Granulocyte macrophage colony-stimulating factor-driven respiratory mucosal sensitization induces Th2 differentiation and function independently of interleukin-4

American Journal of Respiratory Cell and Molecular Biology

Volumn 27, Issue 4, 2002, Pages 428-435

  Ritz, Stacey A ^a   Cundall, Meghan J ^a   Gajewska, Beata U ^a   Alvarez, David ^a   Gutierrez Ramos, José Carlos ^a   Coyle, Anthony J ^a   McKenzie, Andrew N J ^a   Stämpfli, Martin R ^a   Jordana, Manel ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0036789513     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.4824     Document Type: Article

References (58)

1. Beasley, R., J. Crane, C. K. Lai, and N. Pearce. 2000. Prevalence and etiology of asthma. J. Allergy Clin. Immunol. 105:S466-S472.
2. Garlisi, C. G., A. Falcone, T. T. Kung, D. Stelts, K. J. Pennline, A. J. Beabis, S. R. Smith, R. W. Egan, and S. P. Umland. 1995. T cells are necessary for Th2 cytokine production and eosinophil accumulation in airways of antigen-challenged allergic mice. Clin. Immunol. Immunopathol. 75:75-83.
3. Gonzalo, J. A., C. M. Lloyd, L. Kremer, E. Finger, A.-C. Martinez, M. H. Siegelman, M. Cybulsky, and J. C. Gutierrez-Ramos. 1996. Eosinophil recruitment to the lung in a murine model of allergic inflammation: the role of T cells, chemokines, and adhesion receptors. J. Clin. Invest. 98:2332-2345.
4. Finkelman, F. D., I. M. Katona, J. F. Urban, J. Holmes, J. Ohara, A. S. Tung, J. V. Sample, and W. E. Paul. 1988. IL-4 is required to generate and sustain in vivo IgE responses. J. Immunol. 141:2335-2341.
5. Hansel, T. T., R. K. Braun, I. J. De Vries, C. Boer, L. Boer, S. Rihs, and C. Walker. 1993. Eosinophils and cytokines. Agents Actions Suppl. 43:197-208.
6. Ohnishi, T., S. Sur, D. S. Collins, J. E. Fish, G. J. Gleich, and S. P. Peters. 1993. Eosinophil survival activity identified as interleukin-5 is associated with eosinophil recruitment and degranulation and lung injury twenty-four hours after segmental antigen lung challenge. J. Allergy Clin. Immunol. 92:607-615.
7. Corry, D. B., H. G. Folkesson, M. L. Warnock, D. J. Erle, M. A. Matthay, J. P. Wiener-Kronish, and R. M. Locksley. 1996. Interleukin 4, but not interleukin 5 or eosinophils, is required in a murine model of acute airway hyperreactivity. J. Exp. Med. 183:109-117.
8. Hogan, S. P., A. Koskinen, and P. S. Foster. 1997. Interleukin-5 and eosinophils induce airway damage and bronchial hyperreactivity during allergic airway inflammation in BALB/c mice. Immunol. Cell Biol. 75:284-288.
9. 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.
10. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma. Science 282:2258-2261.
11. Hogan, S. P., K. I. Matthei, J. M. Young, A. Kosikinen, I. G. Young, and P. S. Foster. 1998. A novel T cell-regulated mechanism modulating allergen-induced airways hyperreactivity in Balb/c mice independently of IL-4 and IL-5. J. Immunol. 161:1501-1509.
12. Kuperman, D., B. Schofield, M. Wills-Karp, and M. J. Grusby. 1998. Signal transducer and activator of transcription factor 6 (Stat6)-deficient mice are protected from antigen-induced airway hyperrepsonsiveness and mucus production. J. Exp. Med. 187:939-948.
