Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production

Journal of Immunology

Volumn 174, Issue 2, 2005, Pages 1063-1072

  Gessner, André ^a   Mohrs, Katja ^b   Mohrs, Markus ^b  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b TRUDEAU INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 4; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BASOPHIL; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHIL; GENE EXPRESSION; MAST CELL; MOUSE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL;

EID: 11844280961     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.2.1063     Document Type: Article

References (64)

1. Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W. C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15:505.
2. Kawakami, T., and S. J. Galli. 2002. Regulation of mast-cell and basophil function and survival by IgE. Nat. Rev. Immunol. 2:773.
3. Dombrowicz, D., and M. Capron. 2001. Eosinophils, allergy and parasites. Curr. Opin. Immunol. 13:716.
4. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17:255.
5. Galli, S. J., M. Maurer, and C. S. Lantz. 1999. Mast cells as sentinels of innate immunity. Curr. Opin. Immunol. 11:53.
6. de Andres, B., E. Rakasz, M. Hagen, M. L. McCormik, A. L. Mueller, D. Elliot, A. Metwali, M. Sandor, B. E. Britigan, J. V. Weinstock, et al. 1997. Lack of Fc-ε receptors on marine eosinophils: implications for the functional significance of elevated IgE and eosinophils in parasitic infections. Blood 89:3826.
7. Walsh, G. M. 2001. Eosinophil granule proteins and their role in disease. Curr. Opin. Hematol. 8:28.
8. 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.
9. Brown, M. A., and J. Hural. 1997. Functions of IL-4 and control of its expression. Crit. Rev. Immunol. 17:1.
10. Abbas, A. K., K. M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature 383:787.
11. 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.
12. 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.
13. Mohrs, M., B. Ledermann, G. Köhler, A. Dorfmüller, A. Gessner, and F. Brombacher. 1999. Differences between IL-4- and IL-4 receptor α-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 162:7302.
14. + T cell IL-4 production is revealed in IL-4 receptor-deficient mice. Proc. Natl. Acad. Sci. USA 94:10838.
15. Rumbley, C. A., H. Sugaya, S. A. Zekavat, M. El Refaei, P. J. Perrin, and S. M. Phillips. 1999. Activated eosinophils are the major source of Th2-associated cytokines in the schistosome granuloma. J. Immunol. 162:1003.
16. Sherman, M. A., V. H. Secor, S. K. Lee, R. D. Lopez, and M. A. Brown. 1999. STAT6-independent production of IL-4 by mast cells. Eur. J. Immunol. 29:1235.
17. 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.
18. Belkaid, Y., K. F. Hoffmann, S. Mendez, S. Kamhawi, M. C. Udey, T. A. Wynn, and D. L. Sacks. 2001. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J. Exp. Med. 194:1497.
19. Laky, K., L. Lefrancois, and L. Puddington. 1997. Age-dependent intestinal lymphoproliferative disorder due to stem cell factor receptor deficiency: parameters in small and large intestine. J. Immunol. 158:1417.
20. Coleman, J. W., M. R. Holliday, I. Kimber, K. M. Zsebo, and S. J. Galli. 1993. Regulation of mouse peritoneal mast cell secretory function by stem cell factor, IL-3 or IL-4. J. Immunol. 150:556.
21. Rodewald, H. R., M. Dessing, A. M. Dvorak, and S. J. Galli. 1996. Identification of a committed precursor for the mast cell lineage. Science 271:818.
22. Yamaguchi, M., C. S. Lantz, H. C. Oettgen, I. M. Katona, T. Fleming, I. Miyajima, J. P. Kinet, and S. J. Galli. 1997. IgE enhances mouse mast cell FcεRI expression in vitro and in vivo: evidence for a novel amplification mechanism in IgE-dependent reactions. J. Exp. Med. 185:663.
