Stem cell factor-mediated activation pathways promote murine eosinophil CCL6 production and survival

Journal of Leukocyte Biology

Volumn 81, Issue 4, 2007, Pages 1111-1119

  Dolgachev, Vladislav ^a   Thomas, Molly ^a   Berlin, Aaron ^a   Lukacs, Nicholas W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cell signaling; SCF

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CHEMOKINE; CHEMOKINE CCL6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL KINASE; STEM CELL FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; EOSINOPHIL; GENE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BUTADIENES; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINES, CC; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EOSINOPHILS; MAP KINASE KINASE 1; MICE; NITRILES; SIGNAL TRANSDUCTION; STEM CELL FACTOR;

MURINAE;

EID: 33947681718     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0906595     Document Type: Article

References (80)

1. Boehme, S. A., Sullivan, S. K., Crowe, P. D., Santos, M., Conlon, P. J., Sriramarao, P., Bacon, K. B. (1999) Activation of mitogen-activated protein kinase regulates eotaxin-induced eosinophil migration. J. Immunol. 163, 1611-1618.
2. Elsner, J., Hochstetter, R., Kimmig, D., Kapp, A. (1996) Human eotaxin represents a potent activator of the respiratory burst of human eosinophils. Eur. J. Immunol. 26, 1919-1925.
3. Weltman, J. K., Karim, A. S. (1998) Interleukin-5: a proeosinophil cytokine mediator of inflammation in asthma and a target for antisense therapy. Allergy Asthma Proc. 19, 257-261.
4. Gleich, G. J. (2000) Mechanisms of eosinophil-associated inflammation. J. Allergy Clin. Immunol. 105, 651-663.
5. Kay, A. B., Phipps, S., Robinson, D. S. (2004) A role for eosinophils in airway remodeling in asthma. Trends Immunol. 25, 477-482.
6. Rothenberg, M. E., Hogan, S. P. (2006) The eosinophil. Annu. Rev. Immunol. 24, 147-174.
7. Esnault, S., Malter, J. S. (2002) GM-CSF regulation in eosinophils. Arch. Immunol. Ther. Exp. (Warsz.) 50, 121-130.
8. Lalani, T., Simmons, R.K., Ahmed, A.R. (1999) Biology of IL-5 in health and disease. Ann. Allergy Asthma Immunol. 82, 317-332.
9. Moqbel, R. (1994) Eosinophils, cytokines, and allergic inflammation. Ann. N. Y. Acad. Sci. 725, 223-233.
10. Hansel, T. T., Braun, R. K., De Vries, I. J., Boer, C., Boer, L., Rihs, S., Walker, C. (1993) Eosinophils and cytokines. Agents Actions Suppl. 43, 197-208.
11. Reber, L., Da Silva, C. A., Frossard, N. (2006) Stem cell factor and its receptor c-kit as targets for inflammatory diseases. Eur. J. Pharmacol. 533, 327-340.
12. Yuan, Q., Austen, K. F., Friend, D. S., Heidtman, M., Boyce, J. A. (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.
13. Oliveira, S. H., Taub, D. D., Nagel, J., Smith, R., Hogaboam, C. M., Berlin, A., Lukacs, N. W. (2002) Stem cell factor induces eosinophil activation and degranulation: mediator release and gene array analysis. Blood 100, 4291-4297.
14. Berlin, A. A., Lukacs, N. W. (2005) Treatment of cockroach allergen asthma model with imatinib attenuates airway responses. Am. J. Respir. Crit. Care Med. 171, 35-39.
15. Berlin, A. A., Lincoln, P., Tomkinson, A., Lukacs, N. W. (2004) Inhibition of stem cell factor reduces pulmonary cytokine levels during allergic airway responses. Clin. Exp. Immunol. 136, 15-20.
16. Lukacs, N. W., Strieter, R. M., Lincoln, P. M., Brownell, E., Pullen, D. M., Schock, H. J., Chensue, S. W., Taub, D. D., Kunkel, S. L. (1996) Stem cell factor (c-kit ligand) influences eosinophil recruitment and histamine levels in allergic airway inflammation. J. Immunol. 156, 3945-3951.