13. Hogan, S. P., A. Mould, H. Kikutani, A. J. Ramsay, and P. S. Foster. 1997. Aeroallergen-induced eosinophilic inflammation, lung damage, and airways hyperreactivity in mice can occur independently of IL-4 and allergen-specific immunoglobulins. J. Clin. Invest. 99:1329-1339.
14. Kips, J. C., G. G. Brusselle, G. F. Joos, R. A. Peleman, R R. Devos, J. H. Tavernier, and R. A. Pauwels, 1995. Importance of interleukin-4 and interleukin-12 in allergen-induced airway changes in mice. Int. Arch. Allergy Immunol. 107:115-118.
15. Brusselle, C. G., J. C. Kips, J. H. Tavernier, G. H. van der Heyden, C. A. Cuvelier, R. A. Pauwels, and H. Bluethmann. 1994. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin. Exp. Allergy 24:73-80.
16. Coyle, A. J., G. Le Gros, C. Bertrand, S. Tsuyuki, C. H. Heusser, M. Kopf, and G. P. Anderson. 1995. Interleukin-4 is required for the induction of lung Th2 mucosal immunity. Am. J. Respir. Cell Mol. Biol. 13:54-59.
17. Herrick, C. A., H. MacLeod, E. Glusac, R. E. Tigellar, and K. Bottomly. 2000. Th2 responses induced by epicutaneous or inhalational protein exposure are differentially dependent on IL-4. J. Clin. Invest. 105:765-775.
18. Akimoto, T., F. Numata, M. Tamura, Y. Takata, N. Higashida, T. Takashi, K. Takeda, and S. Akira. 1998. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187:1537-1542.
19. Kopf, M., G. G. Le Gros, M. Bachmann, M. C. Lamers, H. Bluethmann, and G. Koehler. 1993. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362:245-248.
20. Noben-Trauth, N., L. D. Shultz, F. Brombacher, J. F. Urban, 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.
21. Hogarth, P. J., M. J. Taylor, and A. E. Bianco. 1998. IL-5-dependent immunity to microfilariae is independent of IL-4 in a mouse model of onchocerciasis. J. Immunol. 160:5436-5440.
22. Kopf, M., F. Brombacher, G. Kohler, G. Kienzle, K. H. Widmann, K. Lefrang, C. Humborg, B. Ledermann, and W. Solbach. 1996. IL-4-deficient Balb/c mice resist infection with Leishmania major. J. Exp. Med. 184:1127-1136.
23. Brewer, J. M., M. Conacher, C. A. Hunter, M. Mohrs, F. Brombacher, and J. Alexander. 1999. Aluminum hydroxide adjuvant initiates strong antigen-specific Th2 responses in the absence of IL-4- or IL-13-mediated signaling. J. Immunol. 163:6448-6454.
24. Chensue, S. W., K. Warmington, J. H. Ruth, N. Lukacs, and S. L. Kunkel. 1997. Mycobacterial and schistosomal antigen-elicited granuloma formation in IFN-γ and IL-4 knockout mice. J. Immunol. 159:3565-3573.
25. Noben-Trauth, N., P. Kropf, and I. Muller. 1996. Susceptibility to Leishmania major infection in interleukin-4-deficient mice. Science 271:987-990.
26. 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.
27. Kropf, P., L. R. Schopf, C. L. Chung, D. Xu, F. Y. Liew, J. P. Sypek, and I. Muller. 1999. Expression of Th2 cytokines and the stable Th2 marker ST2L in the absence of IL-4 during Leishmania major infection. Eur. J. Immunol. 29:3621-3628.
28. Holt, P. G., and C. McMenamin. 1989. Defence against allergic sensitization in the healthy lung: the role of inhalation tolerance. Clin. Exp. Allergy 19:255-262.
29. Swirski, F. K., B. U. Gajewska, D. Alvarez, S. A. Ritz, M. J. Cundall, E. C. Cates, A. J. Coyle, J. C. Gutierrez-Ramos, M. D. Inman, M. Jordana, and M. R. Stämpfli. 2002. Inhalation of a harmless antigen (ovalbumin) elicits immune activation but divergent immunoglobulin and cytokine activities in mice. Clin. Exp. Allergy 32:411-421.
