Pulmonary IL-17E (IL-25) production and IL-17RB+ myeloid cell-derived Th2 cytokine production are dependent upon stem cell factor-induced responses during chronic allergic pulmonary disease

Journal of Immunology

Volumn 183, Issue 9, 2009, Pages 5705-5715

  Dolgachev, Vladislav ^a   Petersen, Bryan C ^a   Budelsky, Alison L ^b   Berlin, Aaron A ^a   Lukacs, Nicholas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CD11B ANTIGEN; CD4 ANTIGEN; ENHANCED GREEN FLUORESCENT PROTEIN; GLYCOPROTEIN P 15095; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 25; INTERLEUKIN 25 RECEPTOR B; INTERLEUKIN 4; INTERLEUKIN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; STEM CELL FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; ATTENUATION; BONE MARROW CELL; CELL MATURATION; CELL POPULATION; CHRONIC ALLERGIC PULMONARY DISEASE; CHRONIC LUNG DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHIL; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN BLOOD LEVEL; INFLAMMATION; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH2 CELL;

ANIMALS; ANTIGENS, CD11B; BONE MARROW CELLS; CELL DIFFERENTIATION; CHRONIC DISEASE; CYTOKINES; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-4; INTERLEUKINS; LUNG; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MYELOID CELLS; RECEPTORS, CHEMOKINE; RECEPTORS, INTERLEUKIN-17; RESPIRATORY HYPERSENSITIVITY; STEM CELL FACTOR; TH2 CELLS;

EID: 77953795713     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901666     Document Type: Article

References (44)

