Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system

Journal of Experimental Medicine

Volumn 203, Issue 6, 2006, Pages 1435-1446

  Voehringer, David ^a   Reese, Tiffany A ^a   Huang, Xiaozhu ^a   Shinkai, Kanade ^a   Locksley, Richard M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 4;

ANIMAL MODEL; ARTICLE; BASOPHIL; BRONCHUS HYPERREACTIVITY; CELL DIFFERENTIATION; CELLULAR IMMUNITY; EOSINOPHIL; HELMINTHIASIS; HEMATOPOIETIC CELL; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LYMPH NODE; MOUSE; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT DISEASE; TISSUE REACTION; WORM EXPULSION;

ANIMALS; ANTIBODIES, HELMINTH; EOSINOPHILS; FLOW CYTOMETRY; HEMATOPOIESIS; IMMUNITY, NATURAL; IMMUNOGLOBULIN E; INFLAMMATION; INTERLEUKIN-13; INTERLEUKIN-4; LUNG; LYMPH NODES; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MODELS, ANIMAL; NIPPOSTRONGYLUS; STRONGYLIDA INFECTIONS; TH2 CELLS;

EID: 33745036694     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052448     Document Type: Article

References (51)

1. Cliffe, L.J., N.E. Humphreys, T.E. Lane, C.S. Potten, C. Booth, and R.K. Grencis. 2005. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science. 308:1463-1465.
2. 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.
3. 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.
4. Cunningham, A.F., P.G. Fallon, M. Khan, S. Vacheron, H. Acha-Orbea, I.C. MacLennan, A.N. McKenzie, and K.M. Toellner. 2002. Th2 activities induced during virgin T cell priming in the absence of IL-4, IL-13, and B cells. J. Immunol. 169:2900-2906.
5. Urban, J.F., Jr., C.R. Maliszewski, K.B. Madden, I.M. Katona, and F.D. Finkelman. 1995. IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. J. Immunol. 154:4675-4684.
6. 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.
7. Kuperman, D.A., X. Huang, L.L. Koth, G.H. Chang, G.M. Dolganov, Z. Zhu, J.A. Elias, D. Sheppard, and D.J. Erle. 2002. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8:885-889.
8. Grunig, G., M. Warnock, A.E. Wakil, R. Venkayya, F. Brombacher, D.M. Rennick, D. Sheppard, M. Mohrs, D.D. Donaldson, R.M. Locksley, and D.B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science. 282:2261-2263.
9. Morimoto, M., J. Whitmire, S. Xiao, R.M. Anthony, H. Mirakami, R.A. Star, J.F. Urban Jr., and W.C. Gause. 2004. Peripheral CD4 T cells rapidly accumulate at the host: parasite interface during an inflammatory Th2 memory response. J. Immunol. 172:2424-2430.
10. Noben-Trauth, N., L.D. Shultz, F. Brombacher, J.F. Urban Jr., H. Gu, and W.E. Paul. 1997. An interleukin 4 (IL-4)-independent pathway for CD4+ T cell IL-4 production is revealed in IL-4 receptor-deficient mice. Proc. Natl. Acad. Sci. USA. 94:10838-10843.
11. Finkelman, F.D., S.C. Morris, T. Orekhova, M. Mori, D. Donaldson, S.L. Reiner, N.L. Reilly, L. Schopf, and J.F. Urban Jr. 2000. Stat6 regulation of in vivo IL-4 responses. J. Immunol. 164:2303-2310.
12. 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.
13. Jankovic, D., M.C. Kullberg, N. Noben-Trauth, P. Caspar, W.E. Paul, and A. Sher. 2000. Single cell analysis reveals that IL-4 receptor/Stat6 signaling is not required for the in vivo or in vitro development of CD4+ lymphocytes with a Th2 cytokine profile. J. Immunol. 164:3047-3055.
14. 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-mediated responses. J. Exp. Med. 189:1565-1572.
