T cell-derived IL-4/IL-13 protects mice against fatal schistosoma mansoni infection independently of basophils

Journal of Immunology

Volumn 193, Issue 7, 2014, Pages 3590-3599

  Schwartz, Christian ^a   Oeser, Katharina ^a   Da Costa, Clarissa Prazeres ^b   Layland, Laura E ^c   Voehringer, David ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; TUMOR NECROSIS FACTOR ALPHA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALTERNATIVELY ACTIVATED MACROPHAGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHELMINTIC ACTIVITY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BASOPHIL; BASOPHILIA; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EFFECTOR CELL; EOSINOPHIL; GENE DELETION; GENE IDENTIFICATION; GRANULOMATOSIS; HOST PARASITE INTERACTION; HUMORAL IMMUNITY; IL13 GENE; IL4 GENE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOGLOBULIN PRODUCTION; IMMUNOREGULATION; INNATE IMMUNITY; KNOCKOUT MOUSE; LIVER GRANULOMA; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MACROPHAGE; MACROPHAGE ACTIVATION; MAST CELL; MORTALITY; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TH1 CELL; TH2 CELL; WEIGHT REDUCTION; WORM EGG; ANIMAL; BAGG ALBINO MOUSE; GENETICS; GRANULOMA; IMMUNOLOGY; LIVER; PARASITOLOGY; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; BASOPHILS; GRANULOMA; IMMUNOGLOBULIN E; INTERLEUKIN-13; INTERLEUKIN-4; LIVER; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TH2 CELLS;

EID: 84907200774     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401155     Document Type: Article

References (60)

1. Hotez, P. J., P. J. Brindley, J. M. Bethony, C. H. King, E. J. Pearce, and J. Jacobson. 2008. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 118: 1311-1321.
2. Fairfax, K., M. Nascimento, S. C. Huang, B. Everts, and E. J. Pearce. 2012. Th2 responses in schistosomiasis. Semin. Immunopathol. 34: 863-871.
3. Pearce, E. J., and A. S. MacDonald. 2002. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2: 499-511.
4. Wynn, T. A., R. W. Thompson, A. W. Cheever, and M. M. Mentink-Kane. 2004. Immunopathogenesis of schistosomiasis. Immunol. Rev. 201: 156-167.
5. Pearce, E. J., P. Caspar, J. M. Grzych, F. A. Lewis, and A. Sher. 1991. Downregulation of Th1 cytokine production accompanies induction of Th2 responses b y a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 173: 159-166.
6. Pearce, E. J., C. M. Kane, J. Sun, J. J. Taylor, A. S. McKee, and L. Cervi. 2004. Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol. Rev. 201: 117-126.
7. Doenhoff, M. J., R. H. Curtis, J. Ngaiza, and J. Modha. 1990. Proteases in the schistosome life cycle: a paradigm for tumour metastasis. Cancer Metastasis Rev. 9: 381-392.
8. Asch, H. L., and M. H. Dresden. 1979. Acidic thiol proteinase activity of Schistosoma mansoni egg extracts. J. Parasitol. 65: 543-549.
9. Kloetzel, K. 1968. A collagenaselike substance produced by eggs of Schistosoma mansoni. J. Parasitol. 54: 177-178.
10. Amiri, P., R. M. Locksley, T. G. Parslow, M. Sadick, E. Rector, D. Ritter, and J. H. McKerrow. 1992. Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice. Nature 356: 604-607.
11. Buchanan, R. D., D. P. Fine, and D. G. Colley. 1973. Schistosoma mansoni infection in mice depleted of thymus-dependent lymphocytes. II. Pathology and altered pathogenesis. Am. J. Pathol. 71: 207-218.
12. Hernandez, H. J., Y. Wang, N. Tzellas, and M. J. Stadecker. 1997. Expression of class II, but not class I, major histocompatibility complex molecules is required for granuloma formation in infection with Schistosoma mansoni. Eur. J. Immunol. 27: 1170-1176.
13. Mathew, R. C., and D. L. Boros. 1986. Anti-L3T4 antibody treatment suppresses hepatic granuloma formation and abrogates antigen-induced interleukin-2 production i n Schistosoma mansoni infection. Infect. Immun. 54: 820-826.
