Oxidant-mediated mitochondrial injury in eosinophil apoptosis: Enhancement by glucocorticoids and inhibition by granulocyte-macrophage colony-stimulating factor

Journal of Immunology

Volumn 170, Issue 1, 2003, Pages 556-566

  Gardai, Shyra J ^b   Hoontrakoon, Raweewan ^a   Goddard, Cally D ^a   Day, Brian J ^a,b   Chang, Ling Yi ^a,b   Henson, Peter M ^a,b   Bratton, Donna L ^a,b  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; DEXAMETHASONE; FLAVOPROTEIN; GLUCOCORTICOID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MANGANESE SUPEROXIDE DISMUTASE; OXIDIZING AGENT; PHOSPHOTRANSFERASE INHIBITOR; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE;

APOPTOSIS; ARTICLE; ASTHMA; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVATION; EOSINOPHIL; HUMAN; HUMAN CELL; HYPOXIA; INJURY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; OXIDATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; X CHROMOSOME LINKAGE;

EID: 0037222933     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.1.556     Document Type: Article

References (70)

1. Wardlaw, A. J. 1999. Molecular basis for selective eosinophil trafficking in asthma: A multistep paradigm. J. Allergy Clin. Immunol. 104:917.
2. Hoontrakoon, R., H. W. Chu, S. J. Gardai, S. E. Wenzel, P. McDonald, V. A. Fadok, P. M. Henson, and D. L. Bratton. 2002. Interleukin-15 inhibits spontaneous apoptosis in human eosinophils via autocrine production of granulocyte macrophage-colony stimulating factor and nuclear factor-κB activation. Am. J. Respir. Cell Mol. Biol. 26:404.
3. Gleich, G. J. 2000. Mechanisms of eosinophil-associated inflammation. J. Allergy Clin. Immunol. 105:651.
4. Kankaanranta, H., M. A. Lindsay, M. A. Giembycz, X. Zhang, E. Moilanen, and P. J. Barnes. 2000. Delayed eosinophil apoptosis in asthma. J. Allergy Clin. Immunol. 106:77.
5. Wedi, B., U. Raap, H. Lewrick, and A. Kapp. 1997. Delayed eosinophil programmed cell death in vitro: A common feature of inhalant allergy and extrinsic and intrinsic atopic dermatitis. J. Allergy Clin. Immunol. 100:536.
6. Simon, H.-U., S. Yousefi, C. Schranz, A. Schapowal, C. Bachert, and K. Blaser. 1997. Direct demonstration of delayed eosinophil apoptosis as a mechanism causing tissue eosinophilia. J. Immunol. 158:3902.
7. Vignola, A. M., P. Chanez, G. Chiappara, L. Siena, A. Merendino, C. Reina, R. Gagliardo, M. Profita, J. Bousquet, and G. Bonsignore. 1999. Evaluation of apoptosis of eosinophils, macrophages, and T lymphocytes in mucosal biopsy specimens of patients with asthma and chronic bronchitis. J. Allergy Clin. Immunol. 103:563.
8. Bratton, D. L., and V. A. Fadok. 1999. Their's but to do and die: Eosinophil longevity in asthma. J. Allergy Clin. Immunol. 103:555.
9. Peachman, K. K., D. S. Lyles, and D. A. Bass. 2001. Mitochondria in eosinophils: Functional role in apoptosis but not respiration. Proc. Natl. Acad. Sci. USA 98:1717.
10. Dewson, G., G. M. Cohen, and A. J. Wardlaw. 2001. Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 98:2239.
11. Kawabori, S., K. Soda, M. H. Perdue, and J. Bienenstock. 1991. The dynamics of intestinal eosinophil depletion in rats treated with dexamethasone. Lab. Invest. 64:224.
12. Zangrilli, J., N. Robertson, A. Sherry, J. Wu, A. Hastie, J. E. Fish, G. Litwack, and S. P. Peters. 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.
13. Zhang, J. P., C. K. Wong, and C. W. Lam. 2000. Role of caspases in dexamethasone-induced apoptosis and activation of c-Jun NH2-terminal kinase and p38 mitogen-activated protein kinase in human eosinophils. Clin. Exp. Immunol. 122:20.