23. Openshaw, P., E. E. Murphy, N. A. Hosken, V. Maino, K. Davis, K. Murphy, and A. O'Garra. 1995. Heterogeneity of intracellular cytokine synthesis at the single-cell level in polarized T helper 1 and T helper 2 populations. J. Exp. Med. 182:1357.
24. Shinkai, K., M. Mohrs, and R. M. Locksley. 2002. Helper T cells regulate type-2 innate immunity in vivo. Nature 420:825.
25. Overbergh, L., D. Valckx, M. Waer, and C. Mathieu. 1999. Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine 11:305.
26. Johnson, L. L., K. N. Berggren, F. M. Szaba, W. Chen, and S. T. Smiley. 2003. Fibrin-mediated protection against infection-stimulated immunopathology. J. Exp. Med. 197:801.
27. Brown, M. A., J. H. Pierce, C. J. Watson, J. Falco, J. N. Ihle, and W. E. Paul. 1987. B cell stimulatory factor-1/interleukin-4 mRNA is expressed by normal and transformed mast cells. Cell 50:809.
28. Dvorak, A. M., R. A. Seder, W. E. Paul, E. S. Morgan, and S. J. Galli. 1994. Effects of interleukin-3 with or without the c-Kit ligand, stem cell factor, on the survival and cytoplasmic granule formation of mouse basophils and mast cells in vitro. Am. J. Pathol 144:160.
29. Igarashi, H., S. C. Gregory, T. Yokota, N. Sakaguchi, and P. W. Kincade. 2002. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17:117.
30. Gurish, M. F., and K. F. Austen. 2001. The diverse roles of mast cells. J. Exp. Med. 194:F1
31. Reynolds, D. S., R. L. Stevens, W. S. Lane, M. H. Carr, K. F. Austen, and W. E. Serafin. 1990. Different mouse mast cell populations express various combinations of at least six distinct mast cell serine proteases. Proc. Natl. Acad. Sci. USA 87:3230.
32. Galli, S. J. 1990. New insights into "the riddle of the mast cells:" microenvironmental regulation of mast cell development and phenotypic heterogeneity. Lab. Invest. 62:5.
33. Galli, S. J., and C. S. Lantz. 1999. Allergy. In Fundamental Immunology. W. E. Paul, ed. Lippincott-Raven Press, Philadelphia, p. 1127.
34. Grimaldi, J. C., N. X. Yu, G. Grunig, B. W. Seymour, F. Cottrez, D. S. Robinson, N. Hosken, W. G. Ferlin, X. Wu, H. Soto, et al. 1999. Depletion of eosinophils in mice through the use of antibodies specific for C-C chemokine receptor 3 (CCR3). J. Leukocyte Biol. 65:846.
35. 7 integrin) for tissue-specific homing. J. Exp. Med. 194:1243.
36. Kawakami, Y., J. Kitaura, A. B. Satterthwaite, R. M. Kato, K. Asai, S. E. Hartman, M. Maeda-Yamamoto, C. A. Lowell, D. J. Rawlings, O. N. Witte, et al. 2000. Redundant and opposing functions of two tyrosine kinases, Btk and Lyn, in mast cell activation. J. Immunol. 165:1210.
37. Weiss, D. L., J. Hural, D. Tara, L. A. Timmerman, G. Henkel, and M. A. Brown. 1996. Nuclear factor of activated T cells is associated with a mast cell interleukin 4 transcription complex. Mol. Cell. Biol. 16:228.
38. Solymar, D. C., S. Agarwal, C. H. Bassing, F. W. Alt, and A. Rao. 2002. A 3′ enhancer in the IL-4 gene regulates cytokine production by Th2 cells and mast cells. Immunity 17:41.
39. Jain, J., C. Loh, and A. Rao. 1995. Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol. 7:333.
40. Swanson, B. J., M. Murakami, T. C. Mitchell, J. Kappler, and P. Marrack. 2002. RANTES production by memory phenotype T cells is controlled by a posttranscriptional, TCR-dependent process. Immunity 17:605.
41. Bochner, B. S., and R. P. Schleimer. 2001. Mast cells, basophils, and eosinophils: distinct but overlapping pathways for recruitment. Immunol. Rev. 179:5.
42. Chen, L., K. A. Grabowski, J. P. Xin, J. Coleman, Z. Huang, B. Espiritu, S. Alkan, H. B. Xie, Y. Zhu, F. A. White, et al. 2004. IL-4 induces differentiation and expansion of Th2 cytokine-producing eosinophils. J. Immunol. 172:2059.
