Role of adult worm antigen-specific immunoglobulin E in acquired immunity to Schistosoma mansoni infection in baboons

Infection and Immunity

Volumn 67, Issue 2, 1999, Pages 636-642

  Nyindo, Mramba ^a   Kariuki, Thomas M ^a   Mola, Paul W ^a   Farah, Idle O ^a   Elson, Lynne ^a   Blanton, Ronald E ^b   King, Christopher L ^b  

^a INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PRAZIQUANTEL; RECOMBINANT INTERLEUKIN 12;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BABOON; CERCARIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNITY; INFECTION RESISTANCE; LYMPHOCYTE PROLIFERATION; MALE; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

EID: 0032964316     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.2.636-642.1999     Document Type: Article

References (53)

1. Andrew, S. M., and J. A. Titus. 1992. Antibody detection and preparation, p. 2.7.4-2.7.6. In J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober (ed.), Current protocols in immunology, vol. 1. John Wiley & Sons, New York, N.Y.
2. Bliss, J., V. Van Cleave, K. Murray, A. Wiencis, M. Ketchum, R. Maylor, T. Haire, C. Resmini, A. K. Abbas, and S. F. Wolf. 1996. IL-12, as an adjuvant, promotes a T helper 1 cell, but does not suppress a T helper 2 cell recall response. J. Immunol. 156:887-894.
3. Boulanger, D., G. D. Reid, R. F. Sturrock, I. Wolowczuk, J. M. Balloul, D. Grezel, R. J. Pierce, M. F. Otieno, S. Guerret, J. A. Grimaud, et al. 1991. Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunol. 13:473-490.
4. Butterworth, A. E. 1987. Immunity in human schistosomiasis. Acta Trop. 12(Suppl.):31-40.
5. Capron, A., J.-P. Dessaint, M. Capron, M. Joseph, and J. Pestel. 1980. Role of anaphylactic antibodies in immunity to schistosomes. Am. J. Trop. Med. Hyg. 29:849-857.
6. Capron, A., J. P. Dessaint, M. Capron, and H. Bazin. 1975. Specific IgE antibodies in immune adherence of normal macrophages to Schistosoma mansoni schistosomules. Nature 253:474-475.
7. Capron, A., J. P. Dessaint, M. Capron, J. H. Ouma, and A. E. Butterworth. 1987. Immunity to schistosomes: progress toward vaccine. Science 238:1065-1072.
8. Capron, M., and A. Capron. 1994. Immunoglobulin E and effector cells in schistosomiasis. Science 264:1876-1877.
9. Cheever, A. W., R. E. Kuntz, B. J. Myers, J. A. Moore, and T. C. Huang. 1974. Schistosomiasis haematobia in African, hamadryas, and gelada baboons. Am. J. Trop. Med. Hyg. 23:429-448.
10. Damian, R. T., N. D. Greene, and K. Fitzgerald. 1974. Schistosomiasis mansoni in baboons. II. Acquisition of immunity to challenge infection after repeated small exposures to cercariae of Schistosoma mansoni. Am. J. Trop. Med. Hyg. 23:78-80.
11. Damian, R. T., N. D. Greene, T. Suzuki, and D. A. Dean. 1981. Schistosomiasis mansoni in baboons. V. Antibodies and immediate hypersensitivity in multiply infected Papio cynocephalus. Am. J. Trop. Med. Hyg. 30:836-843.
12. Dunne, D. W., A. E. Butterworth, A. J. Fulford, J. H. Ouma, and R. F. Sturrock. 1992. Human IgE responses to Schistosoma mansoni and resistance to reinfection. Mem. Inst. Oswaldo Cruz 87:99-103.
13. Farah, I. O., and M. Nyindo. 1996. Schistosoma mansoni induces in the Kenyan baboon a novel intestinal pathology that is manifestly modulated by an irradiated cercarial vaccine. J. Parasitol. 82:601-607.
14. Farah, I. O., M. Nyindo, M. A. Suleman, J. Nyaundi, T. M. Kariuki, R. E. Blanton, L. H. Elson, and C. L. King. 1997. Schistosoma mansoni: development and modulation of the granuloma after single or multiple exposures in the baboon (Papio cynocephalus anubis). Exp. Parasitol. 86:93-101.
15. Fenwick, A. 1969. Baboons as reservoir hosts of Schistosoma mansoni. Trans. R. Soc. Trop. Med. Hyg. 63:557-567.
16. Germann, T., S. Guckes, M. Bongartz, H. Dlugonska, E. Schmitt, L. Kolbe, E. Kolsch, F. J. Podlaski, M. K. Gately, and E. Rude. 1995. Administration of IL-12 during ongoing immune responses fails to permanently suppress and can even enhance the synthesis of antigen-specific IgE. Int. Immunol. 7: 1649-1657.
17. Greene, N. D. 1974. Schistosoma mansoni: IgG and IgE skin-sensitizing antibodies in infected baboons. Exp. Parasitol. 35:219-224.
