Interleukin-9 induces mucous cell metaplasia independent of inflammation

American Journal of Respiratory Cell and Molecular Biology

Volumn 28, Issue 6, 2003, Pages 664-672

  Reader, J Rachel ^a   Hyde, Dallas M ^b   Schelegle, Edward S ^b   Aldrich, Melinda C ^b   Stoddard, Amy M ^b   McLane, Michael P ^b   Levitt, Roy C ^b   Tepper, Jeffrey S ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALCIAN BLUE; INTERLEUKIN 13; INTERLEUKIN 9; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHUS HYPERREACTIVITY; BRONCHUS MUCUS; CONTROLLED STUDY; EVALUATION; IMMUNOGLOBULIN BLOOD LEVEL; INFLAMMATION; INFLAMMATORY CELL; LUNG INFECTION; LUNG LAVAGE; MALE; MEDICAL ASSESSMENT; METAPLASIA; MOUSE; MUCOUS CELL; NONHUMAN; PERIODIC ACID SCHIFF STAIN; PHENOTYPE; PROTEIN EXPRESSION; SINGLE DRUG DOSE; UPREGULATION;

ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; CELL DIFFERENTIATION; CELL DIVISION; IMMUNOGLOBULIN E; INTERLEUKIN-13; INTERLEUKIN-9; MALE; METAPLASIA; MICE; MICE, INBRED C57BL; MUCINS; PNEUMONIA; PROTEINS; RESPIRATORY MUCOSA; UP-REGULATION;

ANIMALIA; BRONCHUS;

EID: 0038652023     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2002-0207OC     Document Type: Article

References (35)