30. Stämpfli, M. R., R. E. Wiley, G. S. Neigh, B. U. Gajewska, X. F. Lei, D. P. Snider, Z. Xing, and M. Jordana. 1998. GM-CSF transgene expression in the airway allows aerosolized ovalbumin to induce allergic sensitization in mice. J. Clin. Invest. 102:1704-1714.
31. 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.
32. Glimcher, L. H., and K. M. Murphy. 2000. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 14:1693-1711.
33. Zhang, D. H., L. Cohn, P. Ray, K. Bottomly, and A. Ray. 1997. Transcription factor GATA-3 is differentially expressed in murine Th1 and Th2 cells and controls Th2-specific expression of the interleukin-5 gene. J. Biol. Chem. 272:21597-21603.
34. Szabo, S. J., S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, and L. H. Glimcher. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100:655-669.
35. Bonecchi, R., G. Bianchi, P. P. Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P. A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187:129-134.
36. Lohning, M., A. Stroehmann, A. J. Coyle, J. L. Grogan, S. Lin, J. C. Gutierrez-Ramos, D. Levinson, A. Radbruch, and T. Kamradt. 1998. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc. Natl. Acad. Sci. USA 95:6930-6935.
37. Meisel, C., K. Bonhagen, M. Lohning, A. J. Coyle, J. C. Gutierrez-Ramos, A. Radbruch, and T. Kamradt. 2001. Regulation and function of T1/ST2 expression on CD4+ T cells: induction of type 2 cytokine production by T1/ST2 cross-linking. J. Immunol. 166:3143-3150.
38. Townsend, M. J., P. G. Fallon, D. J. Matthews, H. E. Jolin, and A. N. McKenzie. 2000. T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J. Exp. Med. 191:1069-1076.
39. Zheng, W., and R. A. Flavell. 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89:587-596.
40. Stampfli, M. R., S. A. Ritz, G. S. Neigh, P. J. Sime, X. F. Lei, Z. Xing, K. Croitoru, and M. Jordana. 1998. Adenoviral infection inhibits allergic airways inflammation in mice. Clin. Exp. Allergy 28:1581-1590.
41. Matsukura, S., C. Stellato, S. N. Georas, V. Casolaro, J. R. Plitt, K. Miura, S. Kurosawa, U. Schindler, and R. P. Schleimer. 2001. Interleukin-13 upregulates eotaxin expression in airway epithelial cells by a STAT6-dependent mechanism. Am. J. Respir. Cell Mol. Biol. 24:755-761.
42. Pope, S. M., E. B. Brandt, A. Mishra, S. P. Hogan, N. Zimmerman, K. I. Matthaei, P. S. Foster, and M. E. Rothenberg. 2001. IL-13 induces eosinophil recruitment into the lung by an IL-5- and eotaxin-dependent mechanism. J. Allergy Clin. Immunol. 108:594-601.
43. Li, L., Y. Xia, A. Nguyen, Y. H. Lai, L. Feng, T. R. Mosmann, and D. Lo. 1999. Effects of Th2 cytokines on chemokine expression in the lung: IL-13 potently induces eotaxin expression by airway epithelial cells. J. Immunol. 162:2477-2487.
44. Nonaka, M., R. Nonaka, M. Jordana, and J. Dolovich. 1996. GM-CSF, IL-8, IL-IR, TNF-α R, and HLA-DR in nasal epithelial cells in allergic rhinitis. Am. J. Respir. Crit Care Med. 153:1675-1681.
45. Ohno, I., R. Lea, S. Finotto, J. Marshall, J. Denburg, J. Dolovich, J. Gauldie, and M. Jordana. 1991. Granulocyte/macrophage colony-stimulating factor (GM-CSF) gene expression in eosinophils in nasal polyposis. Am. J. Respir. Cell Mol. Biol. 5:505-510.
