Interleukin-4-promoted T helper 2 responses enhance Nippostrongylus brasiliensis-induced pulmonary pathology

Infection and Immunity

Volumn 76, Issue 12, 2008, Pages 5535-5542

  Mearns, Helen ^a,c   Horsnell, William G C ^a   Hoving, J Claire ^a   Dewals, Benjamin ^a   Cutler, Antony J ^a,d   Kirstein, Frank ^a   Myburgh, Elmarie ^a,e   Arendse, Berenice ^a   Brombacher, Frank ^a,b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^d NHS BLOOD AND TRANSPLANT   (United Kingdom)

^e UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; EOSINOPHIL; HOOKWORM INFECTION; IMMUNE RESPONSE; LUNG ALVEOLUS CELL; LUNG INFECTION; LYMPHOCYTE; MEDIASTINUM LYMPH NODE; MOUSE; MUCUS SECRETION; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; TH2 CELL;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-4; LUNG; MICE; MICE, KNOCKOUT; NIPPOSTRONGYLUS; STRONGYLIDA INFECTIONS; TH2 CELLS;

EID: 57349191517     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00210-08     Document Type: Article

References (43)

1. Barner, M., M. Mohrs, F. Brombacher, and M. Kopf. 1998. Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr. Biol. 8:669-672.
2. Bradding, P., J. A. Roberts, K. M. Britten, S. Montefort, R. Djukanovic, R. Mueller, C. H. Heusser, P. H. Howarth, and S. T. Holgate. 1994. Interleukin-4, -5, and -6 and tumor necrosis factor-alpha in normal and asthmatic airways: evidence for the human mast cell as a source of these cytokines. Am. J. Respir. Cell Mol. Biol. 10:471-480.
3. Brombacher, F. 2000. The role of interleukin-13 in infectious diseases and allergy. Bioessays 22:646-656.
4. Coffman, R. L., J. Ohara, M. W. Bond, J. Carty, A. Zlotnik, and W. E. Paul. 1986. B cell stimulatory factor-1 enhances the IgE response of lipopolysaccharide-activated B cells. J. Immunol. 136:4538-4541.
5. Cohn, L., R. J. Homer, H. MacLeod, M. Mohrs, F. Brombacher, and K. Bottomly. 1999. Th2-induced airway mucus production is dependent on IL-4Ralpha, but not on eosinophils. J. Immunol. 162:6178-6183.
6. Cohn, L., R. J. Homer, A. Marinov, J. Rankin, and K. Bottomly. 1997. Induction of airway mucus production by T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production. J. Exp. Med. 186:1737-1747.
7. Cohn, L., J. S. Tepper, and K. Bottomly. 1998. IL-4-independent induction of airway hyperresponsiveness by Th2, but not Th1, cells. J. Immunol. 161:3813-3816.
8. Cunningham, A. F., K. Serre, K. M. Toellner, M. Khan, J. Alexander, F. Brombacher, and I. C. MacLennan. 2004. Pinpointing IL-4-independent acquisition and IL-4-influenced maintenance of Th2 activity by CD4 T cells. Eur. J. Immunol. 34:686-694.
9. Dubucquoi, S., P. Desreumaux, A. Janin, O. Klein, M. Goldman, J. Tavernier, A. Capron, and M. Capron. 1994. Interleukin 5 synthesis by eosinophils: association with granules and immunoglobulin-dependent secretion. J. Exp. Med. 179:703-708.
10. Dunn, A., and A. Keymer. 1986. Factors affecting the reliability of the Mc-Master technique. J. Helminthol. 60:260-262.
11. Finkelman, F. D., T. Shea-Donohue, S. C. Morris, L. Gildea, R. Strait, K. B. Madden, L. Schopf, and J. F. Urban, Jr. 2004. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201:139-155.
12. Holgate, S. T. 1999. The epidemic of allergy and asthma. Nature 402:B2-4.
13. Holland, M. J., Y. M. Harcus, A. Balic, and R. M. Maizels. 2005. Th2 induction by Nippostrongylus secreted antigens in mice deficient in B cells, eosinophils or MHC class I-related receptors. Immunol. Lett. 96:93-101.
14. Horsnell, W. G., A. J. Cutler, C. J. Hoving, H. Mearns, E. Myburgh, B. Arendse, F. D. Finkelman, G. K. Owens, D. Erle, and F. Brombacher. 2007. Delayed goblet cell hyperplasia, acetylcholine receptor expression, and worm expulsion in SMC-specific IL-4Ralpha-deficient mice. PLoS Pathog. 3:e1.
15. + lymphocytes with a Th2 cytokine profile. J. Immunol. 164:3047-3055.
16. Kopf, M., G. Le Gros, M. Bachmann, M. C. Lamers, H. Bluethmann, and G. Kohler. 1993. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362:245-248.
17. Madden, K. B., J. F. Urban, Jr., H. J. Ziltener, J. W. Schrader, F. D. Finkelman, and I. M. Katona. 1991. Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis. J. Immunol. 147:1387-1391.
18. Marsland, B. J., M. Kurrer, R. Reissmann, N. L. Harris, and M. Kopf. 2008. Nippostrongylus brasiliensis infection leads to the development of emphysema associated with the induction of alternatively activated macrophages. Eur. J. Immunol. 38:479-488.
19. Matsuda, S., Y. Tani, M. Yamada, K. Yoshimura, and N. Arizono. 2001. Type 2-biased expression of cytokine genes in lung granulomatous lesions induced by Nippostrongylus brasiliensis infection. Parasite Immunol. 23:219-226.
