Mitochondria in the center of human eosinophil apoptosis and survival

International Journal of Molecular Sciences

Volumn 15, Issue 3, 2014, Pages 3952-3969

  Ilmarinen, Pinja ^a   Moilanen, Eeva ^a   Kankaanranta, Hannu ^a,b  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b SEINÄJOKI CENTRAL HOSPITAL   (Finland)

Author keywords

Apoptosis; Asthma; Eosinophil; Glucocorticoids; Mitochondria; Mitochondrial permeability transition; Mitogen activated protein kinase; Nitric oxide; Reactive oxygen species; Survival

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; APOPTOSIS SIGNAL REGULATING KINASE 1; CYTOCHROME C; FAS ASSOCIATED DEATH DOMAIN PROTEIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROGEN PEROXIDE; INTERLEUKIN 5; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEIN MCL 1; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE 1; SUPEROXIDE DISMUTASE; UNINDEXED DRUG;

APOPTOSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DNA FRAGMENTATION; EOSINOPHIL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; REVIEW; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; DRUG EFFECTS; HUMAN; METABOLISM; PHYSIOLOGY;

APOPTOSIS; CELL SURVIVAL; EOSINOPHILS; GLUCOCORTICOIDS; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; NITRIC OXIDE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84896479466     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15033952     Document Type: Review

References (115)