18. Greene, N. D., and R. T. Damian. 1972. Skin-sensitizing antibodies in Schistosoma mansoni infected baboons: evidence for the presence of two types. Proc. Soc. Exp. Biol. Med. 141:291-294.
19. Hagan, P. 1992. Reinfection, exposure and immunity in human schistosomiasis. Parasitol. Today 8:12-16.
20. Hagan, P., U. J. Blumenthal, D. Dunn, A. J. Simpson, and H. A. Wilkins. 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349:243-245.
21. Harn, D. A., M. Mitsuyama, and J. R. David. 1984. Schistosoma mansoni. Anti-egg monoclonal antibodies protect against cercarial challenge in vivo. J. Exp. Med. 159:1371-1387.
22. Higashi, G. I., A. M. El-Asfahani, M. N. El-Bolkainy, E. W. Chu, and M. Raafat. 1980. Assessment of immediate and delayed hypersensitivity skin tests with Schistosoma mansoni adult worm antigen in a rural Egyptian population. Trop. Geogr. Med. 32:245-250.
23. Hussain, R., R. G. Hamilton, V. Kumaraswami, N. F. Adkinson, and E. A. Ottesen. 1981. IgE response in human filariasis. I. Quantitation of filaria-specific IgE. J. Immunol. 127:1623-1629.
24. Jankovic, D., M. C. Kullberg, D. Dombrowicz, S. Barbieri, P. Caspar, T. A. Wynn, W. E. Paul, A. W. Cheever, J. P. Kinet, and A. Sher. 1997. Fc epsilonR1-deficient mice infected with Schistosoma mansoni mount normal Th2-type responses while displaying enhanced liver pathology. J. Immunol. 159:1868-1875.
25. Joseph, M., A. Capron, A. E. Butterworth, R. F. Sturrock, and V. Houba. 1978. Cytotoxicity of human and baboon mononuclear phagocytes against schistosomula in vitro: induction by immune complexes containing IgE and Schistosoma mansoni antigens. Clin. Exp. Immunol. 33:48-56.
26. Kigoni, E. P., P. P. X. Elsas, H. L. Lenzi, and A. J. Dessein. 1986. IgE antibody and resistance to infection. II. Effect of IgE suppression on the early and late skin reaction and resistance of rats to Schistosoma mansoni infection. Eur. J. Immunol. 16:589.
27. King, C. L., J. Xianli, I. Malhotra, S. Liu, A. A. Mahmoud, and H. C. Oettgen. 1997. Mice with a targeted deletion of the IgE gene have increased worm burdens and reduced granulomatous inflammation following primary infection with Schistosoma mansoni. J. Immunol. 158:294-300.
28. Koster, B., and M. Strand. 1994. Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes. Parasitology 108: 433-446.
29. Lobos, E. 1997. The basis of IgE responses to specific antigenic determinants in helminthiasis. Chem. Immunol. 66:1-25.
30. Mahanty, S., C. L. King, V. Kumaraswami, J. Regunathan, A. Maya, K. Jayaraman, J. S. Abrams, E. A. Ottesen, and T. B. Nutman. 1993. IL-4- and IL-5-secreting lymphocyte populations are preferentially stimulated by parasite-derived antigens in human tissue invasive nematode infections. J. Immunol. 151:3704-3711.
31. Medhat, A., M. Shehata, K. Bucci, S. Mohamed, A. Diab, S. Badary, H. Galal, M. Nafeh, and C. L. King. 1998. Increased interleukin-4 and interleukin-5 production in response to Schistosoma haematobium adult worm antigens correlates with lack of reinfection after treatment. J. Infect. Dis. 178:512-519.
32. Miller, J. H. 1960. Papio doguera (dog face baboon), a primate reservoir host of Schistosoma mansoni in East Africa. Trans. R. Soc. Trop. Med. Hyg. 54:44-53.
33. Mutapi, F., P. D. Ndhlovu, P. Hagan, J. T. Spicer, T. Mduluza, C. M. Turner, S. K. Chandiwana, and M. E. Woolhouse. 1998. Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. J. Infect. Dis. 178:289-293.
34. Reid, G. D., R. F. Sturrock, R. A. Harrison, and R. P. Tarara. 1995. Schistosoma haematobium in the baboon (Papio anubis): assessment of protection levels against either a single mass challenge or repeated trickle challenges after vaccination with irradiated schistosomula. J. Helminthol. 69:139-147.
35. Rempel, J. D., M. Wang, and K. T. HayGlass. 1997. In vivo IL-12 administration induces profound but transient commitment to T helper cell type 1-associated patterns of cytokine and antibody production. J. Immunol. 159: 1490-1496.