1. Lukacs, N. W., S. L. Kunkel, R. M. Strieter, H. L. Evanoff, R. G. Kunkel, M. L. Key, and D. D. Taub. 1996. The role of stem cell factor (c-kit ligand) and inflammatory cytokines in pulmonary mast cell activation. Blood 87: 2262-2268.
2. Lukacs, N. W., R. M. Strieter, P. M. Lincoln, E. Brownell, D. M. Pullen, H. J. Schock, S. W. Chensue, D. D. Taub, and S. L. Kunkel. 1996. Stem cell factor (c-kit ligand) influences eosinophil recruitment and histamine levels in allergic airway inflammation. J. Immunol. 156: 3945-3951.
3. Campbell, E., C. Hogaboam, P. Lincoln, and N. W. Lukacs. 1999. Stem cell factor-induced airway hyperreactivity in allergic and normal mice. Am. J. Pathol. 154: 1259-1265. (Pubitemid 29169759)
4. Oliveira, S. H., C. M. Hogaboam, A. Berlin, and N. W. Lukacs. 2001. SCF-induced airway hyperreactivity is dependent on leukotriene production. Am. J. Physiol. 280: L1242-L1249.
5. Reber, L., C. A. Da Silva, and N. Frossard. 2006. Stem cell factor and its receptor c-Kit as targets for inflammatory diseases. Eur. J. Pharmacol. 533: 327-340.
6. Krishnaswamy, G., J. Kelley, D. Johnson, G. Youngberg, W. Stone, S. K. Huang, J. Bieber, and D. S. Chi. 2001. The human mast cell: functions in physiology and disease. Front. Biosci. 6: D1109-D1127.
7. Kassel, O., F. Schmidlin, C. Duvernelle, F. de Blay, and N. Frossard. 1998. Upand down-regulation by glucocorticoids of the constitutive expression of the mast cell growth factor stem cell factor by human lung fibroblasts in culture. Mol. Pharmacol. 54: 1073-1079.
8. Columbo, M., E. M. Horowitz, L. M. Botana, D. W. MacGlashan, Jr., B. S. Bochner, S. Gillis, K. M. Zsebo, S. J. Galli, and L. M. Lichtenstein. 1992. The human recombinant c-kit receptor ligand, rhSCF, induces mediator release from human cutaneous mast cells and enhances IgE-dependent mediator release from both skin mast cells and peripheral blood basophils. J. Immunol. 149: 599-608.
9. Sutcliffe, A., D. Kaur, S. Page, L. Woodman, C. L. Armour, M. Baraket, P. Bradding, J. M. Hughes, and C. E. Brightling. 2006. Mast cell migration to Th2 stimulated airway smooth muscle from asthmatics. Thorax 61: 657-662.
10. Berger, P., P. O. Girodet, and J. M. Tunon-de-Lara. 2005. Mast cell myositis: a new feature of allergic asthma? Allergy 60: 1238-1240.
11. Da Silva, C. A., and N. Frossard. 2005. Potential role of stem cell factor in the asthma control by glucocorticoids. Chem. Immunol. Allergy 87: 154-162. (Pubitemid 43093186)
12. Al-Muhsen, S. Z., G. Shablovsky, R. Olivenstein, B. Mazer, and Q. Hamid. 2004. The expression of stem cell factor and c-kit receptor in human asthmatic airways. Clin. Exp. Allergy 34: 911-916.
13. Kowalski, M. L., A. Lewandowska-Polak, J. Wozniak, A. Ptasinska, A. Jankowski, M. Wagrowska-Danilewicz, M. Danilewicz, and R. Pawliczak. 2005. Association of stem cell factor expression in nasal polyp epithelial cells with aspirin sensitivity and asthma. Allergy 60: 631-637.
14. Lei, Z., G. Liu, Q. Huang, M. Lv, R. Zu, G. M. Zhang, Z. H. Feng, and B. Huang. 2007. SCF and IL-31 rather than IL-17 and BAFF are potential indicators in patients with allergic asthma. Allergy 63: 327-332.
15. Oliveira, S. H., D. D. Taub, J. Nagel, R. Smith, C. M. Hogaboam, A. Berlin, and N. W. Lukacs. 2002. Stem cell factor induces eosinophil activation and degranulation: mediator release and gene array analysis. Blood 100: 4291-4297.
16. Berlin, A. A., P. Lincoln, A. Tomkinson, and N. W. Lukacs. 2004. Inhibition of stem cell factor reduces pulmonary cytokine levels during allergic airway responses. Clin. Exp. Immunol. 136: 15-20.
17. Dolgachev, V., M. Thomas, A. Berlin, and N. W. Lukacs. 2007. Stem cell factormediated activation pathways promote murine eosinophil CCL6 production and survival. J. Leukocyte Biol. 81: 1111-1119.
18. Berlin, A. A., C. M. Hogaboam, and N. W. Lukacs. 2006. Inhibition of SCF attenuates peribronchial remodeling in chronic cockroach allergen-induced asthma. Lab. Invest. 86: 557-565.
19. Kawaguchi, M., M. Adachi, N. Oda, F. Kokubu, and S. K. Huang. 2004. IL-17 cytokine family. J. Allergy Clin. Immunol. 114: 1265-1273.
20. Fort, M. M., J. Cheung, D. Yen, J. Li, S. M. Zurawski, S. Lo, S. Menon, T. Clifford, B. Hunte, R. Lesley, et al. 2001. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15: 985-995.
21. Ballantyne, S. J., J. L. Barlow, H. E. Jolin, P. Nath, A. S. Williams, K. F. Chung, G. Sturton, S. H. Wong, and A. N. McKenzie. 2007. Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. J. Allergy Clin. Immunol. 120: 1324-1331.
22. Angkasekwinai, P., H. Park, Y. H. Wang, Y. H. Wang, S. H. Chang, D. B. Corry, Y. J. Liu, Z. Zhu, and C. Dong. 2007. Interleukin 25 promotes the initiation of proallergic type 2 responses. J. Exp. Med. 204: 1509-1517.