15. Horsley, V., K.M. Jansen, S.T. Mills, and G.K. Pavlath. 2003. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell. 113:483-494.
16. Nakajima, H., G.J. Gleich, and H. Kita. 1996. Constitutive production of IL-4 and IL-10 and stimulated production of IL-8 by normal peripheral blood eosinophils. J. Immunol. 156:4859-4866.
17. Gessner, A., K. Mohrs, and M. Mohrs. 2005. 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. 174:1063-1072.
18. Scheu, S., D.B. Stetson, R.L. Reinhardt, J.H. Leber, M. Mohrs, and R.M. Locksley. 2006. Activation of the integrated stress response during T helper cell differentiation. Nat. Immunol. In press.
19. Ikeda, R.K., M. Miller, J. Nayar, L. Walker, J.Y. Cho, K. McElwain, S. McElwain, E. Raz, and D.H. Broide. 2003. Accumulation of peribronchial mast cells in a mouse model of ovalbumin allergen induced chronic airway inflammation: modulation by immunostimulatory DNA sequences. J. Immunol. 171:4860-4867.
20. Lee, N.A., M.P. McGarry, K.A. Larson, M.A. Horton, A.B. Kristensen, and J.J. Lee. 1997. Expression of IL-5 in thymocytes/T cells leads to the development of a massive eosinophilia, extramedullary eosinophilopoiesis, and unique histopathologies. J. Immunol. 158:1332-1344.
21. Yu, C., A.B. Cantor, H. Yang, C. Browne, R.A. Wells, Y. Fujiwara, and S.H. Orkin. 2002. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J. Exp. Med. 195:1387-1395.
22. Daly, C.M., G. Mayrhofer, and L.A. Dent. 1999. Trapping and immobilization of Nippostrongylus brasiliensis larvae at the site of inoculation in primary infections of interleukin-5 transgenic mice. Infect. Immun. 67:5315-5323.
23. Shin, E.H., Y. Osada, J.Y. Chai, N. Matsumoto, K. Takatsu, and S. Kojima. 1997. Protective roles of eosinophils in Nippostrongylus brasiliensis infection. Int. Arch. Allergy Immunol. 114:45-50.
24. Katona, I.M., J.F. Urban Jr., and F.D. Finkelman. 1988. The role of L3T4+ and Lyt-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J. Immunol. 140:3206-3211.
25. Wills-Karp, M. 2004. Interleukin-13 in asthma pathogenesis. Immunol. Rev. 202:175-190.
26. Noben-Trauth, N., J. Hu-Li, and W.E. Paul. 2000. Conventional, naive CD4+ T cells provide an initial source of IL-4 during Th2 differentiation. J. Immunol. 165:3620-3625.
27. Liu, Z., Q. Liu, H. Hamed, R.M. Anthony, A. Foster, F.D. Finkelman, J.F. Urban Jr., and W.C. Gause. 2005. IL-2 and autocrine IL-4 drive the in vivo development of antigen-specific Th2 T cells elicited by nematode parasites. J. Immunol. 174:2242-2249.
28. Fearon, D.T., and R.M. Locksley. 1996. The instructive role of innate immunity in the acquired immune response. Science. 272:50-53.
29. Coffman, R.L., and T. von der Weid. 1997. Multiple pathways for the initiation of T helper 2 (Th2) responses. J. Exp. Med. 185:373-375.
30. Urban, J.F., Jr., N. Noben-Trauth, L. Schopf, K.B. Madden, and F.D. Finkelman. 2001. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J. Immunol. 167:6078-6081.
31. Spencer, L., L. Shultz, and T.V. Rajan. 2003. T cells are required for host protection against Brugia malayi but need not produce or respond to interleukin-4. Infect. Immun. 71:3097-3106.
32. 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.
33. Mitchell, L.A., R.B. Wescott, and L.E. Perryman. 1983. Kinetics of expulsion of the nematode, Nippostrongylus brasiliensis, in mast-cell deficient W/WV mice. Parasite Immunol. 5:1-12.