36. Rihet, P., C. E. Demeure, A. Bourgois, A. Prata, and A. J. Dessein. 1991. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur. J. Immunol. 21:2679-2686.
37. Roberts, M., A. E. Butterworth, G. Kimani, T. Kamau, A. J. Fulford, D. W. Dunne, J. H. Ouma, and R. F. Sturrock. 1993. Immunity after treatment of human schistosomiasis: association between cellular responses and resistance to reinfection. Infect. Immun. 61:4984-4993.
38. Sher, A., R. Correa-Oliveira, S. Hieny, and R. Hussain. 1983. Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. IV. Analysis of the role of IgE antibodies and mast cells. J. Immunol. 131:1460-1465.
39. Smythies, L. E., P. S. Coulson, and R. A. Wilson. 1992. Monoclonal antibody to IFN-gamma modifies pulmonary inflammatory responses and abrogates immunity to Schistosoma mansoni in mice vaccinated with attenuated cercariae. J. Immunol. 149:3654-3658.
40. Soisson, L. A., G. D. Reid, I. O. Farah, M. Nyindo, and M. Strand. 1993. Protective immunity in baboons vaccinated with a recombinant antigen or radiation-attenuated cercariae of Schistosoma mansoni is antibody-dependent. J. Immunol. 151:4782-4789.
41. Sturrock, R. F., A. E. Butterworth, and V. Houba. 1976. Schistosoma mansoni in the baboon (Papio anubis): parasitological responses of Kenyan baboons to different exposures of a local parasite strain. Parasitology 73:239-252.
42. Sturrock, R. F., A. E. Butterworth, V. Houba, S. D. Karamsadkar, and R. Kimani. 1978. Schistosoma mansoni in the Kenyan baboon (Papio anubis): the development and predictability of resistance to homologous challenge. Trans. R. Soc. Trop. Med. Hyg. 72:251-261.
43. Sturrock, R. F., B. J. Cottrell, and R. Kimani. 1984. Observations on the ability of repeated, light exposures to Schistosoma mansoni cercariae to induce resistance to reinfection in Kenyan baboons (Papio anubis). Parasitology 88:505-514.
44. Sturrock, R. F., B. J. Cottrell, S. Lucas, G. D. Reid, H. M. Seitz, and R. A. Wilson. 1988. Observations on the implications of pathology induced by experimental schistosomiasis in baboons in evaluating the development of resistance to challenge infection. Parasitology 96:37-48.
45. Sturrock, R. F., C. James, E. R. James, and G. Webbe. 1980. Immunization of baboons (Papio anubis) against Schistosoma haematobium with irradiated cercariae or schistosomula. Trans. R. Soc. Trop. Med. Hyg. 74:834-835. (Letter.)
46. Suzuki, T., and R. T. Damian. 1981. Schistosomiasis mansoni in baboons. IV. The development of antibodies to Schistosoma mansoni adult worm, egg, and cercarial antigens during acute and chronic infections. Am. J. Trop. Med. Hyg. 30:825-835.
47. Vella, A. T., and E. J. Pearce. 1992. CD4+ Th2 response induced by Schistosoma mansoni eggs develops rapidly, through an early, transient, Th0-like stage. J. Immunol. 148:2283-2290.
48. Velupillai, P., and D. A. Harn. 1994. Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: a mechanism for regulation of CD4+ T-cell subsets. Proc. Natl. Acad. Sci. USA 91:18-22.
49. Verwaerde, C., C. Auriault, M. Damonneville, J. L. Neyrinck, C. Vendeville, and A. Capron. 1986. Role of serine proteases of Schistosoma mansoni in the regulation of IgE synthesis. Scand. J. Immunol 24:509-516.
50. Verwaerde, C., C. Auriault, J. L. Neyrinck, and A. Capron. 1988. Properties of serine proteases of Schistosoma mansoni schistosomula involved in the regulation of IgE synthesis. Scand. J. Immunol. 27:17-24.
51. Webbe, G., C. James, G. S. Nelson, S. R. Smithers, and R. J. Terry. 1976. Acquired resistance to Schistosoma haematobium in the baboon (Papio anubis) after cercarial exposure and adult worm transplantation. Ann. Trop. Med. Parasitol. 70:411-424.
52. Webster, M., P. G. Fallon, A. J. Fulford, A. E. Butterworth, J. H. Ouma, G. Kimani, and D. W. Dunne. 1997. Effect of praziquantel and oxamniquine treatment on human isotype responses to Schistosoma mansoni: elevated IgE to adult worm. Parasite Immunol. 19:333-335.
53. Yole, D. S., R. Pemberton, G. D. Reid, and R. A. Wilson. 1996. Protective immunity to Schistosoma mansoni induced in the olive baboon Papio anubis by the irradiated cercaria vaccine. Parasitology 112:37-46.