Schistosome eggs have a direct role in the induction of basophils capable of a high level of IL-4 production: Comparative study of single-and bisexual infection of schistosoma mansoni in vivo

Tropical Medicine and Health

Volumn 38, Issue 1, 2010, Pages 13-22

  Anyan, William K ^a,b   Kumagai, Takashi ^a   Shimogawara, Rieko F ^a   Seki, Takenori ^a   Akao, Nobuaki ^a   Obata, Kazushige ^a   Kwansa Bentum, Bethel ^a,b   Bosompem, Kwabena Mante ^b   Boakye, Daniel A ^b   Wilson, Michael D ^b   Karasuyama, Hajime ^a   Ohta, Nobuo ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b University of Ghana   (Ghana)

Author keywords

Basophils; Eggs antigens; Granuloma; Immunoregulation; Schsitosoma mansoni

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOPHIL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE MODEL; EGG PRODUCTION; FEMALE; FLOW CYTOMETRY; HOST PARASITE INTERACTION; IN VIVO STUDY; LEUKOCYTE ACTIVATION; LEUKOCYTE COUNT; LIVER GRANULOMA; MOUSE; NONHUMAN; PARASITE VIRULENCE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SPLEEN CELL; SPLENOMEGALY; TH1 CELL; TH2 CELL; TIME; UPREGULATION;

EID: 77953447529     PISSN: 13488945     EISSN: 13494147     Source Type: Journal    
DOI: 10.2149/tmh.2009-24     Document Type: Article

References (43)