17. Fireman, E., Kivity, S., Shahar, I., Reshef, T., Mekori, Y. A. (1999) Secretion of stem cell factor by alveolar fibroblasts in interstitial lung diseases. Immunol. Lett. 67, 229-236.
18. El-Koraie, A. F., Baddour, N. M., Adam, A. G., El Kashef, E. H., El Nahas, A. M. (2001) Role of stem cell factor and mast cells in the progression of chronic glomerulonephritides. Kidney Int. 60, 167-172.
19. Al-Muhsen, S. Z., Shablovsky, G., Olivenstein, R., Mazer, B., Hamid, Q. (2004) The expression of stem cell factor and c-kit receptor in human asthmatic airways. Clin. Exp. Allergy 34, 911-916.
20. Kowalski, M. L., Lewandowska-Polak, A., Wozniak, J., Ptasinska, A., Jankowski, A., Wagrowska-Danilewicz, M., Danilewicz, M., Pawliczak, R. (2005) Association of stem cell factor expression in nasal polyp epithelial cells with aspirin sensitivity and asthma. Allergy 60, 631-637.
21. Lennartsson, J., Blume-Jensen, P., Hermanson, M., Ponten, E., Carlberg, M., Ronnstrand, L. (1999) Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c-kit-mediated activation of the Ras/MAP kinase pathway and c-fos induction. Oncogene 18, 5546-5553.
22. Lennartsson, J., Jelacic, T., Linnekin, D., Shivakrupa, R. (2005) Normal and oncogenic forms of the receptor tyrosine kinase kit. Stem Cells 23, 16-43.
23. Roskoski Jr., R. (2005) Structure and regulation of kit protein-tyrosine kinase - the stem cell factor receptor. Biochem. Biophys. Res. Commun. 338, 1307-1315.
24. Ueda, S., Mizuki, M., Ikeda, H., Tsujimura, T., Matsumura, I., Nakano, K., Daino, H., Honda Zi, Z., Sonoyama, J., Shibayama, H., Sugahara, H., Machii, T., Kanakura, Y. (2002) Critical roles of c-kit tyrosine residues 567 and 719 in stem cell factor-induced chemotaxis: contribution of src family kinase and PI3-kinase on calcium mobilization and cell migration. Blood 99, 3342-3349.
25. Shivakrupa, R., Bernstein, A., Watring, N., Linnekin, D. (2003) Phosphatidylinositol 3′-kinase is required for growth of mast cells expressing the kit catalytic domain mutant. Cancer Res. 63, 4412-4419.
26. Roskoski Jr., R. (2005) Signaling by kit protein-tyrosine kinase - the stem cell factor receptor. Biochem. Biophys. Res. Commun. 337, 1-13.
27. Van Dijk, T. B., van Den Akker, E., Amelsvoort, M. P., Mano, H., Lowenberg, B., von Lindern, M. (2000) Stem cell factor induces phosphatidylinositol 3′-kinase-dependent Lyn/Tec/Dok-1 complex formation in hematopoietic cells. Blood 96, 3406-3413.
28. Pouyssegur, J., Volmat, V., Lenormand, P. (2002) Fidelity and spatio-temporal control in MAP kinase (ERKs) signaling. Biochem. Pharmacol. 64, 755-763.
29. Lukacs, N. W., Standiford, T. J., Chensue, S. W., Kunkel, R. G., Strieter, R. M., Kunkel, S. L. (1996) C-C chemokine-induced eosinophil chemotaxis during allergic airway inflammation. J. Leukoc. Biol. 60, 573-578.
30. Dolgachev, V., Oberley, L. W., Huang, T. T., Kraniak, J. M., Tainsky, M. A., Hanada, K., Separovic, D. (2005) A role for manganese superoxide dismutase in apoptosis after photosensitization. Biochem. Biophys. Res. Commun. 332, 411-417.
31. Dolgachev, V., Farooqui, M. S., Kulaeva, O. I., Tainsky, M. A., Nagy, B., Hanada, K., Separovic, D. (2004) De novo ceramide accumulation due to inhibition of its conversion to complex sphingolipids in apoptotic photosensitized cells. J. Biol. Chem. 279, 23238-23249.
