Basophil depletion downregulates Schistosoma mansoni egg-induced granuloma formation

Parasitology International

Volumn 62, Issue 6, 2013, Pages 508-513

  Anyan, William K ^a,b   Seki, Takenori ^a   Kumagai, Takashi ^a   Obata Ninomiya, Kazushige ^a   Furushima Shimogawara, Rieko ^a   Kwansa Bentum, Bethel ^a,b,c   Akao, Nobuaki ^a   Bosompem, Kwabena M ^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)

^c UNIVERSITY OF GHANA   (Ghana)

Author keywords

Ba103; Basophils; Egg granuloma; Parasite eggs; Schistosoma mansoni

Indexed keywords

INTERLEUKIN 4; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOPHIL; BASOPHIL DEPLETION; CELL INFILTRATION; CONTROLLED STUDY; DOWN REGULATION; EGG PARASITOID; FEMALE; GRANULOMA; GRANULOMATOUS INFLAMMATION; IMMUNOHISTOCHEMISTRY; LEUKOPENIA; LUNG GRANULOMA; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SPLEEN; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; LIVER; MALE; METABOLISM; OOCYTE; PATHOLOGY; SCHISTOSOMIASIS MANSONI;

MUS; SCHISTOSOMA MANSONI;

ANIMALS; ANTIBODIES, MONOCLONAL; BASOPHILS; DISEASE MODELS, ANIMAL; FEMALE; GRANULOMA; INTERLEUKIN-4; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OVUM; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SPLEEN;

EID: 84881162288     PISSN: 13835769     EISSN: 18730329     Source Type: Journal    
DOI: 10.1016/j.parint.2013.07.003     Document Type: Article

References (46)

