig. Dermatol. 102:828-832.
30. Petit, G., M. Diagne, P. Marechal, D. Owen, D. Taylor, and O. Bain. 1992. Maturation of the filaria Litomosoides sigmodontis in BALB/c mice: comparative susceptibility of nine other inbred strains. Ann. Parasitol. Hum. Comp. 67:144-150.
31. Pfaff, A. W., H. Schulz-Key, P. T. Soboslay, S. M. Geiger, and W. H. Hoffmann. 2000. The role of nitric oxide in the innate resistance to microfilariae of Litomosoides sigmodontis in mice. Parasite Immunol. 22:397-405.
32. Rot, A. 1992. Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration. Immunol. Today 13:291-294.
33. Rubio de Krömer, M. T., M. Krömer, K. Luersen, and N. W. Brattig. 1998. Detection of a chemotactic factor for neutrophils in extracts of female Onchocerca volvulus. Acta Trop. 71:45-56.
34. Sabin, E. A., M. A. Kopf, and E. J. Pearce. 1996. Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils. J. Exp. Med. 184:1871-1878.
35. Saeftel, M., L. Volkmann, S. Korten, N. Brattig, K. M. Al-Qaoud, B. Fleischer, and A. Hoerauf. 2001. Lack of IFN-γ confers impaired neutrophil granulocyte function and imparts prolonged survival of adult filarial worms in murine filariasis. Microbes Infect. 3:203-213.
36. Sartono, E., Y. C. Kruize, A. Kurniawan, R. M. Maizels, and M. Yazdanbakhsh. 1997. Depression of antigen-specific interleukin-5 and interferon-gamma responses in human lymphatic filariasis as a function of clinical status and age. J. Infect. Dis. 175:1276-1280.
37. Satoguina, J., M. Mempel, J. Larbi, M. Badusche, C. Loliger, O. Adjei, G. Gachelin, B. Fleischer, and A. Hoerauf. 2002. Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 4:1291-1300.
38. Scott, P. 1991. IFN-gamma modulates the early development of Th1 and Th2 responses in a murine model of cutaneous leishmaniasis. J. Immunol. 147:3149-3155.
39. Taylor, M. J., H. F. Cross, and K. Bilo. 2000. Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. J. Exp. Med. 191:1429-1436.
40. Taylor, M. J., H. F. Cross, A. A. Mohammed, A. J. Trees, and A. E. Bianco. 1996. Susceptibility of Burgia 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.
41. Thomas, R., M. McCrossan, and M. Selkrik. 1997. Cytostatic and cytotoxic effects of activated macrophages and nitric oxide donors on Brugia malayi. Infect. Immun. 65:2732-2739.
42. Unanue, E. R. 1997. Inter-relationship among macrophages, natural killer cells and neutrophils in early stages of Listeria resistance. Curr. Opin. Immunol. 9:35-43.
43. Urban, J. F. J., K. B. Madden, A. W. Cheever, P. P. Trotta, I. M. Katona, and F. D. Finkelman. 1993. IFN inhibits inflammatory responses and protective immunity in mice infected with the nematode parasite, Nippostrongvlus brasiliensis. J. Immunol. 151:7086-7094.
44. Verhagen, C. E., T. C. van der Pouw Kraan, A. A. Buffing, M. A. Chand, W. R. Faber, L. A. Aarden, and P. K. Das. 1998. Type 1- and type 2-like lesional skin-derived Mycobacterium leprae-responsive T cell clones are characterized by coexpression of IFN-gamma/TNF-alpha and IL-4/IL-5/IL-13, respectively. J. Immunol. 160:2380-2387.
45. Volkmann, L., O. Bain, M. Saeftel, S. Specht, K. Fischer, F. Brombacher, K. I. Matthaei, and A. Hoerauf. 2002. Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different developmental stages. Med. Microbiol. Immunol. 191:23-31.
46. Volkmann, L., M. Saeftel, B. Fleischer, and A. Hoerauf. 2001. IL-4 is essential for the control of microfilariae in murine infection with the filaria Litomosoides sigmodontis. Infect. Immun. 69:2950-2956.
47. Wildenburg, G., A. Plenge-Bönig, A. Renz, P. Fischer, and D. W. Büttner. 1997. Distribution of mast cells and their correlation with inflammatory cells around Onchocerca gutturosa, O. tarsicola, O. ochengi, and O. flexuosa. Parasitol. Res. 83:109-120.