32. Reers, M., Smiley, S. T., Mottola-Hartshorn, C., Chen, A., Lin, M., Chen, L. B. (1995) Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 260, 406-417.
33. Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A., Hirsch, T., Susin, S. A., Petit, P. X., Mignotte, B., Kroemer, G. (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182, 367-377.
34. Salvioli, S., Ardizzoni, A., Franceschi, C., Cossarizza, A. (1997) JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess Δ ψ changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett. 411, 77-82.
35. Sandstrom, K., Hakansson, L., Lukinius, A., Venge, P. (2000) A method to study apoptosis in eosinophils by flow cytometry. J. Immunol. Methods 240, 55-68.
36. Godard, T., Deslandes, E., Lebailly, P., Vigreux, C., Poulain, L., Sichel, F., Poul, J. M., Gauduchon, P. (1999) Comet assay and DNA flow cytometry analysis of staurosporine-induced apoptosis. Cytometry 36, 117-122.
37. Bates, M. E., Green, V. L., Bertics, P. J. (2000) ERK1 and ERK2 activation by chemotactic factors in human eosinophils is interleukin 5-dependent and contributes to leukotriene C(4) biosynthesis. J. Biol. Chem. 275, 10968-10975.
38. Dunn, S. E., Torres, J. V., Oh, J. S., Cykert, D. M., Barrett, J. C. (2001) Up-regulation of urokinase-type plasminogen activator by insulin-like growth factor-I depends upon phosphatidylinositol-3 kinase and mitogen-activated protein kinase kinase. Cancer Res. 61, 1367-1374.
39. Wu, Y., Prystowsky, M. B., Orlofsky, A. (1999) Sustained high-level production of murine chemokine C10 during chronic inflammation. Cytokine 11, 523-530.
40. Simon, H. U. (2001) Regulation of eosinophil and neutrophil apoptosis - similarities and differences. Immunol. Rev. 179, 156-162.
41. Moulding, D. A., Akgul, C., Derouet, M., White, M. R., Edwards, S. W. (2001) BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J. Leukoc. Biol. 70, 783-792.
42. Kashatus, D., Cogswell, P., Baldwin, A. S. (2006) Expression of the Bcl-3 proto-oncogene suppresses p53 activation. Genes Dev. 20, 225-235.
43. Hogan, S. P., Foster, P. S. (1996) Cellular and molecular mechanisms involved in the regulation of eosinophil trafficking in vivo. Med. Res. Rev. 16, 407-432.
44. Hogan, S. P., Koskinen, A., Foster, P. S. (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.
45. Garlisi, C. G., Falcone, A., Hey, J. A., Paster, T. M., Fernandez, X., Rizzo, C. A., Minnicozzi, M., Jones, H., Billah, M. M., Egan, R. W., Umland, S. P. (1997) Airway eosinophils, T cells, Th2-type cytokine mRNA, and hyperreactivity in response to aerosol challenge of allergic mice with previously established pulmonary inflammation. Am. J. Respir. Cell Mol. Biol. 17, 642-651.
46. Kay, A. B. (2005) The role of eosinophils in the pathogenesis of asthma. Trends Mol. Med. 11, 148-152.
47. Justice, J. P., Borchers, M. T., Crosby, J. R., Hines, E. M., Shen, H. H., Ochkur, S. I., McGarry, M. P., Lee, N. A., Lee, J. J. (2003) Ablation of eosinophils leads to a reduction of allergen-induced pulmonary pathology. Am. J. Physiol. Lung Cell. Mol. Physiol. 284, L169-L178.
48. Shen, H. H., Ochkur, S. I., McGarry, M. P., Crosby, J. R., Hines, E. M., Borchers, M. T., Wang, H., Biechelle, T. L., O'Neill, K. R., Ansay, T. L., Colbert, D. C., Cormier, S. A., Justice, J. P., Lee, N. A., Lee, J. J. (2003) A causative relationship exists between eosinophils and the development of allergic pulmonary pathologies in the mouse. J. Immunol. 170, 3296-3305.
49. Sui, X., Krantz, S. B., You, M., Zhao, Z. (1998) Synergistic activation of MAP kinase (ERK1/2) by erythropoietin and stem cell factor is essential for expanded erythropoiesis. Blood 92, 1142-1149.
