Specificity and Mechanism of Immunoglobulin M (IgM)- and IgG-Dependent Protective Immunity to Larval Strongyloides stercoralis in Mice

Infection and Immunity

Volumn 71, Issue 12, 2003, Pages 6835-6843

  Ligas, Jessica A ^a   Kerepesi, Laura A ^a   Galioto, Ann Marie ^a   Lustigman, Sara ^b   Nolan, Thomas J ^c   Schad, Gerhard A ^c   Abraham, David ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b NEW YORK BLOOD CENTER   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYCHOLIC ACID; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 5;

ACTIVE IMMUNIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CONTROLLED STUDY; EOSINOPHIL; GRANULOCYTE; HOST PARASITE INTERACTION; IMMUNITY; IMMUNOELECTRON MICROSCOPY; KNOCKOUT MOUSE; LARVA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURIFICATION; STRONGYLOIDES STERCORALIS; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, HELMINTH; ANTIBODY SPECIFICITY; HUMANS; IMMUNE SERA; IMMUNIZATION; IMMUNIZATION, PASSIVE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN-5; LARVA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, FC; STRONGYLOIDES STERCORALIS; STRONGYLOIDIASIS;

EID: 0345283117     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.12.6835-6843.2003     Document Type: Article

References (41)

1. Abraham, D., H. L. Rotman, H. F. Haberstroh, W. Yutanawiboonchai, R. A. Brigandi, O. Leon, T. J. Nolan, and G. A. Schad. 1995. Strongyloicles stercoralis: protective immunity to third-stage larvae in BALB/cByJ mice. Exp. Parasitol. 80:297-307.
2. Anwar, A. R., S. R. Smithers, and A. B. Kay. 1979. Killing of schistosomula of Schistosoma mansoni coated with antibody and/or complement by human leukocytes in vitro: requirement for complement in preferential killing by eosinophils. J. Immunol. 122:628-637.
3. Bell, R. G., J. A. Appleton, D. A. Negrao-Correa, and L. S. Adams. 1992. Rapid expulsion of Trichinella spiralis in adult rats mediated by monoclonal antibodies of distinct IgG isotypes. Immunology 75:520-527.
4. Brigandi, R. A., H. L. Rotman, W. Yutanawiboonchai, O. Leon, T. J. Nolan, G. A. Schad, and D. Abraham. 1996. Strongyloides stercoralis: role of antibody and complement in immunity to the third stage of larvae in BALB/cByJ mice. Exp. Parasitol. 82:279-289.
5. Carvalho, E. M., T. M. Andrade, J. A. Andrade, and H. Rocha. 1983. Immunological features in different clinical forms of strongyloidiasis. Trans. R. Soc. Trop. Med. Hyg. 77:346-349.
6. Coxon, A., X. Cullere, S. Knight, S. Sethi, M. W. Wakelin, G. Stavrakis, F. W. Luscinskas, and T. N. Mayadas. 2001. Fc gamma RIII mediates neutrophil recruitment to immune complexes. A mechanism for neutrophil accumulation in immune-mediated inflammation. Immunity 14:693-704.
7. de Messias, I. J., R. M. Genta, and W. D. Mohren. 1994. Adherence of monocytes and polymorphonuclear cells to infective larvae of Strongyloides stercoralis after complement activation. J. Parasitol. 80:267-274.
8. Egwang, T. G., J. Gauldie, and D. Befus. 1984. Complement-dependent killing of Nippostrongylus brasiliensis infective larvae by rat alveolar macrophages. Clin. Exp. Immunol. 55:149-156.
9. Genta, R. M., J. S. Harper III, A. A. Gam, W. I. London, and F. A. Neva. 1984. Experimental disseminated strongyloidiasis in Erythrocebus patas. II. Immunology. Am. J. Trop. Med. Hyg. 33:444-450.
10. Goes, A. M., and F. J. Ramalho-Pinto. 1991. Protective immunity to Schistosoma mansoni in mice is dependent on antibody and complement but not on radiosensitive leukocytes. Immunol. Lett. 28:57-63.
11. Gray, C. A., and R. A. Lawrence. 2002. A role for antibody and Fc receptor in the clearance of Brugia malayi microfilariae. Eur. J. Immunol. 32:1114-1120.
12. Grove, D. I., and C. Northern. 1982. Infection and immunity in dogs infected with a human strain of Strongloides stercoralis. Trans. R. Soc. Trop. Med. Hyg. 76:833-838.
13. Hall, L. R., E. Diaconu, and E. Pearlman. 2001. A dominant role for Fc gamma receptors in antibody-dependent corneal inflammation. J. Immunol. 167:919-925.
14. Hanski, C., M. Naumann, A. Grutzkau, G. Pluschke, B. Friedrich, H. Hahn, and E. O. Riecken. 1991. Humoral and cellular defense against intestinal murine infection with Yersinia enterocolitica. Infect. Immun. 59:1106-1111.
15. Herbert, D. R., J. J. Lee, N. A. Lee, T. J. Nolan, G. A. Schad, and D. Abraham. 2000. Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J. Immunol. 165:4544-4551.
16. Herbert, D. R., T. J. Nolan, G. A. Schad, and D. Abraham. 2002. The role of B cells in immunity against larval Strongyloides stercoralis in mice. Parasite Immunol. 24:95-101.
17. Herbert, D. R., T. J. Nolan, G. A. Schad, S. Lustigman, and D. Abraham. 2002. Immunoaffinity-isolated antigens induce protective immunity against larval Strongyloides stereoralis in mice. Exp. Parasitol. 100:112-120.
