Acidic mammalian chitinase regulates epithelial cell apoptosis via a chitinolytic-independent mechanism

Journal of Immunology

Volumn 182, Issue 8, 2009, Pages 5098-5106

  Hartl, Dominik ^a   He, Chuan Hua ^a   Koller, Babara ^a   Da Silva, Carla A ^a   Kobayashi, Yasushi ^a   Lee, Chun Geun ^a   Flavell, Richard A ^a   Elias, Jack A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC MAMMALIAN CHITINASE; ALLOSAMIDIN; CHITINASE; FAS LIGAND; GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; CHIA PROTEIN, HUMAN; CHITIN; INTERLEUKIN 13;

APOPTOSIS; ARTICLE; CELL PROTECTION; DRUG MECHANISM; ENZYME INHIBITION; EPITHELIUM CELL; LUNG ALVEOLUS CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG; METABOLISM; MOUSE; PROTEIN BINDING; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CHITIN; CHITINASE; ENZYME ACTIVATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTERLEUKIN-13; LUNG; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 65249168882     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803446     Document Type: Article

References (49)

1. Busse, W. W., and R. F. Lemanske, Jr. 2001. Asthma. N. Engl. J. Med. 344: 350-362.
2. Bochner, B. S., and W. W. Busse. 2005. Allergy and asthma. J. Allergy Clin. Immunol. 115: 953-959.
3. Cohn, L., J. A. Elias, and G. L. Chupp. 2004. Asthma: mechanisms of disease persistence and progression. Annu. Rev. Immunol. 22: 789-815. (Pubitemid 38680442)
4. Elias, J. A., Z. Zhu, G. Chupp, and R. J. Homer. 1999. Airway remodeling in asthma. J. Clin. Invest. 104: 1001-1006.
5. Elias, J. A., C. G. Lee, T. Zheng, B. Ma, R. J. Homer, and Z. Zhu. 2003. New insights into the pathogenesis of asthma. J. Clin. Invest. 111: 291-297.
6. Holgate, S. T. 1988. Inflammatory cells and their mediators in the pathogenesis of asthma. Postgrad. Med. J. 64 Suppl. 4: 82-95.
7. Holgate, S. T. 1997. Asthma: a dynamic disease of inflammation and repair. Ciba Found. Symp. 206: 5-28.
8. Holgate, S. T. 2002. Airway inflammation and remodeling in asthma: current concepts. Mol. Biotechnol. 22: 179-189. (Pubitemid 35193342)
9. Holgate, S. T. 2008. Pathogenesis of asthma. Clin. Exp. Allergy 38: 872-897.
10. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17: 255-281. (Pubitemid 29241125)
11. Wills-Karp, M. 2004. Interleukin-13 in asthma pathogenesis. Curr. Allergy Asthma Rep. 4: 123-131.
12. Hamid, Q., M. Azzawi, S. Ying, R. Moqbel, A. J. Wardlaw, C. J. Corrigan, B. Bradley, S. R. Durham, J. V. Collins, P. K. Jeffery, et al. 1991. Expression of mRNA for interleukin-5 in mucosal bronchial biopsies from asthma. J. Clin. Invest 87: 1541-1546.
13. Hamid, Q. A., and L. A. Cameron. 2000. Recruitment of T cells to the lung in response to antigen challenge. J. Allergy Clin. Immunol. 106: S227-S234.
14. Leung, D. Y., R. J. Martin, S. J. Szefler, E. R. Sher, S. Ying, A. B. Kay, and Q. Hamid. 1995. Dysregulation of interleukin 4, interleukin 5, and interferon γ gene expression in steroid-resistant asthma. J. Exp. Med. 181: 33-40.
15. + T cells, increased TH2-type cytokine mRNA expression, and eosinophil recruitment in bronchoalveolar lavage after allergen inhalation challenge in patients with atopic asthma. J. Allergy Clin. Immunol. 92: 313-324.
16. Robinson, D. S., Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A. M. Bentley, C. Corrigan, S. R. Durham, and A. B. Kay. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326: 298-304.