50. Tan, B. L., Yazicioglu, M. N., Ingram, D., McCarthy, J., Borneo, J., Williams, D. A., Kapur, R. (2003) Genetic evidence for convergence of c-kit- and α4 integrin-mediated signals on class IA PI-3 kinase and the Rac pathway in regulating integrin-directed migration in mast cells. Blood 101, 4725-4732.
51. Kinashi, T., Escobedo, J. A., Williams, L. T., Takatsu, K., Springer, T. A. (1995) Receptor tyrosine kinase stimulates cell-matrix adhesion by phosphatidylinositol 3 kinase and phospholipase C-γ 1 pathways. Blood 86, 2086-2090.
52. Dastych, J., Metcalfe, D. D. (1994) Stem cell factor induces mast cell adhesion to fibronectin. J. Immunol. 152, 213-219.
53. Letuve, S., Druilhe, A., Grandsaigne, M., Aubier, M., Pretolani, M. (2002) Critical role of mitochondria, but not caspases, during glucocorticosteroid-induced human eosinophil apoptosis. Am. J. Respir. Cell Mol. Biol. 26, 565-571.
54. Dewson, G., Cohen, G. M., Wardlaw, A. J. (2001) Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 98, 2239-2247.
55. Dewson, G., Walsh, G. M., Wardlaw, A. J. (1999) Expression of Bcl-2 and its homologues in human eosinophils. Modulation by interleukin-5. Am. J. Respir. Cell Mol. Biol. 20, 720-728.
56. Ochiai, K., Kagami, M., Matsumura, R., Tomioka, H. (1997) IL-5 but not interferon-γ (IFN-γ) inhibits eosinophil apoptosis by up-regulation of bcl-2 expression. Clin. Exp. Immunol. 107, 198-204.
57. Zangrilli, J., Robertson, N., Shetty, A., Wu, J., Hastie, A., Fish, J. E., Litwack, G., Peters, S. P. (2000) Effect of IL-5, glucocorticoid, and Fas ligation on Bcl-2 homologue expression and caspase activation in circulating human eosinophils. Clin. Exp. Immunol. 120, 12-21.
58. Druilhe, A., Arock, M., Le Goff, L., Pretolani, M. (1998) Human eosinophils express bcl-2 family proteins: modulation of Mcl-1 expression by IFN-γ. Am. J. Respir. Cell Mol. Biol. 18, 315-322.
59. Bauer, A., Villunger, A., Labi, V., Fischer, S. F., Strasser, A., Wagner, H., Schmid, R. M., Hacker, G. (2006) The NF-κB regulator Bcl-3 and the BH3-only proteins Bim and Puma control the death of activated T cells. Proc. Natl. Acad. Sci. USA 103, 10979-10984.
60. Simon, H. U. (2006) Molecules involved in the regulation of eosinophil apoptosis. Chem. Immunol. Allergy 91, 49-58.
61. Domae, M., Sagara, H., Sakaue, M., Fukuda, T., Kamikawa, Y. (2003) The antiallergic drug oxatomide promotes human eosinophil apoptosis and suppresses IL-5-induced eosinophil survival. J. Allergy Clin. Immunol. 111, 567-572.
62. Letuve, S., Druilhe, A., Grandsaigne, M., Aubier, M., Pretolani, M. (2001) Involvement of caspases and of mitochondria in Fas ligation-induced eosinophil apoptosis: modulation by interleukin-5 and interferon-γ. J. Leukoc. Biol. 70, 767-775.
63. Iemura, A., Tsai, M., Ando, A., Wershil, B. K., Galli, S. J. (1994) The c-kit ligand, stem cell factor, promotes mast cell survival by suppressing apoptosis. Am. J. Pathol. 144, 321-328.
64. Berlin, A. A., Hogaboam, C. M., Lukacs, N. W. (2006) Inhibition of SCF attenuates peribronchial remodeling in chronic cockroach allergen-induced asthma. Lab. Invest. 86, 557-565.