20. Mattes, J., M. Yang, A. Siqueira, K. Clark, J. MacKenzie, A. N. McKenzie, D. C. Webb, K. I. Matthaei, and P. S. Foster. 2001. IL-13 induces airways hyperreactivity independently of the IL-4R alpha chain in the allergic lung. J. Immunol. 167:1683-1692.
21. McKenzie, G. J., A. Bancroft, R. K. Grencis, and A. N. McKenzie. 1998. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr. Biol. 8:339-342.
22. McNeil, K. S., D. P. Knox, and L. Proudfoot. 2002. Anti-inflammatory responses and oxidative stress in Nippostrongylus brasiliensis-induced pulmonary inflammation. Parasite Immunol. 24:15-22.
23. Mohrs, M., C. Holscher, and F. Brombacher. 2000. Interleukin-4 receptor alpha-deficient BALB/c mice show an unimpaired T helper 2 polarization in response to Leishmania major infection. Infect. Immun. 68:1773-1780.
24. Mohrs, M., B. Ledermann, G. Kohler, A. Dorfmuller, A. Gessner, and F. Brombacher. 1999. Differences between IL-4- and IL-4 receptor alpha-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 162:7302-7308.
25. Mohrs, M., K. Shinkai, K. Mohrs, and R. M. Locksley. 2001. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15:303-311.
26. Mosmann, T. R., and R. L. Coffman. 1989. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:145-173.
27. Nelms, K., A. D. Keegan, J. Zamorano, J. J. Ryan, and W. E. Paul. 1999. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17:701-738.
28. + T cell-specific deletion of IL-4 receptor alpha prevents ovalbumin-induced anaphylaxis by an IFN-gamma-dependent mechanism. J. Immunol. 179:2758-2765.
29. + T cell IL-4 production is revealed in IL-4 receptor-deficient mice. Proc. Natl. Acad. Sci. USA 94:10838-10843.
30. Radwanska, M., A. J. Cutler, J. C. Hoving, S. Magez, C. Holscher, A. Bohms, B. Arendse, R. Kirsch, T. Hunig, J. Alexander, P. Kaye, and F. Brombacher. 2007. Deletion of IL-4Ralpha on CD4 T cells renders BALB/c mice resistant to Leishmania major Infection. PLoS Pathog. 3:e68.
31. Ritz, S. A., M. J. Cundall, B. U. Gajewska, D. Alvarez, J. C. Gutierrez-Ramos, A. J. Coyle, A. N. McKenzie, M. R. Stampfli, and M. Jordana. 2002. Granulocyte macrophage colony-stimulating factor-driven respiratory mucosal sensitization induces Th2 differentiation and function independently of interleukin-4. Am. J. Respir. Cell Mol. Biol. 27:428-435.
32. Svetic, A., K. B. Madden, X. D. Zhou, P. Lu, I. M. Katona, F. D. Finkelman, J. F. Urban, Jr., and W. C. Gause. 1993. A primary intestinal helminthic infection rapidly induces a gut-associated elevation of Th2-associated cytokines and IL-3. J. Immunol. 150:3434-3441.
33. Tomita, M., T. Kobayashi, H. Itoh, T. Onitsuka, and Y. Nawa. 2000. Goblet cell hyperplasia in the airway of Nippostrongylus brasiliensis-infected rats. Respiration 67:565-569.
34. Urban, J. F., Jr., I. M. Katona, W. E. Paul, and F. D. Finkelman. 1991. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc. Natl. Acad. Sci. USA 88:5513-5517.
35. Urban, J. F., Jr., N. Noben-Trauth, D. D. Donaldson, K. B. Madden, S. C. Morris, M. Collins, and F. D. Finkelman. 1998. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8:255-264.
36. Venkayya, R., M. Lam, M. Willkom, G. Grunig, D. B. Corry, and D. J. Erle. 2002. The Th2 lymphocyte products IL-4 and IL-13 rapidly induce airway hyperresponsiveness through direct effects on resident airway cells. Am. J. Respir. Cell Mol. Biol. 26:202-208.
37. Vitetta, E. S., J. Ohara, C. D. Myers, J. E. Layton, P. H. Krammer, and W. E. Paul. 1985. Serological, biochemical, and functional identity of B cell-stimulatory factor 1 and B cell differentiation factor for IgG1. J. Exp. Med. 162:1726-1731.
38. Voehringer, D., T. A. Reese, X. Huang, K. Shinkai, and R. M. Locksley. 2006. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J. Exp. Med. 203:1435-1446.
39. Voehringer, D., K. Shinkai, and R. M. Locksley. 2004. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 20:267-277.
40. Webb, D. C., S. Mahalingam, Y. Cai, K. I. Matthaei, D. D. Donaldson, and P. S. Foster. 2003. Antigen-specific production of interleukin (IL)-13 and IL-5 cooperate to mediate IL-4Ralpha-independent airway hyperreactivity. Eur. J. Immunol. 33:3377-3385.
41. Whittaker, L., N. Niu, U. A. Temann, A. Stoddard, R. A. Flavell, A. Ray, R. J. Homer, and L. Cohn. 2002. Interleukin-13 mediates a fundamental pathway for airway epithelial mucus induced by CD4 T cells and interleukin-9. Am. J. Respir. Cell Mol. Biol. 27:593-602.
42. Zhao, A., J. McDermott, J. F. Urban, Jr., W. Gause, K. B. Madden, K. A. Yeung, S. C. Morris, F. D. Finkelman, and T. Shea-Donohue. 2003. Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J. Immunol. 171:948-954.
43. Zurawski, G., and J. E. de Vries. 1994. Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol. Today 15:19-26.