46. Sousa, A. R., R. N. Poston, S. J. Lane, J. A. Nakhosteen, and T. H. Lee. 1993. Detection of GM-CSF in asthmatic bronchial epithelium and decrease by inhaled corticosteroids. Am. Rev. Respir. Dis. 147:1557-1561.
47. Marini, M., E. Vittori, J. Hollemborg, and S. Mattoli. 1992. Expression of the potent inflammatory cytokines, granulocyte-macrophage-colony-stimulating factor and interleukin-6 and interleukin-8, in bronchial epithelial cells of patients with asthma. J. Allergy Clin. Immunol. 89:1001-1009.
48. Rohrbach, M., U. Frey, R. Kraemer, and S. Liechti-Gallati. 1999. A variant in the gene for GM-CSF, I117T, is associated with atopic asthma in a population of asthmatic children. J. Allergy Clin. Immunol. 104:247-248.
49. Devalia, J. L., H. Bayram, M. M. Abdelaziz, R. J. Sapsford, and R. J. Davies. 1999. Differences between cytokine release from bronchial epithelial cells of asthmatic patients and non-asthmatic subjects: effect of exposure to diesel exhaust particles. Int. Arch. Allergy Immunol. 118:437-439.
50. Gauvreau, G. M., P. M. O'Byrne, R. Moqbel, J. Velazquez, R. M. Watson, K. J. Howie, and J. A. Denburg. 1998. Enhanced expression of GM-CSF in differentiating eosinophils of atopic and atopic asthmatic subjects. Am. J. Respir. Cell Mol. Biol. 19:55-62.
51. Nakamura, Y., T. Ozaki, T. Kamei, K. Kawaji, K. Banno, S. Miki, K. Fujisawa, S. Yasuoka, and T. Ogura. 1993. Increased granulocyte/macrophage colony-stimulating factor production by mononuclear cells from peripheral blood of patients with bronchial asthma. Am. Rev. Respir. Dis. 147:87-91.
52. Christensen, P. J., L. R. Armstrong, J. J. Fak, G. H. Chen, R. A. McDonald, G. B. Toews, and R. Paine III. 1995. Regulation of rat pulmonary dendritic cell immunostimulatory activity by alveolar epithelial cell-derived granulocyte macrophage colony-stimulating factor. Am. J. Respir. Cell Mol. Biol. 13:426-433.
53. Suda, T., K. McCarthy, Q. Vu, J. McCormack, and E. E. Schneeberger. 1998. Dendritic cell precursors are enriched in the vascular compartment of the lung. Am. J. Respir. Cell Mol. Biol. 19:728-737.
54. Wang, J., D. P. Snider, B. R. Hewlett, N. W. Lukacs, J. Gauldie, H. Liang, and Z. Xing. 2000. Transgenic expression of granulocyte macrophage colony-stimulating factor induces the differentiation and activation of a novel dendritic cell population in the lung. Blood 95:2337-2345.
55. Bilyk, N., and P. G. Holt. 1993. Inhibition of the immunosuppressive activity of resident pulmonary alveolar macrophages by granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 177:1773-1777.
56. Bilyk, N., and P. G. Holt. 1995. Cytokine modulation of the immunosuppressive phenotype of pulmonary macrophage populations. Immunology 86:231-237.
57. Pulendran, B., J. L. Smith, G. Caspary, K. Brasel, D. Pettit, E. Maraskovsky, and C. R. Maliszewski. 1999. Distinct dendritic cell subset differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 96:1036-1041.
58. Maldonado-Lopez, R., C. Maliszewski, J. Urbain, and M. Moser. 2001. Cytokines regulate the capacity of CD8α+ and CD8α- dendritic cells to prime Th1/Th2 cells in vivo. J. Immunol. 167:4345-4350.