17. Robinson, D. S., S. Ying, A. M. Bentley, Q. Meng, J. North, S. R. Durham, A. B. Kay, and Q. Hamid. 1993. Relationships among numbers of bronchoalveolar lavage cells expressing messenger ribonucleic acid for cytokines, asthma symptoms, and airway methacholine responsiveness in atopic asthma. J. Allergy Clin. Immunol. 92: 397-403.
18. Ying, S., S. R. Durham, C. J. Corrigan, Q. Hamid, and A. B. Kay. 1995. Phenotype of cells expressing mRNA for TH2-type (interleukin 4 and interleukin 5) and TH1-type (interleukin 2 and interferon γ) cytokines in bronchoalveolar lavage and bronchial biopsies from atopic asthmatic and normal control subjects. Am. J. Respir. Cell Mol. Biol. 12: 477-487.
19. Elias, J. A., R. J. Homer, Q. Hamid, and C. G. Lee. 2005. Chitinases and chitinase-like proteins in TH2 inflammation and asthma. J. Allergy Clin. Immunol. 116: 497-500.
20. Moqbel, R., and D. I. Pritchard. 1990. Parasites and allergy: evidence for a "cause and effect" relationship. Clin. Exp. Allergy 20: 611-618.
21. Weiss, S. T. 2000. Parasites and asthma/allergy: what is the relationship? J. Allergy Clin. Immunol. 105: 205-210.
22. Zhu, Z., T. Zheng, R. J. Homer, Y. K. Kim, N. Y. Chen, L. Cohn, Q. Hamid, and J. A. Elias. 2004. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678-1682. (Pubitemid 38765861)
23. Hartl, D., H. He, B. Koller, C. Da Silva, R. Homer, C. G. Lee, and J. A. Elias. 2008. Acidic mammalian chitinase is secreted via an ADAM17/EGFR-dependent pathway and stimulates chemokine production by pulmonary epithelial cells. J Biol. Chem. 283: 33472-33482.
24. Zheng, T., Z. Zhu, Z. Wang, R. J. Homer, B. Ma, R. J. Riese, Jr., H. A. Chapman, Jr., S. D. Shapiro, and J. A. Elias. 2000. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J. Clin. Invest. 106: 1081-1093.
25. Schutte, B., M. M. Tinnemans, G. F. Pijpers, M. H. Lenders, and F. C. Ramaekers. 1995. Three parameter flow cytometric analysis for simultaneous detection of cytokeratin, proliferation associated antigens and DNA content. Cytometry 21: 177-186.
26. Rochat, T. R., J. M. Casale, and G. W. Hunninghake. 1988. Characterization of type II alveolar epithelial cells by flow cytometry and fluorescent markers. J. Lab. Clin. Med. 112: 418-425.
27. Spindler, K. D., and M. Spindler-Barth. 1999. Inhibitors of chitinases. EXS 87: 201-209.
28. Reese, T. A., H. E. Liang, A. M. Tager, A. D. Luster, N. Van Rooijen, D. Voehringer, and R. M. Locksley. 2007. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature 447: 92-96.
29. de Souza, P. M., and M. A. Lindsay. 2005. Apoptosis as a therapeutic target for the treatment of lung disease. Curr. Opin. Pharmacol. 5: 232-237. (Pubitemid 40674244)
30. Demedts, I. K., T. Demoor, K. R. Bracke, G. F. Joos, and G. G. Brusselle. 2006. Role of apoptosis in the pathogenesis of COPD and pulmonary emphysema. Respir. Res. 7: 53.
31. Druilhe, A., B. Wallaert, A. Tsicopoulos, Lapa e Silva, J. R., I. Tillie-Leblond, A. B. Tonnel, and M. Pretolani. 1998. Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am. J. Respir. Cell Mol. Biol. 19: 747-757.
32. Henson, P. M. 2003. Possible roles for apoptosis and apoptotic cell recognition in inflammation and fibrosis. Am. J. Respir. Cell Mol. Biol. 29: S70-S76.