14. Brunet, L. R., F. D. Finkelman, A. W. Cheever, M. A. Kopf, and E. J. Pearce. 1997. IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. J. Immunol. 159: 777-785.
15. Fallon, P. G., E. J. Richardson, G. J. McKenzie, and A. N. McKenzie. 2000. Schistosome infection of transgenic mice defines dist inct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164: 2585-2591.
16. Hoffmann, K. F., A.W. Cheever, and T. A. Wynn. 2000. IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 164: 6406-6416.
17. Neill, D. R., S. H. Wong, A. Bellosi, R. J. Flynn, M. Daly, T. K. Langford, C. Bucks, C. M. Kane, P. G. Fallon, R. Pannell, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370.
18. Herbert, D. R., C. Hö lscher, M. Mohrs, B. Arendse, A. Schwegmann, M. Radwanska, M. Leeto, R. Kirsch, P. Hall, H. Mossmann, et al. 2004. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20: 623-635.
19. Herbert, D. R., T. Orekov, C. Perkins, M. E. Rothenberg, and F. D. Finkel man. 2008. IL-4R alpha expression by bone marrow-derived cells is necessary and sufficient for host protection against acute schistosomiasis. J. Immunol. 180: 4948-4955.
20. Shimoda, K., J. van Deursen, M. Y. Sangster, S. R. Sarawar, R. T. Carson, R. A. Tripp, C. Chu, F. W. Quelle, T. Nosaka, D. A. Vignali, et al. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nat ure 380: 630-633.
21. Lebman D.A.,R.L. Coffman, 1988, Interleukin 4 causes isotype switching to IgE in T cell-stimulated clonal B cell cultures, J. Exp. Med., 168, 853-862.
22. Dunne, D. W., A. E. Butterworth, A. J. Fulford, H. C. Kariuki, J. G. Langley, J. H. Ouma, A. Capron, R. J. Pierce, and R. F. Sturrock. 1992. Immunity after treatment of human schistosomiasis: association b etween IgE antibodies to adult worm antigens and resistance to reinfection. Eur. J. Immunol. 22: 1483-1494.
23. Byram, J. E., M. J. Doenhoff, R. Musallam, L. H. Brink, and F. von Lichtenberg. 1979. Schistosoma mansoni infections in T-cell deprived mice, and the ameliorating effect of administering homologous chronic infection serum. II. Pathology. Am. J. Trop. Med. Hyg. 28: 274-285.
24. Doenhoff, M., R. Musall am, J. Bain, and A. McGregor. 1979. Schistosoma mansoni infections in T-cell deprived mice, and the ameliorating effect of administering homologous chronic infection serum. I. Pathogenesis. Am. J. Trop. Med. Hyg. 28: 260-2 63.
25. Doenhoff, M. J., S. Pearson, D. W. Dunne, Q. Bickle, S. Lucas, J. Bain, R. Musallam, and O. Hassounah. 1981. Immunological control of hepatotoxicity and parasite egg excretion in Schistosoma mansoni infections: stage specificity of the reactivity of immune s erum in T-cell deprived mice. Trans. R. Soc. Trop. Med. Hyg. 75: 41-53.
26. Fairfax, K. C., E. Amiel, I. L. King, T. C. Freitas, M. Mohrs, and E. J. Pearce . 2012. IL-10R blockade during chronic schistosomiasis mansoni results in the loss of B cells from the liver and the development of severe pulmonary disease. PLoS Pathog. 8: e1002490.
27. Jankovic, D., A. W. Chee ver, M. C. Kullberg, T. A. Wynn, G. Yap, P. Caspar, F. A. Lewis, R. Clynes, J. V. Ravetch, and A. Sher. 1998. CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent me chanism requiring Fc receptor signaling. J. Exp. Med. 187: 619-629.
28. MacDonald, A. S., E. A. Patton, A. C. La Flamme, M. I. Araujo, C. R. Huxtable, B. Bauman, and E. J. Pearce. 2002. Im paired Th2 development and increased mortality during Schistosoma mansoni infection in the absence of CD40/CD154 interaction. J. Immunol. 168: 4643-4649.