14. Woolley, K., P. Gibson, K. Carty, A. Wilson, S. Twaddell, and M. Woolley. 1996. Eosinophil apoptosis and the resolution of airway inflammation in asthma. Am. J. Respir. Crit. Care Med. 154:237.
15. Druilhe, A., B. Wallaert, A. Tsicopoulos, J.-R. Lapa e Silva, 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. Ant. J. Respir. Cell Mol. Biol. 19:747.
16. Mann, C. L., F. M. Hughes Jr., and J. A. Cidlowski. 2000. Delineation of the signaling pathways involved in glucocorticoid-induced and spontaneous apoptosis of rat thymocytes. Endocrinology 141:528.
17. Petit, P. X., H. Lecoeur, E. Zorn, C. Dauguet, B. Mignotte, and M. L. Gougeon. 1995. Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. J. Cell Biol. 130:157.
18. Brunetti, M., N. Martelli, A. Colasante, M. Piantelli, P. Musiani, and F. B. Aiello. 1995. Spontaneous and glucocorticoid-induced apoptosis in human mature T lymphocytes. Blood 86:4199.
19. Zamzami, N., P. Marchetti, M. Castedo, C. Zanin, J. L. Vayssiere, P. X. Petit, and G. Kroemer. 1995. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1661.
20. Hirsch, T., P. Marchetti, S. A. Susin, B. Dallaporta, N. Zamzami, I. Marzo, M. Geuskens, and G. Kroemer. 1997. The apoptosis-necrosis paradox: Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15:1573.
21. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S. A. Susin, P. X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367.
22. Hildeman, D. A., T. Mitchell, T. K. Teague, P. Henson, B. J. Day, J. Kappler, and P. C. Marrack. 1999. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10:735.
23. Hockenbery, D. M., Z. N. Oltvai, X. M. Yin, C. L. Milliman, and S. J. Korsmeyer, 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241.
24. Van Houten, N., S. F. Blake, E. J. Li, T. A. Hallam, D. G. Chilton, W. K. Gourley, L. H. Boise, C. B. Thompson, and E. B. Thompson. 1997. Elevated expression of Bcl-2 and Bcl-x by intestinal intraepithelial lymphocytes: Resistance to apoptosis by glucocorticoids and irradiation. Int. Immunol. 9:945.
25. Miyashita, T., K. Nagao, S. Krajewski, G. S. Salvesen, J. C. Reed, T. Inoue, and M. Yamada. 1998. Investigation of glucocorticoid-induced apoptotic pathway: Processing of caspase-6 but not caspase-3. Cell Death Differ. 5:1034.
26. Arai, Y., Y. Nakamura, F. Inoue, K. Yamamoto, K. Saito, and S. Furusawa. 2000. Glucocorticoid-induced apoptotic pathways in eosinophils: Comparison with glucocorticoid-sensitive leukemia cells. Int. J. Hematol. 71:340.
27. Letuve, S., A. Druilhe, M. Grandsaigne, M. Aubier, and M. Pretolani. 2002. Critical role of mitochondria, but not caspases, during glucocorticosteroid-induced human eosinophil apoptosis. Am. J. Respir. Cell Mol. Biol. 26:565.
28. Li, Y., and M. A. Trush. 1998. Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem. Biophys. Res. Commun. 253:295.
29. Day, B. J., S. Shawen, S. I. Liochev, and J. D. Crapo. 1995. A metalloporphyrin superoxide dismutase mimetic protects against paraquat-induced endothelial cell injury, in vitro. J. Pharmacol. Exp. Ther. 275:1227.
30. Frasch, S. C., P. M. Henson, J. M. Kailey, D. A. Richter, M. S. Janes, V. A. Fadok, and D. L. Bratton. 2000. Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cδ. J. Biol. Chem. 275:23065.
31. Cossarizza, A., C. Franceschi, D. Monti, S. Salvioli, E. Bellesia, R. Rivabene, L. Biondo, G. Rainaldi, A. Tinari, and W. Malorni. 1995. Protective effect of N-acetylcysteine in tumor necrosis factor-α-induced apoptosis in U937 cells: The role of mitochondria. [Published erratum appears in 1996 Exp. Cell Res. 222:251.] Exp. Cell Res. 220:232.