23. Tamachi, T., Y. Maezawa, K. Ikeda, S. Kagami, M. Hatano, Y. Seto, A. Suto, K. Suzuki, N. Watanabe, Y. Saito, T. Tokuhisa, I. Iwamoto, and H. Nakajima. 2006. IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J. Allergy Clin. Immunol. 118: 606-614.
24. Tamachi, T., Y. Maezawa, K. Ikeda, I. Iwamoto, and H. Nakajima. 2006. Interleukin 25 in allergic airway inflammation. Int. Arch. Allergy Immunol. 140(Suppl. 1): 59-62.
25. Fallon, P. G., S. J. Ballantyne, N. E. Mangan, J. L. Barlow, A. Dasvarma, D. R. Hewett, A. McIlgorm, H. E. Jolin, and A. N. McKenzie. 2006. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 203: 1105-1116.
26. Wong, C. K., P. W. Li, and C. W. Lam. 2007. Intracellular JNK, p38 MAPK and NF-κB regulate IL-25 induced release of cytokines and chemokines from costimulated T helper lymphocytes. Immunol. Lett. 112: 82-91.
27. Wang, Y. H., P. Angkasekwinai, N. Lu, K. S. Voo, K. Arima, S. Hanabuchi, A. Hippe, C. J. Corrigan, C. Dong, B. Homey, et al. 2007. IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J. Exp. Med. 204: 1837-1847.
28. Montero Vega, M. T. 2006. New aspects on inflammation in allergic diseases. Allergol. Immunopathol. (Madr.). 34: 156-170.
29. Kim, E. Y., J. T. Battaile, A. C. Patel, Y. You, E. Agapov, M. H. Grayson, L. A. Benoit, D. E. Byers, Y. Alevy, J. Tucker, et al. 2008. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14: 633-640.
30. Rickel, E. A., L. A. Siegel, B. R. Yoon, J. B. Rottman, D. G. Kugler, D. A. Swart, P. M. Anders, J. E. Tocker, M. R. Comeau, and A. L. Budelsky. 2008. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J. Immunol. 181: 4299-4310.
31. Campbell, E. M., S. L. Kunkel, R. M. Strieter, and N. W. Lukacs. 1998. Temporal role of chemokines in a murine model of cockroach allergen-induced airway hyperreactivity and eosinophilia. J. Immunol. 161: 7047-7053.
32. Lindell, D. M., A. A. Berlin, M. A. Schaller, and N. W. Lukacs. 2008. B cell antigen presentation promotes Th2 responses and immunopathology during chronic allergic lung disease. PLoS ONE 3: e3129.
33. Yuan, Q., K. F. Austen, D. S. Friend, M. Heidtman, and J. A. Boyce. 1997. Human peripheral blood eosinophils express a functional c-kit receptor for stem cell factor that stimulates very late antigen 4 (VLA-4)-mediated cell adhesion to fibronectin and vascular cell adhesion molecule 1 (VCAM-1). J. Exp. Med. 186: 313-323.
34. Dolgachev, V. A., M. R. Ullenbruch, N. W. Lukacs, and S. H. Phan. 2009. Role of stem cell factor and bone marrow-derived fibroblasts in airway remodeling. Am. J. Pathol. 174: 390-400.
35. Finotto, S., M. Buerke, K. Lingnau, E. Schmitt, P. R. Galle, and M. F. Neurath. 2001. Local administration of antisense phosphorothioate oligonucleotides to the c-kit ligand, stem cell factor, suppresses airway inflammation and IL-4 production in a murine model of asthma. J. Allergy Clin. Immunol. 107: 279-286.
36. Da Silva, C. A., and N. Frossard. 2005. Regulation of stem cell factor expression in inflammation and asthma. Mem. Inst. Oswaldo Cruz 100(Suppl. 1): 145-151. (Pubitemid 40685455)
37. Sharkhuu, T., K. I. Matthaei, E. Forbes, S. Mahalingam, S. P. Hogan, P. M. Hansbro, and P. S. Foster. 2006. Mechanism of interleukin-25 (IL-17E)-induced pulmonary inflammation and airways hyper-reactivity. Clin. Exp. Allergy. 36: 1575-1583.
38. Ray, P., N. Krishnamoorthy, and A. Ray. 2008. Emerging functions of c-kit and its ligand stem cell factor in dendritic cells: regulators of T cell differentiation. Cell Cycle 7: 2826-2832.
39. Krishnamoorthy, N., T. B. Oriss, M. Paglia, M. Fei, M. Yarlagadda, B. Vanhaesebroeck, A. Ray, and P. Ray. 2008. Activation of c-Kit in dendritic cells regulates T helper cell differentiation and allergic asthma. Nat. Med. 14: 565-573.
40. Dolgachev, V., A. A. Berlin, and N. W. Lukacs. 2007. Eosinophil activation of fibroblasts from chronic allergen-induced disease utilizes stem cell factor for phenotypic changes. Am. J. Pathol. 172: 68-76.
41. + inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29: 306-317.
42. Engel, D. R., J. Maurer, A. P. Tittel, C. Weisheit, T. Cavlar, B. Schumak, A. Limmer, N. van Rooijen, C. Trautwein, F. Tacke, and C. Kurts. 2008. CCR2 mediates homeostatic and inflammatory release of Gr1high monocytes from the bone marrow, but is dispensable for bladder infiltration in bacterial urinary tract infection. J. Immunol. 181: 5579-5586.
43. Serbina, N. V., and E. G. Pamer. 2006. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7: 311-317.
44. Ikeda, K., H. Nakajima, K. Suzuki, S. Kagami, K. Hirose, A. Suto, Y. Saito, and I. Iwamoto. 2003. Mast cells produce interleukin-25 upon FcεRI-mediated activation. Blood 101: 3594-3596.