33. Lu, Q., E. O. Harrington, and S. Rounds. 2005. Apoptosis and lung injury. Keio J. Med. 54: 184-189.
34. Tesfaigzi, Y. 2006. Roles of apoptosis in airway epithelia. Am. J. Respir. Cell Mol. Biol. 34: 537-547.
35. Xu, G., and Y. Shi. 2007. Apoptosis signaling pathways and lymphocyte homeostasis. Cell Res. 17: 759-771. (Pubitemid 47411431)
36. Wright, J. L., and A. Churg. 2007. Current concepts in mechanisms of emphysema. Toxicol. Pathol. 35: 111-115.
37. Plataki, M., E. Tzortzaki, P. Rytila, M. Demosthenes, A. Koutsopoulos, and N. M. Siafakas. 2006. Apoptotic mechanisms in the pathogenesis of COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 1: 161-171.
38. Spurzem, J. R., and S. I. Rennard. 2005. Pathogenesis of COPD. Semin. Respir. Crit. Care Med. 26: 142-153.
39. Kim, D., and J. Chung. 2002. Akt: versatile mediator of cell survival and beyond. J. Biochem. Mol. Biol. 35: 106-115. (Pubitemid 35216586)
40. Chupp, G. L., C. G. Lee, N. Jarjour, Y. M. Shim, C. T. Holm, S. He, J. D. Dziura, J. Reed, A. J. Coyle, P. Kiener, et al. 2007. A chitinase-like protein in the lung and circulation of patients with severe asthma. N. Engl. J. Med. 357: 2016-2027.
41. Da Silva, C. A., D. Hartl, W. Liu, C. G. Lee, and J. A. Elias. 2008. TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J. Immunol. 181: 4279-4286.
42. Boot, R. G., E. F. Blommaart, E. Swart, K. Ghauharali-van der Vlugt, N. Bijl, C. Moe, A. Place, and J. M. Aerts. 2001. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J. Biol. Chem. 276: 6770-6778. (Pubitemid 37373543)
43. Cohen, L., E. Xueping, J. Tarsi, T. Ramkumar, T. K. Horiuchi, R. Cochran, S. DeMartino, K. B. Schechtman, I. Hussain, M. J. Holtzman, and M. Castro. 2007. Epithelial cell proliferation contributes to airway remodeling in severe asthma. Am. J. Respir. Crit. Care Med. 176: 138-145. (Pubitemid 47057849)
44. Boot, R. G., G. H. Renkema, A. Strijland, A. J. van Zonneveld, and J. M. Aerts. 1995. Cloning of a cDNA encoding chitotriosidase, a human chitinase produced by macrophages. J. Biol. Chem. 270: 26252-26256.
45. Rejman, J. J., and W. L. Hurley. 1988. Isolation and characterization of a novel 39 kilodalton whey protein from bovine mammary secretions collected during the nonlactating period. Biochem. Biophys. Res. Commun. 150: 329-334.
46. Hakala, B. E., C. White, and A. D. Recklies. 1993. Human cartilage gp-39, a major secretory product of articular chondrocytes and synovial cells, is a mammalian member of a chitinase protein family. J. Biol. Chem. 268: 25803-25810.
47. Brameld, K. A., W. D. Shrader, B. Imperiali, and W. A. Goddard, III. 1998. Substrate assistance in the mechanism of family 18 chitinases: theoretical studies of potential intermediates and inhibitors. J. Mol. Biol. 280: 913-923.
48. Sakuda, S., A. Isogai, S. Matsumoto, and A. Suzuki. 1987. Search for microbial insect growth regulators. II. Allosamidin, a novel insect chitinase inhibitor. J. Antibiot. 40: 296-300. (Pubitemid 17044876)
49. Suzuki, S., E. Nakanishi, T. Ohira, R. Kawachi, H. Nagasawa, and S. Sakuda. 2006. Chitinase inhibitor allosamidin is a signal molecule for chitinase production in its producing Streptomyces, I: analysis of the chitinase whose production is promoted by allosamidin and growth accelerating activity of allosamidin. J. Antibiot. 59: 402-409. (Pubitemid 44433245)