65. Hall, D. J., Cui, J., Bates, M. E., Stout, B. A., Koenderman, L., Coffer, P. J., Bertics, P. J. (2001) Transduction of a dominant-negative H-Ras into human eosinophils attenuates extracellular signal-regulated kinase activation and interleukin-5-mediated cell viability. Blood 98, 2014-2021.
66. Wong, C. K., Zhang, J. P., Lam, C. W., Ho, C. Y., Hjelm, N. M. (1999) Opposing effects of sodium salicylate and haematopoietic cytokines IL-3, IL-5 and GM-CSF on mitogen-activated protein kinases and apoptosis of EoL-1 cells. Immunol. Invest. 28, 365-379.
67. Huang, H. M., Huang, C. J., Yen, J. J. (2000) Mcl-1 is a common target of stem cell factor and interleukin-5 for apoptosis prevention activity via MEK/MAPK and PI-3K/Akt pathways. Blood 96, 1764-1771.
68. Zhu, Y., Chen, L., Huang, Z., Alkan, S., Bunting, K. D., Wen, R., Wang, D., Huang, H. (2004) Cutting edge: IL-5 primes Th2 cytokine-producing capacity in eosinophils through a STAT5-dependent mechanism. J. Immunol. 173, 2918-2922.
69. Hogan, M. B., Weissman, D. N., Hubbs, A. F., Gibson, L. F., Piktel, D., Landreth, K. S. (2003) Regulation of eosinophilopoiesis in a murine model of asthma. J. Immunol. 171, 2644-2651.
70. Williams, T. J. (2004) The eosinophil enigma. J. Clin. Invest. 113, 507-509.
71. Stock, P., Akbari, O., Dekruyff, R. H., Umetsu, D. T. (2005) Respiratory tolerance is inhibited by the administration of corticosteroids. J. Immunol. 175, 7380-7387.
72. Zhang, S., Howarth, P. H., Roche, W. R. (1996) Cytokine production by cell cultures from bronchial subepithelial myofibroblasts. J. Pathol. 180, 95-101.
73. Kim, Y. K., Nakagawa, N., Nakano, K., Sulakvelidze, I., Dolovich, J., Denburg, J. (1997) Stem cell factor in nasal polyposis and allergic rhinitis: increased expression by structural cells is suppressed by in vivo topical corticosteroids. J. Allergy Clin. Immunol. 100, 389-399.
74. Hogaboam, C., Kunkel, S. L., Strieter, R. M., Taub, D. D., Lincoln, P., Standiford, T. J., Lukacs, N. W. (1998) Novel role of transmembrane SCF for mast cell activation and eotaxin production in mast cell-fibroblast interactions. J. Immunol. 160, 6166-6171.
75. Jippo-Kanemoto, T., Adachi, S., Ebi, Y., Matsuda, H., Kasugai, T., Nishikawa, S., Kitamura, Y. (1992) BALB/3T3 fibroblast-conditioned medium attracts cultured mast cells derived from W/W but not from mi/mi mutant mice, both of which are deficient in mast cells. Blood 80, 1933-1939.
76. Fireman, E., Kivity, S., Shahar, I., Reshef, T., Mekori, Y. A. (1999) Secretion of stem cell factor by alveolar fibroblasts in interstitial lung diseases. Immunol. Lett. 67, 229-236.
77. Linenberger, M. L., Jacobson, F. W., Bennett, L. G., Broudy, V. C., Martin, F. H., Abkowitz, J. L. (1995) Stem cell factor production by human marrow stromal fibroblasts. Exp. Hematol. 23, 1104-1114.
78. Kassel, O., Schmidlin, F., Duvernelle, C., Gasser, B., Massard, G., Frossard, N. (1999) Human bronchial smooth muscle cells in culture produce stem cell factor. Eur. Respir. J. 13, 951-954.
79. Oliveira, S. H., Hogaboam, C. M., Berlin, A., Lukacs, N. W. (2001) SCF-induced airway hyperreactivity is dependent on leukotriene production. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L1242-L1249.
80. Campbell, E., Hogaboam, C., Lincoln, P., Lukacs, N. W. (1999) Stem cell factor-induced airway hyperreactivity in allergic and normal mice. Am. J. Pathol. 154, 1259-1265.