29. 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.
30. Perrigoue, J. G., S. A. Saenz, M. C. Siracusa, E. J. Allenspach, B. C. Taylor, P. R. Giacomin, M. G. Nair, Y. Du, C. Zaph, N. van Rooijen, et al. 2009. MHC class II-dependent basop hil-CD4+ T cell interactions promote T(H)2 cytokinedependent immunity. Nat. Immunol. 10: 697-705.
31. Ohnmacht, C., C. Schwartz, M. Panzer, I. Schiedewitz, R. Naumann, and D. Voehringer. 2010. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 33: 364-374.
32. Ohnmacht, C., and D. Voehringer. 2010. Basophils protect against reinfection with hookworms independently of mast cells and memory Th2 cells. J. Immunol. 184: 344-350.
33. Wada, T., K. Ishiwata, H. Koseki, T. Ishikura, T. Ugajin, N. Ohnuma, K. Obata, R. Ishikawa, S. Yoshikawa, K. Mukai, et al. 2010. Selective ablation of basophils in mice reveals their nonredundant role in acquired immunity against ticks. J. Clin. Invest. 120: 2867-2875.
34. Min, B., M. Prout, J. Hu-Li, J . Zhu, D. Jankovic, E. S. Morgan, J. F. Urban, Jr., A. M. Dvorak, F. D. Finkelman, G. LeGros, and W. E. Paul. 2004. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J. Exp. Med. 200: 507-517.
35. Schramm, G., K. Mohrs, M. Wodrich, M. J. Doenhoff, E. J. Pearce, H. Haas, and M. Mohrs. 2007. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni egg s, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J. Immunol. 178: 6023-6027.
36. Phythian-Adams, A. T., P. C. Cook, R. J. Lundie, L. H. Jones, K. A. Smith, T. A. Barr, K. Hochweller, S. M. Anderton, G. J. Hämmerling, R. M. Maizels, and A. S. MacDonald. 2010. CD11c depletion severely disrupts Th2 induction and development in vivo. J. Exp. Med. 207: 2089-2096.
37. Sullivan, B. M., H. E. Liang, J. K. Bando, D. Wu, L. E. Cheng, J. K. McKerrow, C. D. Allen, and R. M. Locksley. 2011. Genetic analysis of basophil function in vivo. Nat. Immunol. 12: 527-535.
38. McKenzie, G. J., P. G. Fallon, C. L. Emson, R. K. Grencis, and A. N. McKenzie. 1999. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediate d responses. J. Exp. Med. 189: 1565-1572.
39. Voehringer, D., D. Wu, H. E. Liang, and R. M. Locksley. 2009. Efficient generation of long-distance conditional alleles using recombineering and a dual selection strategy in replicate plates. BMC Biotechnol. 9: 69.
40. Lee, P. P., D. R. Fitzpatrick, C. Beard, H. K. Jessup, S. Lehar, K. W. Makar, M. Pérez-Melgosa, M. T. Sweetser, M. S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15: 763-774.
41. Mohrs, M., K. S hinkai, K. Mohrs, and R. M. Locksley. 2001. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15: 303-311.
42. Layland L. E.,J. Mages,C. Loddenkemper,A. Hoerauf,H. Wagner,R. Lang,.C. U. da Costa., 2010. Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J. Immunol., 184, 713-724.
43. Swartz, J. M., K. D. Dyer, A. W. Cheever, T. Ramalingam, L. Pesnicak, J. B. Domachowske, J. J. Lee, N. A. Lee, P. S. Foster, T. A. Wynn, and H. F. Rosenberg. 2006. Schistosoma mansoni infection in eosinophil lineageablated mice. Blo od 108: 2420-2427.
44. Chiaramonte, M. G., L. R. Schopf, T. Y. Neben, A. W. Cheever, D. D. Donaldson, and T. A. Wynn. 1999. IL-13 is a key regulatory cytokine for Th2 cell-mediated pulmonary g ranuloma formation and IgE responses induced by Schistosoma mansoni eggs. J. Immunol. 162: 920-930.