1. World Health Organization (WHO). Report on the Regional Workshop on comprehensive approaches for schistosomiasis control. Alexandria, June 1993, WHO-EM
2. Southgate VR. Schistosomiasis in the Senegal River Basin: before and after the construction of the dams at Diama, Senegal and Manantali, Mali and future prospects. J Helminthol 1997; 71: 125-132.
3. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Tropica 2000; 7: 41-51.
4. Phillips SM, Linette GP, Doughty BL, Byram JE, von Lichtenberg F. In vivo T cell depletion regulates resistance and morbidity in murine schistosomiasis. J Immunol 1987; 139: 919-926.
5. Pearce EJ, MacDonald AS. The immunobiology of schis-tosomiasis. Nat Immunol 2002; 2: 499-511.
6. Grzych JM, Pearce E, Cheever A, Caulada Z.A, Caspar P, Hieny S, Lewis FA, Sher, A. Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol 1991; 146: 1322.
7. Hirata M, Fukuma T. Cytokine regulation in experimentally induced Schistosoma japonicum egg granuloma formation. Parasitol Int 2003; 52: 341-349.
8. Pearce EJ, Kane CM, Sun J, Taylor JJ, McKees AS, Cervi L. Th2 response polarization during infection with the helminth parasite Schistosoma manosoni. Immunol Rev 2004; 201: 117-126.
9. Capron M, Capron A. Effector function of eosinophils in schistosomiasis. Mem Inst Oswaldo Cruz 1992; 87: 167-172.
10. + T cells acts in an autocrine manner to induce Th2 differentiation. Eur J Immunol 2002; 32: 1428-1433.
11. Haas H, Falcone FH, Schramm G, Haisch K, Gibbs BF, Klaucke J, Poppelmann M, Becker, Gabius HJ, Schlaak M. Dietary lectins can induce in vitro release of IL-4 and IL-13 from human basophils. Eur J Immunol 1999; 29: 918-927.
12. Shinkai K, Mohr, M, Locksley RM. Helper T cells regulate type 2 innate immunity in vivo. Nature 2000; 420: 825-829.
13. Seder RA, Paul WE, Dvorak AM, Sharkis SJ, Kagey-Sobotka A, Niv Y, Finkelman FD, Barbieri SA, Galli, Plaut M. Mouse splenic and bone marrow cell populations that express highaffinity Fce receptors and produce interleukin 4 are highly enriched in basophils. Proc Natl Acad Sci USA 1991; 88: 2835-2839.
14. Arock M, Merle-Beral H, Dugas B, Ougas B, Ouaaz F, Goff LL, Vouldoukis I, Menciahuerta JM, Schmitt C, Leblond-Missenard V, Debre P. IL-4 release by human leukemic and activated normal basophils. J Immunol 1993; 151: 1441-1447.
15. Gibbs BF, Haas H, Wolff H, Grabbe J. Early IgEdependent release of IL-4 and IL-13 from leukocytes is restricted to basophils: a comparison with other granulocytes and mononuclear cells. Inflamm Res 2000; 49 (Spl. 1): S9-S10.
16. Gessner A, Mohrs K, Mohrs M. Mast cells, basophils and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J Immunol 2005; 174: 1063-1072.
17. Min B, Prout M, Hu-Li J, Zhu J, Jankovic D, Morgan ES, Urban JF, Dvorak AM, Finkelman FD, LeGros G, Paul WE. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 2004; 200: 507-517.
18. Gibbs BF. Human basophils as effectors and immunomodulators of allergic inflammation and innate immunity. Clin Exp Med 2005; 5: 43-49.
19. Oh K, Shen T, Le Gros G, Min B. Induction of Th2 type immunity in a mouse system reveals a novel immunoregulatory role of basophils. Blood 2007; 109: 2921-2927.
20. Sokol CL, Barton GM, Farr AG, Medzhitov RA. Mechanism for the initiation of allergeninduced T helper type 2 responses. Nature Immunol 2008; 9: 310-318.
21. Karasuyama H, Mukai K, Tsujimura Y, Obata K. Newlydiscovered roles for basophils: a neglected minority gains new respect. Nat Rev Immunol, 2009; 9: 9-13.
22. Costa JJ, Weller PF, Galli SJ. The cells of the allergic response. Mast cells, basophils, and eosinophils. JAMA 1997; 278: 1815-1822.
23. Marone G, Trigiani M, de Paulis A. Mast cells and basophils: friend as well as foes in bronchial asthma? Trends Immunol 2004; 26: 26-31.
24. Falcone FH, Haas H, Gibbs BF. The human basophil: a new appreciation of its role in immune responses. Blood 2000; 96: 4028-4038.
25. Obata K, Mukai K, Tsujimura Y, Ishiwata K, Kawano Y, Minegeshi Y, Watanabe N, Karasuyama H. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 2007; 110: 913-920.
26. Tsujimura Y, Obata K, Mukai K, Shindo H, Yoshida N, Nishikado H, Kawano Y, Minegishi Y, Shimizu T, Karasuyama H. Basophils play a pivotal role in immunoglobulin -G-mediated but not immunoglobulin-Emediated systemic anaphylaxis. Immunity 2008; 28: 581-589.
27. Denzel A, Maus UA, Gonmez M R, Moll C, Niedermeier M, Winter C, Maus R, Hollingshead S, Brile, DR, Kunz-Schughart LA, Talke Y, Mack M. Basophils enhance immunological memory responses. Nature Immunol 2008; 9: 733-742.
28. Schramm G, Gronow A, Knobloch J, Wippersteg V, Grevelding CG, Galle J, Fuller H, Stanley RG, Chiodini PL, Haas H, Doenhoff MJ. IPSE/alpha-1: a major immunogenic component secreted from Schistosoma mansoni eggs. Mol Biochem Parasitol 2006; 147: 9-19.
29. Wynn TA, Eltoum I, Oswald IP, Cheever AW, Sher A. Endogenous interleukin 12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogenous IL-12 both inhibits and prophylatically immunizes against egg pathology. J Exp Med 1994; 179: 1551-1561.
30. Smithers SR, Terry RJ. The infection of laboratory host with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 1965; 55: 695-700.
31. Pinelli E, Brandes S, Dormans J, Fonville M, Hamilton CM, Der GJ. Toxocara canis: effect of pulmonary pathology and cytokine expression in BALB/c mice. Exp Parasitol 2007; 115: 76-82.
32. + T lymphocytes correlates with down regulation of Th1 cytokine synthesis in helminth infection. J Immunol 1991; 147: 2713-2716.
33. Capron M, Capron A. Immunoglobulin E and effector cells in schistosomiasis. Science 1994; 264: 1876-1877.
34. Falcone HF, Dahinden CA, Gibbs BE, Noll T, Amon U, Hebestreit H, Abramamsen O, Klaucke J, Schlaak M, Haas H. Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. Eur J Immunol 1996; 26: 1147-1155.
35. Schramm G, Falcone FH, Cronow A, Haischi K, Mamat U, Doenhoff MJ, Olivera G, Galle J, Dahinden CA, Haas H. Molecular characterizationof an interleukin-4-inducing factor from Schistosoma mansoni eggs. J Biol Chem 2003; 278: 18384-18392.
36. Shaw JR, Erasmus DA. Schistoma mansoni; an examination of the reproductive status of females from single sex infection. Parasitol 1981; 82: 121-124.
37. Warren KS. The secret of the immunopathogenesis of schistosomiasis: In vivo models. Immunol Rev 1982; 61: 189-213.
38. Williams ME, Kullberg MC, Barbieri S, Caspar P, Berzofsky JA, Seder RA, Sher A Fc epsilon receptor-positive cells are a major source of antigen-induced interleukin-4 in spleens of mice infected with Schistosoma mansoni. Eur J Immunol 1993; 23: 1910-1916.
39. Mukai K, Matsuoka K, Taya C, Suzuki H, Yokozaki H, Nishioka K, Hirokawa K, Etori M, Yamashita M, Kubota T, Minegishi Y, Yonekawa H, Kayasuyama H. Basophils play a critical role in the development of IgEmediated chronic allergic inflammation independently of T cells and mast cells. Immunity 2005; 23: 191-202.
40. Chensue SW, Terebuh PD, Warmington KS, Hershey SD, Evanoff HK, Kunkel SL, Higashi GI. Role of IL-4 and INFg in Schistosoma mansoni egg-induced hypersentivity granuloma formation: Ochestration, relative contribution, and relationship to macrophage function. J Immunol 1992; 148: 900-906.
41. Wedemeyer J, Tsai, M, Galli SJ. Roles of mast cells and basophils in innate and acquired immunity. Curr Opin Immunol 2000; 12: 624-631.
42. Mitre E, Taylor R, Kunofcik J, Nutman TB. Parasite antigen-driven basophils are a major source of IL-4 in human filarial infections. J Immunol 2004; 172: 2439-2445.
43. Min B, Le Gros G, Paul WE. Basophils: a potential liaison between innate and adaptive immunity. Allergol Int 2006; 55: 99-104.