32. Her, E., J. Frazer, K. F. Austen, and W. F. Owen Jr. 1991. Eosinophil hematopoietins antagonize the programmed cell death of eosinophils: Cytokine and glucocorticoid effects on eosinophils maintained by endothelial cell-conditioned medium. J. Clin. Invest. 88:1982.
33. Hannah, S., K. Mecklenburgh, I. Rahman, G. J. Bellingan, A. Greening, C. Haslett, and E. R. Chilvers. 1995. Hypoxia prolongs neutrophil survival in vitro. FEBS Lett. 372:233.
34. Chakraborti, T., S. Das, M. Mondal, S. Roychoudhury, and S. Chakraborti. 1999. Oxidant, mitochondria and calcium: An overview. Cell. Signal. 11:77.
35. Melov, S., J. A. Schneider, B. J. Day, D. Hinerfeld, P. Coskun, S. S. Mirra, J. D. Crapo, and D. C. Wallace. 1998. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18:159.
36. Valentine, J. F., and H. S. Nick. 1994. Glucocorticoids repress basal and stimulated manganese superoxide dismutase levels in rat intestinal epithelial cells. Gastroenterology 107:1662.
37. Pereira, B., L. F. Rosa, D. A. Safi, E. J. Bechara, and R. Curi. 1995. Hormonal regulation of superoxide dismutase, catalase, and glutathione peroxidase activities in rat macrophages. Biochem. Pharmacol. 50:2093.
38. Ito, Y., N. C. Mishra, K. Yoshida, S. Kharbanda, S. Saxena, and D. Kufe. 2001. Mitochondrial targeting of JNK/SAPK in the phorbol ester response of myeloid leukemia cells. Cell Death Differ. 8:794.
39. L in response to DNA damage. J. Biol. Chem. 275:322.
40. Bennett, B. L., D. T. Sasaki, B. W. Murray, E. C. O'Leary, S. T. Sakata, W. Xu, J. C. Leisten, A. Motiwala, S. Pierce, Y. Satoh, et al. 2001. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98:13681.
41. Tang, G., Y. Minemoto, B. Dibling, N. H. Purcell, Z. Li, M. Karin, and A. Lin. 2001. Inhibition of JNK activation through NF-κB target genes. Nature 414:313.
42. Kyriakis, J. M. 2001. Life-or-death decisions. Nature 414:265.
43. Yang, Y., S. Fang, J. P. Jensen, A. M. Weissman, and J. D. Ashwell. 2000. Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 288:874.
44. Yamamoto, H., J. B. Sedgwick, R. F. Vrtis, and W. W. Busse. 2000. The effect of transendothelial migration on eosinophil function. Am. J. Respir. Cell Mol. Biol. 23:379.
45. Horie, S., G. J. Gleich, and H. Kita. 1996. Cytokines directly induce degranulation and superoxide production from human eosinophils. J. Allergy Clin. Immunol. 98:371.
46. Sattler, M., T. Winkler, S. Verma, C. H. Byrne, G. Shrikhande, R. Salgia, and J. D. Griffin. 1999. Hematopoietic growth factors signal through the formation of reactive oxygen species. Blood 93:2928.
47. Carcamo, J. M., O. Borquez-Ojeda, and D. W. Golde. 2002. Vitamin C inhibits granulocyte macrophage-colony-stimulating factor-induced signaling pathways. Blood 99:3205.
48. Loeffler, M., and G. Kroemer. 2000. The mitochondrion in cell death control: Certainties and incognita. Exp. Cell Res. 256:19.
49. Goossens, V., J. Grooten, K. De Vos, and W. Fiers. 1995. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc. Natl. Acad. Sci. USA 92:8115.
50. Wedi, B., J. Straede, B. Wieland, and A. Kapp. 1999. Eosinophil apoptosis is mediated by stimulators of cellular oxidative metabolisms and inhibited by antioxidants: Involvement of a thiol-sensitive redox regulation in eosinophil cell death. Blood 94:2365.
51. Zhang, N. 1996. Characterization of the 5′ flanking region of the human MnSOD gene. Biochem. Biophys. Res. Commun. 220:171.
52. Maehara, K., T. Hasegawa, and K. I. Isobe. 2000. A NF-κB p65 subunit is indispensable for activating manganese superoxide: Dismutase gene transcription mediated by tumor necrosis factor-α. J. Cell. Biochem. 77:474.