1. Mathew R.C., Boros D.L. Anti-L3T4 antibody treatment suppresses hepatic granuloma formation and abrogates antigen-induced interleukin-2 production in Schistosoma mansoni infection. Infection and Immunity 1986, 54:820-826.
2. Jankovic D., Kullberg M.C., Noben-Trauth N., Caspar P., Ward J.M., Cheever A.W., et al. Schistosome-infected IL-4 receptor knockout (KO) mice, in contrast to IL-4 KO mice, fail to develop granulomatous pathology while maintaining the same lymphokine expression profile. Journal of Immunology 1999, 163:337-342.
3. Pearce E.J., MacDonald A.S. The immunobiology of schistosomiasis. Nature Reviews Immunology 2002, 2:499-511.
4. Wilson M.S., Mentink-Kane M.M., Pesce J.T., Ramalingam T.R., Thompson R., Wynn T.A. Immunopathology of schistosomiasis. Immunology and Cell Biology 2007, 85:148-154.
5. Fallon P.G., Richardson E.J., McKenzie G.J., McKenzie A.N. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. Journal of Immunology 2000, 164:2585-2591.
6. Schroeder J.T. Basophils: emerging roles in the pathogenesis of allergic disease. Immunological Reviews 2011, 242:144-160.
7. Karasuyama H., Wada T., Yoshikawa S., Obata K. Emerging roles of basophils in protective immunity against parasites. Trends in Immunology 2011, 32:125-130.
8. Kasugai T., Okada M., Morimoto M., Arizono N., Maeyama K., Yamada M., et al. Infection of Nippostrongylus brasiliensis induces normal increase of basophils in mast cell-deficient Ws/Ws rats with a small deletion at the kinase domain of c-kit. Blood 1993, 81:2521-2529.
9. Ohnmacht C., Voehringer D. Basophil effector function and homeostasis during helminth infection. Blood 2009, 113:2816-2825.
10. Voehringer D., Shinkai K., Locksley R.M. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 2004, 20:267-277.
11. Mukai K., Matsuoka K., Taya C., Suzuki H., Yokozeki H., Nishioka K., et al. Basophils play a critical role in the development of IgE-mediated chronic allergic inflammation independently of T cells and mast cells. Immunity 2005, 23:191-202.
12. Gibbs B.F. Human basophils as effectors and immunomodulators of allergic inflammation and innate immunity. Clinical and Experimental Medicine 2005, 5:43-49.
13. Karasuyama H., Mukai K., Tsujimura Y., Obata K. Newly discovered roles for basophils: a neglected minority gains new respect. Nature Reviews Immunology 2009, 9:9-13.
14. Costa J.J., Weller P.F., Galli S.J. The cells of the allergic response: mast cells, basophils, and eosinophils. JAMA: The Journal of the American Medical Association 1997, 278:1815-1822.
15. Arinobu Y., Iwasaki H., Gurish M.F., Mizuno S., Shigematsu H., Ozawa H., et al. Developmental checkpoints of the basophil/mast cell lineages in adult murine hematopoiesis. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:18105-18110.
16. Poorafshar M., Helmby H., Troye-Blomberg M., Hellman L. MMCP-8, the first lineage-specific differentiation marker for mouse basophils. Elevated numbers of potent IL-4-producing and MMCP-8-positive cells in spleens of malaria-infected mice. European Journal of Immunology 2000, 30:2660-2668.
17. Marone G., Triggiani M., de Paulis A. Mast cells and basophils: friends as well as foes in bronchial asthma?. Trends in Immunology 2005, 26:25-31.
18. Ugajin T., Kojima T., Mukai K., Obata K., Kawano Y., Minegishi Y., et al. Basophils preferentially express mouse Mast Cell Protease 11 among the mast cell tryptase family in contrast to mast cells. Journal of Leukocyte Biology 2009, 86:1417-1425.
19. Arock M., Merle-Béral H., Dugas B., Ouaaz F., Le Goff L., Vouldoukis I., et al. IL-4 release by human leukemic and activated normal basophils. Journal of Immunology 1993, 151:1441-1447.
20. Falcone F.H., Haas H., Gibbs B.F. The human basophil: a new appreciation of its role in immune responses. Blood 2000, 96:4028-4038.
21. Galli S.J., Kalesnikoff J., Grimbaldeston M.A., Piliponsky A.M., Williams C.M., Tsai M. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annual Review of Immunology 2005, 23:749-786.
22. Mack M., Schneider M.A., Moll C., Cihak J., Brühl H., Ellwart J.W., et al. Identification of antigen-capturing cells as basophils. Journal of Immunology 2005, 174:735-741.
23. Obata K., Mukai K., Tsujimura Y., Ishiwata K., Kawano Y., Minegishi Y., et al. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 2007, 110:913-920.
24. Tsujimura Y., Obata K., Mukai K., Shindou H., Yoshida M., Nishikado H., et al. Basophils play a pivotal role in immunoglobulin-G-mediated but not immunoglobulin-E-mediated systemic anaphylaxis. Immunity 2008, 28:581-589.
25. Perrigoue J.G., Saenz S.A., Siracusa M.C., Allenspach E.J., Taylor B.C., Giacomin P.R., et al. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nature Immunology 2009, 10:697-705.
26. 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.
27. Anyan W.K., Kumagai T., Shimogawara R.F., Seki T., Akao N., Obata K., et al. 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 2010, 38:13-22.
28. Falcone F.H., Dahinden C.A., Gibbs B.F., Noll T., Amon U., Hebestreit H., et al. Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. European Journal of Immunology 1996, 26:1147-1155.
29. Schramm G., Falcone F.H., Gronow A., Haisch K., Mamat U., Doenhoff M.J., et al. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. Journal of Biological Chemistry 2003, 278:18384-18392.
30. Sokol C.L., Barton G.M., Farr A.G., Medzhitov R. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nature Immunology 2008, 9:310-318.
31. Denzel A., Maus U.A., Rodriguez Gomez M., Moll C., Niedermeier M., Winter C., et al. Basophils enhance immunological memory responses. Nature Immunology 2008, 9:733-742.
32. Seki T., Kumagai T., Kwansa-Bentum B., Furushima-Shimogawara R., Anyan W.K., Miyazawa Y., et al. Interleukin-4 (IL-4) and IL-13 suppress excessive neutrophil infiltration and hepatocyte damage during acute murine schistosomiasis japonica. Infection and Immunity 2012, 80:159-168.
33. Fairfax K., Nascimento M., Huang S.C., Everts B., Pearce E.J. Th2 responses in schistosomiasis. Seminars in Immunopathology 2012, 34:863-871.
34. Dvorak A.M. The mouse basophil, a rare and rarely recognized granulocyte. Blood 2000, 96:1616-1617.
35. Urbina C., Ortiz C., Hurtado I. A new look at basophils in mice. International Archives of Allergy and Applied Immunology 1981, 66:158-160.
36. Phillips S.M., Lammie P.J. Immunopathology of granuloma formation and fibrosis in schistosomiasis. Parasitology Today 1986, 2:296-302.
37. Grzych J.M., Pearce E., Cheever A., Caulada Z.A., Caspar P., Heiny S., et al. Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. Journal of Immunology 1991, 146:1322-1327.
38. Chensue S.W., Terebuh P.D., Warmington K.S., Hershey S.D., Evanoff H.L., Kunkel S.L., et al. Role of IL-4 and IFN-gamma in Schistosoma mansoni egg-induced hypersensitivity granuloma formation. Orchestration, relative contribution, and relationship to macrophage function. Journal of Immunology 1992, 148:900-906.
39. Wynn T.A., Eltoum I., Cheever A.W., Lewis F.A., Gause W.C., Sher A. Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni. Journal of Immunology 1993, 151:1430-1440.
40. Cheever A.W., Poindexter R.W., Wynn T.A. Egg laying is delayed but worm fecundity is normal in SCID mice infected Schistosoma japonicum and S. mansoni with or without recombinant tumor necrosis factor alpha treatment. Infection and Immunity 1999, 67:2201-2208.
41. Williams M.E., Kullberg M.C., Barbieri S., Caspar P., Berzofsky J.A., Seder R.A., et al. Fc epsilon receptor-positive cells are a major source of antigen-induced interleukin-4 in spleens of mice infected with Schistosoma mansoni. European Journal of Immunology 1993, 23:1910-1916.
42. Phythian-Adams A.T., Cook P.C., Lundie R.J., Jones L.H., Smith K.A., Barr T.A., et al. CD11c depletion severely disrupts Th2 induction and development in vivo. The Journal of Experimental Medicine 2010, 207:2089-2096.
43. Dewals B., Hoving J.C., Leeto M., Marillier R.G., Govender U., Cutler A.J., et al. IL-4Ralpha responsiveness of non-CD4 T cells contributes to resistance in Schistosoma mansoni infection in pan-T cell-specific IL-4Ralpha-deficient mice. American Journal of Pathology 2009, 175:706-716.
44. Li L., Xia Y., Nguyen A., Lai Y.H., Feng L., Mosmann T.R., et al. Effects of Th2 cytokines on chemokine expression in the lung: IL-13 potently induces eotaxin expression by airway epithelial cells. Journal of Immunology 1999, 162:2477-2487.
45. Brown S.J., Galli S.J., Gleich G.J., Askenase P.W. Ablation of immunity to Amblyomma americanum by anti-basophil serum: cooperation between basophils and eosinophils in expression of immunity to ectoparasites (ticks) in guinea pigs. Journal of Immunology 1982, 129:790-796.
46. Wada T., Ishiwata K., Koseki H., Ishikura T., Ugajin T., Ohnuma N., et al. Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks. The Journal of Clinical Investigation 2010, 120:2867-2875.