18. Hestdal, K., F. W. Ruscetti, J. N. Ihle, S. E. Jacobsen, C. M. Dubois, W. C. Kopp, D. L. Longo, and J. R. Keller. 1991. Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J. Immunol. 147:22-28.
19. Irvine, M., T. Huima, A. M. Prince, and S. Lustigman. 1994. Identification and characterization of an Onchocerca volvulus cDNA clone encoding a highly immunogenic calponin-like protein. Mol. Biochem. Parasitol. 65:135-146.
20. Kopf, M., F. Brombacher, P. D. Hodgkin, A. J. Ramsay, E. A. Milbourne, W. J. Dai, K. S. Ovington, C. A. Behm, G. Kohler, I. G. Young, and K. I. Matthaei. 1996. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4:15-24.
21. Lustigman, S., B. Brotman, T. Huima, and A. M. Prince. 1991. Characterization of an Onchocerca volvulus cDNA clone encoding a genus specific antigen present in infective larvae and adult worms. Mol. Biochem. Parasitol. 45:65-75.
22. Lustigman, S., J. H. McKerrow, K. Shah, J. Lui, T. Huima, M. Hough, and B. Brotman. 1996. Cloning of a cysteine protease required for the molting of Onchocerca volvulus third stage larvae. J. Biol. Chem. 271:30181-30189.
23. McGonigle, S., E. R. Yoho, and E. R. James. 2001. Immunisation of mice with fractions derived from the intestines of Dirofilaria immitis. Int. J. Parasitol. 31:1459-1466.
24. Medeiros, F., C. I. Baldwin, and D. A. Denham. 1996. Brugia pahangi in cats: the passive transfer of anti-microfilarial immunity from immune to non-immune cats. Parasite Immunol. 18:79-86.
25. Murrell, K. D. 1981. Protective role of immunoglobulin G in immunity to Strongyloides ratti. J. Parasitol. 67:167-173.
26. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97:8841-8848.
27. Nolan, T. J., H. L. Rotman, V. M. Bhopale, G. A. Schad, and D. Abraham. 1995. Immunity to a challenge infection of Strongyloides stercoralis third-stage larvae in the jird. Parasite Immunol. 17:599-604.
28. Onah, D. N., F. Uchiyama, Y. Nagakui, M. Ono, T. Takai, and Y. Nawa. 2000. Mucosal defense against gastrointestinal nematodes: responses of mucosal mast cells and mouse mast cell protease 1 during primary Strongyloides venezuelensis infection in FcRγ-knockout mice. Infect. Immun. 68:4968-4971.
29. Penttila, I. A., P. L. Ey, and C. R. Jenkin. 1984. Infection of mice with Nematospiroides dubius: demonstration of neutrophil-mediated immunity in vivo in the presence of antibodies. Immunology 53:147-154.
30. Pinder, M., A. Leclerc, and S. Everaere. 1992. Antibody-dependent cell-mediated immune reactions to Loa loa microfilariae in amicrofilaraemic subjects. Parasite Immunol. 14:541-556.
31. Rotman, H. L., S. Schnyder-Candrian, P. Scott, T. J. Nolan, G. A. Schad, and D. Abraham. 1997. IL-12 eliminates the Th-2 dependent protective immune response of mice to larval Strongyloides stercoralis. Parasite Immunol. 19:29-39.
32. Rotman, H. L., W. Yutanawiboonchai, R. A. Brigandi, O. Leon, G. J. Gleich, T. J. Nolan, G. A. Schad, and D. Abraham. 1996. Strongyloides stercoralis: eosinophil-dependent immune-mediated killing of third stage larvae in BALB/cByJ mice. Exp. Parasitol. 82:267-278.
33. Schad, G. A., M. E. Hellman, and D. W. Muncey. 1984. Strongyloides stercoralis: hyperinfection in immunosuppressed dogs. Exp. Parasitol. 57:287-296.
34. Shaio, M. F., S. C. Hou, J. G. Chen, C. C. Wu, K. D. Yang, and F. Y. Chang. 1990. Immunoglobulin G-dependent classical complement pathway activation in neutrophil-mediated cytotoxicity to infective larvae of Angiostrongylus cantonensis. Ann. Trop. Med. Parasitol. 84:185-191.
35. Smith, T. S., E. A. Munn, M. Graham, A. S. Tavernor, and C. A. Greenwood. 1993. Purification and evaluation of the integral membrane protein H11 as a protective antigen against Haemonchus contortus. Int. J. Parasitol. 23:271-280.
36. Smith, W. D., S. K. Smith, and J. M. Murray. 1994. Protection studies with integral membrane fractions of Haemonchus contortus. Parasite Immunol. 16:231-241.
37. Takai, T., M. Li, D. Sylvestre, R. Clynes, and J. V. Ravetch. 1994. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76: 519-529.
38. Venturiello, S. M., G. H. Giambartolomei, and S. N. Costantino. 1993. Immune killing of newborn Trichinella larvae by human leucocytes. Parasite Immunol. 15:559-564.
39. Vignali, D. A., Q. D. Bickle, M. G. Taylor, G. Tennent, and M. B. Pepys. 1988. Comparison of the role of complement in immunity to Schistosoma mansoni in rats and mice. Immunology 63:55-61.
40. Watanabe, K., K. Noda, S. Hamano, M. Koga, K. Kishihara, K. Nomoto, and I. Tada. 2000. The crucial role of granulocytes in the early host defense against Strongyloides ratti infection in mice. Parasitol. Res. 86: 188-193.
41. Williams, D. J., and J. M. Behnke. 1983. Host protective antibodies and serum immunoglobulin isotypes in mice chronically infected or repeatedly immunized with the nematode parasite Nematospiroides dubius. Immunology 48:37-47.