53. Jones, P. L., D. Ping, and J. M. Boss. 1997. Tumor necrosis factor α and interleukin-1β regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-β and NF-κB. Mol. Cell. Biol. 17:6970.
54. Li, Y., T. T. Huang, E. J. Carlson, S. Melov, P. C. Ursell, J. L. Olson, L. J. Noble, M. P. Yoshimura, C. Berger, P. H. Chan, et al. 1995. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11:376.
55. Fujimura, M., Y. Morita-Fujimura, M. Kawase, J. C. Copin, B. Calagui, C. J. Epstein, and P. H. Chan. 1999. Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome C and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J. Neurosci. 19:3414.
56. +/- mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc. Natl. Acad. Sci. USA 98:2278.
57. Chen, K., J. A. Vita, B. C. Berk, and J. F. Keaney Jr. 2001. c-Jun N-terminal kinase activation by hydrogen peroxide in endothelial cells involves SRC-dependent epidermal growth factor receptor transactivation. J. Biol. Chem. 276:16045.
58. Tournier, C., P. Hess, D. D. Yang, J. Xu, T. K. Turner, A. Nimnual, D. Bar-Sagi, S. N. Jones, R. A. Flavell, and R. J. Davis. 2000. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870.
59. Tsujimoto, Y., and S. Shimizu. 2000. Bcl-2 family: Life-or-death switch. FEBS Lett. 466:6.
60. Wang, C. Y., M. W. Mayo, R. G. Korneluk, D. V. Goeddel, and A. S. Baldwin Jr. 1998. NF-κB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680.
61. Du, J., W. E. Mitch, X. Wang, and S. R. Price. 2000. Glucocorticoids induce proteasome C3 subunit expression in L6 muscle cells by opposing the suppression of its transcription by NF-κB. J. Biol. Chem. 275:19661.
62. Shang, F., X. Gong, and A. Taylor. 1997. Activity of ubiquitin-dependent pathway in response to oxidative stress: Ubiquitin-activating enzyme is transiently up-regulated. J. Biol. Chem. 272:23086.
63. Dewson, G., G. M. Walsh, and A. J. Wardlaw. 1999. Expression of Bcl-2 and its homologues in human eosinophils: Modulation by interleukin-5. Am. J. Respir. Cell Mol. Biol. 20:720.
64. Druilhe, A., M. Arock, L. Le Goff, and M. Pretolani. 1998. Human eosinophils express bcl-2 family proteins: Modulation of Mcl-1 expression by IFN-γ. Am. J. Respir. Cell Mol. Biol. 18:315.
65. Sousa, A. R., S. J. Lane, J. A. Cidlowski, D. Z. Staynov, and T. H. Lee. 2000. Glucocorticoid resistance in asthma is associated with elevated in vivo expression of the glucocorticoid receptor β-isoform. J. Allergy Clin. Immunol. 105:943.
66. Hamid, Q. A., S. E. Wenzel, P. J. Hauk, A. Tsicopoulos, B. Wallaert, J. J. Lafitte, G. P. Chrousos, S. J. Szefler, and D. Y. Leung. 1999. Increased glucocorticoid receptor β in airway cells of glucocorticoid-insensitive asthma. Am. J. Respir. Crit. Care Med. 159:1600.
67. Hamilos, D. L., D. Y. Leung, S. Muro, A. M. Kahn, S. S. Hamilos, S. E. Thawley, and Q. A. Hamid. 2001. GRβ expression in nasal polyp inflammatory cells and its relationship to the anti-inflammatory effects of intranasal fluticasone. J. Allergy Clin. Immunol. 108:59.
68. Strickland, I., K. Kisich, P. J. Hauk, A. Vottero, P. Chrousos, D. J. Klemm, and D. Y. M. Leung. 2001. High constitutive glucocorticoid receptor β in human neutrophils enables them to reduce their spontaneous rate of cell death in response to corticosteroids. J. Exp. Med. 193:585.
69. Leung, D. Y. M., 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.
70. Vrugt, B., S. Wilson, J. Underwood, A. Bron, R. de Bruyn, P. Bradding, S. T. Holgate, R. Djukanovic, and R. Aalbers. 1999. Mucosal inflammation in severe glucocorticoid-dependent asthma. Eur. Respir. J. 13:1245.