45. Mallevaey, T., J. Fontaine, L. Breuilh, C. Paget, A. Castro-Keller, C. Vendeville, M. Capron, M. Leite-de-Moraes, F. Trottein, and C. Faveeuw. 2007. Invariant and noninvariant natural killer T cells exert opposite regulatory functions on the immune response during murine schistosomiasis. Infect. Immun. 75: 2171-2180.
46. Schneider, E., M. B. Tonanny, M. Lisbonne, M. Leite-de-Moraes, and M. Dy. 2004. Pro-Th1 cytokines promote Fas-dependent apoptosis of immature peripheral basophils. J. Immunol. 172: 5262-5268.
47. Mitre, E., R. T. Taylor, J. Kubofcik, and T. B. Nutman. 2004. Parasite antigendriven basophils are a major source of IL-4 in human filarial infections. J. Immunol. 172: 2439-2445.
48. Falcone, F. H., C. A. Dahinden, B. F. Gibbs, T. Noll, U. Amon, H. Hebestreit, O. Abrahamsen, J. Klaucke, M. Schlaak, and H. Haas. 1996. Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. Eur. J. Immunol. 26: 1147-1155.
49. Anyan, W. K., T. Seki, T. Kumagai, K. Obata-Ninomiya, R. Furushima-Shimogawara, B. Kwansa-Bentum, N. Akao, K. M. Bosom pem, D. A. Boakye, M. D. Wilson, et al. 2013. Basophil depletion downregulates Schistosoma mansoni egg-induced granuloma formation. Parasitol. Int. 62: 508-513.
50. Kojima, T., K. Obata, K. Mukai, S. Sato, T. Takai, Y. Minegishi, and H. Karasuyama. 2007. Mast cells and basophils are selectively activated in vitro and in vivo through CD200R3 in an IgE-independent manner. J. Immunol. 179: 7093-7100.
51. Sher, A., R. L. Coffman, S. Hieny, P. Scott, and A. W. Cheever. 1990. Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc . Natl. Acad. Sci. USA 87: 61-65.
52. Moore, D. L., D. I. Grove, and K. S. Warren. 1977. The Schistosoma mansoni egg granuloma: quantitation of cell populations. J. Pathol. 121: 41-50.
53. Butterworth, A. E., R. F. Sturrock, V. Houba, A. A. Mahmoud, A. Sher, and P. H. Rees. 1975. Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature 256: 727-729.
54. Martinez, F. O., L. Helming, and S. Gordon. 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27: 451-483.
55. Nair, M. G., Y. Du, J. G. Perrigoue, C. Zaph, J. J. Taylor, M. Goldschmidt, G. P. Swain, G. D. Yancopoulos, D. M. Valenzuela, A. Murphy, et al. 2009. Alternatively activated macrophage-de rived RELM-alpha is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 206: 937-952.
56. Huber, S., R. Hoffmann, F. Muskens, and D. Voehringer. 2010. Alternatively activated macrophages inhibit T-cell proliferation by Stat6-dependent expression of PD-L2. Blood 116: 3311-3320.
57. Bronte, V., P. Serafini, A. Mazzoni, D. M. Segal, and P. Zanovello. 2003. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol. 24: 302-306.
58. Pesce, J. T., T. R. Ramalingam, M. M. Mentink-Kane, M. S. Wilson, K. C. El Kasmi, A. M. Smith, R. W. Thompson, A. W. Cheever, P. J. Murray, and T. A. Wynn. 2009. Arginase-1-expressing macrophages suppress Th2 cytokinedriven inflammation and fibrosis. PLoS Pathog. 5: e1000371.
59. Pesce, J. T., T. R. Ram alingam, M. S. Wilson, M. M. Mentink-Kane, R. W. Thompson, A. W. Cheever, J. F. Urban, Jr., and T. A. Wynn. 2009. Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity. PLoS Pathog. 5: e1000393.
60. Ndlovu, H., and F. Brombacher. 2013. Role of IL-4Ra during acute schistosomiasis in mice. Parasite Immunol. DOI: 10.1111/pim.12080.