34. Jacobson, R.H., N.D. Reed, and D.D. Manning. 1977. Expulsion of Nippostrongylus brasiliensis from mice lacking antibody production potential. Immunology. 32:867-874.
35. Corry, D.B., G. Grunig, H. Hadeiba, V.P. Kurup, M.L. Warnock, D. Sheppard, D.M. Rennick, and R.M. Locksley. 1998. Requirements for allergen-induced airway hyperreactivity in T and B cell-deficient mice. Mol. Med. 4:344-355.
36. Brightling, C.E., P. Bradding, F.A. Symon, S.T. Holgate, A.J. Wardlaw, and I.D. Pavord. 2002. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346:1699-1705.
37. David, J.R., M.A. Vadas, A.E. Butterworth, P.A. de Brito, E.M. Carvalho, R.A. David, J.C. Bina, and Z.A. Andrade. 1980. Enhanced helminthotoxic capacity of eosinophils from patients with eosinophilia. N. Engl. J. Med. 303:1147-1152.
38. Ramalho-Pinto, F.J., D.J. McLaren, and S.R. Smithers. 1978. Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. J. Exp. Med. 147:147-156.
39. Meeusen, E.N., and A. Balic. 2000. Do eosinophils have a role in the killing of helminth parasites? Parasitol. Today. 16:95-101.
40. Vallance, B.A., K.I. Matthaei, S. Sanovic, I.G. Young, and S.M. Collins. 2000. Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunol. 22:487-492.
41. Mitre, E., R.T. Taylor, J. Kubofcik, and T.B. Nutman. 2004. Parasite antigen-driven basophils are a major source of IL-4 in human filarial infections. J. Immunol. 172:2439-2445.
42. MacGlashan, D., Jr., J.M. White, S.K. Huang, S.J. Ono, J.T. Schroeder, and L.M. Lichtenstein. 1994. Secretion of IL-4 from human basophils. The relationship between IL-4 mRNA and protein in resting and stimulated basophils. J. Immunol. 152:3006-3016.
43. Schroeder, J.T., L.M. Lichtenstein, E.M. Roche, H. Xiao, and M.C. Liu. 2001. IL-4 production by human basophils found in the lung following segmental allergen challenge. J. Allergy Clin. Immunol. 107:265-271.
44. Kepley, C.L., P.J. McFeeley, J.M. Oliver, and M.F. Lipscomb. 2001. Immunohistochemical detection of human basophils in postmortem cases of fatal asthma. Am. J. Respir. Crit. Care Med. 164:1053-1058.
45. Koshino, T., S. Teshima, N. Fukushima, T. Takaishi, K. Hirai, Y. Miyamoto, Y. Arai, Y. Sano, K. Ito, and Y. Morita. 1993. Identification of basophils by immunohistochemistry in the airways of post-mortem cases of fatal asthma. Clin. Exp. Allergy. 23:919-925.
46. Khodoun, M.V., T. Orekhova, C. Potter, S. Morris, and F.D. Finkelman. 2004. Basophils initiate IL-4 production during a memory T-dependent response. J. Exp. Med. 200:857-870.
47. Mombaerts, P., A.R. Clarke, M.A. Rudnicki, J. Iacomini, S. Itohara, J.J. Lafaille, L. Wang, Y. Ichikawa, R. Jaenisch, M.L. Hooper, et al. 1992. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature. 360:225-231.
48. Kaplan, M.H., U. Schindler, S.T. Smiley, and M.J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity. 4:313-319.
49. Madsen, L., N. Labrecque, J. Engberg, A. Dierich, A. Svejgaard, C. Benoist, D. Mathis, and L. Fugger. 1999. Mice lacking all conventional MHC class II genes. Proc. Natl. Acad. Sci. USA. 96:10338-10343.
50. Murphy, K.M., A.B. Heimberger, and D.Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science. 250:1720-1723.
51. Weston, S.A., and C.R. Parish. 1990. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J. Immunol. Methods. 133:87-97.