1. Doull, I. J., S. Lawrence, M. Watson, T. Begishvili, R. W. Beasley, F. Lampe, T. Holgate, and N. E. Morton. 1996. Allelic association of gene markers on chromosomes 5q and 11q with atopy and bronchial hyperresponsiveness. Am. J. Respir. Crit. Care Med. 153:1280-1284.
2. Nicolaides, N. C., K. J. Holroyd, S. L. Ewart, S. M. Eleff, M. B. Kiser, C. R. Dragwa, C. D. Sullivan, L. Grasso, L. Y. Zhang, C. J. Messler, T. Zhou, S. R. Kleeberger, K. H. Buetow, and R. C. Levitt. 1997. Interleukin 9: a candidate gene for asthma. Proc. Natl. Acad. Sci. USA 94:13175-13180.
3. Levitt, R. C., M. P. McLane, D. MacDonald, V. Ferrante, C. Weiss, T. Zhou, K. J. Holroyd, and N. C. Nicolaides. 1999. IL-9 pathway in asthma: new therapeutic targets for allergic inflammatory disorders. J. Allergy Clin. Immunol. 103:S485-S491.
4. McLane, M. P., A. Haczku, M. van de Rijn, C. Weiss, V. Ferrante, D. MacDonald, J. C. Renauld, N. C. Nicolaides, K. J. Holroyd, and R. C. Levitt. 1998. Interleukin-9 promotes allergen-induced eosinophilic inflammation and airway hyperresponsiveness in transgenic mice. Am. J. Respir. Cell Mol. Biol. 19:713-720.
5. Temann, U. A., P. Ray, and R. A. Flavell. 2002. Pulmonary overexpression of IL-9 induces Th2 cytokine expression, leading to immune pathology. J. Clin. Invest. 109:29-39.
6. Dong, Q., J. Louahed, A. Vink, C. D. Sullivan, C. J. Messler, Y. Zhou, A. Haczku, F. Huaux, M. Arras, K. J. Holroyd, J. C. Renauld, R. C. Levitt, and N. C. Nicolaides. 1999. IL-9 induces chemokine expression in lung epithelial cells and baseline airway eosinophilia in transgenic mice. Eur. J. Immunol. 29:2130-2139.
7. Temann, U. A., G. P. Geba, J. A. Rankin, and R. A. Flavell. 1998. Expression of interleukin 9 in the lungs of transgenic mice causes airway inflammation, mast cell hyperplasia, and bronchial hyperresponsiveness. J. Exp. Med. 188:1307-1320.
8. Louahed, J., M. Toda, J. Jen, Q. Hamid, J. C. Renauld, R. C. Levitt, and N. C. Nicolaides. 2000. Interleukin-9 upregulates mucus expression in the airways. Am. J. Respir. Cell Mol. Biol. 22:649-656.
9. Townsend, M. J., P. G. Fallon, D. J. Matthews, P. Smith, H. E. Jolin, and A. N. McKenzie. 2000. IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 13:573-583.
10. Shimbara, A., P. Christodoulopoulos, A. Soussi-Gunni, R. Olivenstein, Y. Nakamura, R. C. Levitt, N. C. Nicolaides, K. J. Holroyd, A. Tsicopoulos, J. J. Lafitte, B. Wallaert, and Q. A. Hamid. 1999. IL-9 and its receptor in allergic and nonallergic lung disease: increased expression in asthma. J. Allergy Clin. Immunol. 104:108-115.
11. Longphre, M., D. Li, M. Gallup, E. Drori, C. L. Ordonez, T. Redman, S. Wenzel, D. E. Bice, J. V. Fahy, and C. Basbaum. 1999. Allergen-induced IL-9 directly stimulates mucin transcription in respiratory epithelial cells. J. Clin. Invest. 104:1375-1382.
12. Toda, M., M. K. Tulic, R. C. Levitt, and Q. Hamid. 2002. A calcium-activated chloride channel (HCLCA1) is strongly related to IL-9 expression and mucus production in bronchial epithelium of patients with asthma. J. Allergy Clin. Immunol. 109:246-250.
13. Zhou, Y., M. Mclane, and R. C. Levitt. 2001. Th2 cytokines and asthma: interleukin-9 as a therapeutic target for asthma. Respir. Res. 2:80-84.
14. Grunig, G., M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, 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.
15. 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.
16. Zhu, Z., R. J. Homer, Z. Wang, Q. Chen, G. P. Geba, J. Wang, Y. Zhang, and J. A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103:779-788.
17. Zuhdi, A. M., F. M. Piazza, D. M. Selby, N. Letwin, L. Huang, and M. C. Rose. 2000. Muc-5/5ac mucin messenger RNA and protein expression is a marker of goblet cell metaplasia in murine airways. Am. J. Respir. Cell Mol. Biol. 22:253-260.
18. Louahed, J., A. Kermouni, J. Van Snick, and J. C. Renauld. 1995. IL-9 induces expression of granzymes and high-affinity IgE receptor in murine T helper clones. J. Immunol. 154:5061-5070.
19. Gessner, A., H. Blum, and M. Rollinghoff. 1993. Differential regulation of IL-9-expression after infection with Leishmania major in susceptible and resistant mice. Immunobiology 189:419-435.
20. Petit-Frere, C., B. Dugas, P. Braquet, and J. M. Mencia-Huerta. 1993. Interleukin-9 potentiates the interleukin-4-induced IgE and IgG1 release from murine B lymphocytes. Immunology 79:146-151.
21. Louahed, J., Y. Zhou, W. L. Maloy, P. U. Rani, C. Weiss, Y. Tomer, A. Vink, J. Renauld, J. Van Snick, N. C. Nicolaides, R. C. Levitt, and A. Haczku. 2001. Interleukin 9 promotes influx and local maturation of eosinophils. Blood 97:1035-1042.
22. Zhou, Y., Q. Dong, J. Louahed, C. Dragwa, D. Savio, M. Huang, C. Weiss, Y. Tomer, M. P. McLane, N. C. Nicolaides. and R. C. Levitt. 2001. Characterization of a calcium-activated chloride channel as a shared target of th2 cytokine pathways and its potential involvement in asthma. Am. J. Respir. Cell Mol. Biol. 25:486-491.
23. Little, F. F., W. W. Cruikshank, and D. M. Center. 2001. IL-9 stimulates release of chemotactic factors from human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 25:347-352.
24. McMillan, S. J., B. Bishop, M. J. Townsend, A. N. McKenzie, and C. M. Lloyd. 2002. The absence of interleukin 9 does not affect the development of allergen-induced pulmonary inflammation nor airway hyperreactivity. J. Exp. Med. 195:51-57.
25. Blyth, D. I., M. S. Pedrick, T. J. Savage, E. M. Hessel, and D. Fattah. 1996. Lung inflammation and epithelial changes in a murine model of atopic asthma. Am. J. Respir. Cell Mol. Biol. 14:425-438.
26. Haile, S., J. Lefort, D. Joseph, P. Gounon, M. Huerre, and B. B. Vargaftig. 1999. Mucous-cell metaplasia and inflammatory-cell recruitment are dissociated in allergic mice after antibody-and drug-dependent cell depletion in a murine model of asthma. Am. J. Respir. Cell Mol. Biol. 20:891-902.
27. Voynow, J. A., L. R. Young, Y. Wang, T. Horger, M. C. Rose, and B. M. Fischer. 1999. Neutrophil elastase increases muc5ac mRNA and protein expression in respiratory epithelial cells. Am. J. Physiol. 276:L835-L843.
28. Shim, J. J., K. Dabbagh, I. F. Ueki, T. Dao-Pick, P. R. Burgel, K. Takeyama, D. C. Tam, and J. A. Nadel. 2001. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils. Am. J. Physiol. 280:L134-L140.
29. Shimizu, T., Y. Takahashi, S. Kawaguchi, and Y. Sakakura. 1996. Hypertrophic and metaplastic changes of goblet cells in rat nasal epithelium induced by endotoxin. Am. J. Respir. Crit. Care Med. 153:1412-1418.
30. Lee, H., K. Takeyama, K. Dabbagh, J. A. Lausier, I. F. Ueki, and J. A. Nadel. 2000. Agrose plug installation causes goblet cell metaplasia by activating EGF receptors in rat airways. Am. J. Physiol. 278:L185-L192.
31. Ordonez, C. L., R. Khashayar, H. H. Wong, R. Ferrando, R. Wu, D. M. Hyde, J. A. Hotchkiss, Y. Zhang, A. Novikov, G. Dolganov, and J. V. Fahy. 2001. Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am. J. Respir. Crit. Care Med. 163:517-523.
32. 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.
33. 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.
34. Prieto, J., C. Lensmar, A. Roquet, I. van der Ploeg, D. Gigliotti, A. Eklund, and J. Grunewald. 2000. Increased interleukin-13 mRNA expression in bronchoalveolar lavage cells of atopic patients with mild asthma after repeated low-dose allergen provocations. Respir. Med. 94:806-814.
35. Kung, T. T., B. Luo, Y. Crawley, C. G. Garlisi, K. Devito, M. Minnicozzi, R. W. Egan, W. Kreutner, and R. W. Chapman. 2001. Effect of anti-mIL-9 antibody on the development of pulmonary inflammation and airway hyperresponsiveness in allergic mice. Am. J. Respir. Cell Mol. Biol. 25:600-605.