43. Seder, R. A., W. E. Paul, A. M. Dvorak, S. J. Sharkis, A. Kagey-Sobotka, Y. Niv, F. D. Finkelman, S. A. Barbieri, S. J. Galli, and M. Plaut. 1991. Mouse splenic and bone marrow cell populations that express high-affinity Fcε receptors and produce interleukin 4 are highly enriched in basophils. Proc. Natl. Acad. Sci. USA 88:2835.
44. Conrad, D. H., S. Z. Ben-Sasson, G. Le Gros, F. D. Finkelman, and W. E. Paul. 1990. Infection with Nippostrongylus brasiliensis or injection of anti-IgD antibodies markedly enhances Fc-receptor-mediated interleukin 4 production by non-B, non-T cells. J. Exp. Med. 171:1497.
45. Haisch, K., G. Schramm, F. H. Falcone, C. Alexander, M. Schlaak, and H. Haas. 2001. A glycoprotein from Schistosoma mansoni eggs binds non-antigen-specific immunoglobulin E and releases interleukin-4 from human basophils. Parasite Immunol. 23:427.
46. 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, et al. 2004. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J. Exp. Med. 200:507.
47. H3 region of IgE. J. Immunol. 161:5647.
48. Ochensberger, B., S. Rihs, T. Brunner, and C. A. Dahinden. 1995. IgE-independent interleukin-4 expression and induction of a late phase of leukotriene C4 formation in human blood basophils. Blood 86:4039.
49. Yoshimoto, T., H. Tsutsui, K. Tominaga, K. Hoshino, H. Okamura, S. Akira, W. E. Paul, and K. Nakanishi. 1999. IL-18, although antiallergic when administered with IL-12, stimulates IL-4 and histamine release by basophils. Proc. Natl. Acad. Sci. USA 96:13962.
50. 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.
51. Siden, E. J. 1993. Regulated expression of germline antigen receptor genes in mast cell lines from the murine embryo. J. Immunol. 150:4427.
52. Weiss, D. L., and M. A. Brown. 2001. Regulation of IL-4 production in mast cells: a paradigm for cell-type-specific gene expression. Immunol. Rev. 179:35.
53. Plaut, M., J. H. Pierce, C. J. Watson, J. Hanley-Hyde, R. P. Nordan, and W. E. Paul. 1989. Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature 339:64.
54. Stetson, D. B., M. Mohrs, R. L. Reinhardt, J. L. Baron, Z. E. Wang, L. Gapin, M. Kronenberg, and R. M. Locksley. 2003. Constitutive cytokine mRNAs mark natural killer (NK) and NKT cells poised for rapid effector function. J. Exp. Med. 198:1069.
55. Gibbs, B. P., H. Haas, F. H. Falcone, C. Albrecht, I. B. Vollrath, T. Noll, H. H. Wolff, and U. Amon. 1996. Purified human peripheral blood basophils release interleukin-13 and preformed interleukin-4 following immunological activation. Eur. J. Immunol. 26:2493.
56. 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.
57. 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.
58. Cyr, M. M., and J. A. Denburg. 2001. Systemic aspects of allergic disease: the role of the bone marrow. Curr. Opin. Immunol. 13:727.
59. 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.
60. Ruitenberg, E. J., and A. Elgersma. 1976. Absence of intestinal mast cell response in congenitally athymic mice during Trichinella spiralis infection. Nature 264:258.
61. Hu-Li, J., C. Pannetier, L. Guo, M. Lohning, H. Gu, C. Watson, M. Assenmacher, A. Radbruch, and W. E. Paul. 2001. Regulation of expression of IL-4 alleles: analysis using a chimeric GFP/IL-4 gene. Immunity 14:1.
62. + T cells. Science 281:1352.
63. Rivière, I., M. J. Sunshine, and D. R. Littman. 1998. Regulation of IL-4 expression by activation of individual alleles. Immunity 9:217.
64. Matsuda, J. L., L. Gapin, J. L. Baron, S. Sidobre, D. B. Stetson, M. Mohrs, R. M. Locksley, and M. Kronenberg. 2003. Mouse Vα14i natural killer T cells are resistant to cytokine polarization in vivo. Proc. Natl. Acad. Sci. USA 100:8395.