1. Trivedi, S. G.; Lloyd, C. M. Eosinophils in the pathogenesis of allergic airways disease. Cell. Mol. Life Sci. 2007, 64, 1269-1289.
2. Zuo, L.; Rothenberg, M. E. Gastrointestinal eosinophilia. Immunol. Allergy Clin. N. Am. 2007, 27, 443-455.
3. Gleich, G. J.; Leiferman, K. M. The hypereosinophilic syndromes: Current concepts and treatments. Br. J. Haematol. 2009, 145, 271-285.
4. Ellyard, J. I.; Simson, L.; Parish, C. R. Th2-mediated anti-tumour immunity: Friend or foe? Tissue Antigens 2007, 70, 1-11.
5. Klion, A. D.; Nutman, T. B. The role of eosinophils in host defense against helminth parasites. J. Allergy Clin. Immunol. 2004, 113, 30-37.
6. Hogan, S. P.; Rosenberg, H. F.; Moqbel, R.; Phipps, S.; Foster, P. S.; Lacy, P.; Kay, A. B.; Rothenberg, M. E. Eosinophils: Biological properties and role in health and disease. Clin. Exp. Allergy 2008, 38, 709-750.
7. Jacobsen, E. A.; Ochkur, S. I.; Pero, R. S.; Taranova, A. G.; Protheroe, C. A.; Colbert, D. C.; Lee, N. A.; Lee, J. J. Allergic pulmonary inflammation in mice is dependent on eosinophil-induced recruitment of effector T cells. J. Exp. Med. 2008, 205, 699-710.
8. Humbles, A. A.; Lloyd, C. M.; McMillan, S. J.; Friend, D. S.; Xanthou, G.; McKenna, E. E.; Ghiran, S.; Gerard, N. P.; Yu, C.; Orkin, S. H.; et al. A critical role for eosinophils in allergic airways remodeling. Science 2004, 305, 1776-1779.
9. Nair, P.; Pizzichini, M. M.; Kjarsgaard, M.; Inman, M. D.; Efthimiadis, A.; Pizzichini, E.; Hargreave, F. E.; O'Byrne, P. M. Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N. Engl. J. Med. 2009, 360, 985-993.
10. Haldar, P.; Brightling, C. E.; Hargadon, B.; Gupta, S.; Monteiro, W.; Sousa, A.; Marshall, R. P.; Bradding, P.; Green, R. H.; Wardlaw, A. J.; et al. Mepolizumab and exacerbations of refractory eosinophilic asthma. N. Engl. J. Med. 2009, 360, 973-984.
11. Wenzel, S. E. Eosinophils in asthma-Closing the loop or opening the door? N. Engl. J. Med. 2009, 360, 1026-1028.
12. Lukawska, J. J.; Livieratos, L.; Sawyer, B. M.; Lee, T.; O'Doherty, M.; Blower, P. J.; Kofi, M.; Ballinger, J. R.; Corrigan, C. J.; Gnanasegaran, G.; et al. Real-time differential tracking of human neutrophil and eosinophil migration in vivo. J. Allergy Clin. Immunol. 2014, 133, 233-239.
13. Farahi, N.; Singh, N. R.; Heard, S.; Loutsios, C.; Summers, C.; Solanki, C. K.; Solanki, K.; Balan, K. K.; Ruparelia, P.; Peters, A. M.; et al. Use of 111-Indium-labeled autologous eosinophils to establish the in vivo kinetics of human eosinophils in healthy subjects. Blood 2012, 120, 4068-4070.
14. Walsh, G. Eosinophil apoptosis and clearance in asthma. J. Cell Death 2013, 6, 17-25.
15. Kankaanranta, H.; Moilanen, E.; Zhang, X. Pharmacological regulation of human eosinophil apoptosis. Curr. Drug Targets Inflamm. Allergy 2005, 4, 433-445.
16. Rothenberg, M. E.; Owen, W. F., Jr.; Silberstein, D. S.; Soberman, R. J.; Austen, K. F.; Stevens, R. L. Eosinophils cocultured with endothelial cells have increased survival and functional properties. Science 1987, 237, 645-647.
17. Kankaanranta, H.; Lindsay, M. A.; Giembycz, M. A.; Zhang, X.; Moilanen, E.; Barnes, P. J. Delayed eosinophil apoptosis in asthma. J. Allergy Clin. Immunol. 2000, 106, 77-83.
18. Simon, H. U.; Yousefi, S.; Schranz, C.; Schapowal, A.; Bachert, C.; Blaser, K. Direct demonstration of delayed eosinophil apoptosis as a mechanism causing tissue eosinophilia. J. Immunol. 1997, 158, 3902-3908.
19. Duffin, R.; Leitch, A. E.; Fox, S.; Haslett, C.; Rossi, A. G. Targeting granulocyte apoptosis: Mechanisms, models, and therapies. Immunol. Rev. 2010, 236, 28-40.
20. Galluzzi, L.; Vitale, I.; Abrams, J. M.; Alnemri, E. S.; Baehrecke, E. H.; Blagosklonny, M. V.; Dawson, T. M.; Dawson, V. L.; El-Deiry, W. S.; Fulda, S.; et al. Molecular definitions of cell death subroutines: Recommendations of the nomenclature committee on cell death 2012. Cell Death Differ. 2012, 19, 107-120.
21. Kroemer, G.; Galluzzi, L.; Brenner, C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87, 99-163.
22. 2+-dependent apoptosis and necrosis. Cell Calcium 2011, 50, 222-233.
23. Letuve, S.; Druilhe, A.; Grandsaigne, M.; Aubier, M.; Pretolani, M. Involvement of caspases and of mitochondria in Fas ligation-induced eosinophil apoptosis: Modulation by interleukin-5 and interferon-gamma. J. Leukoc. Biol. 2001, 70, 767-775.
24. Sharma, S. K.; Almeida, F. A.; Kierstein, S.; Hortobagyi, L.; Lin, T.; Larkin, A.; Peterson, J.; Yagita, H.; Zangrilli, J. G.; Haczku, A. Systemic FasL neutralization increases eosinophilic inflammation in a mouse model of asthma. Allergy 2012, 67, 328-335.
25. Beauvais, F.; Joly, F. Effects of nitric oxide on the eosinophil survival in vitro. A role for nitrosyl-heme. FEBS Lett. 1999, 443, 37-40.
26. Zhang, X.; Msc; Moilanen, E.; Lahti, A.; Hamalainen, M.; Giembycz, M. A.; Barnes, P. J.; Lindsay, M. A.; Kankaanranta, H. Regulation of eosinophil apoptosis by nitric oxide: Role of c-Jun-N-terminal kinase and signal transducer and activator of transcription 5. J. Allergy Clin. Immunol. 2003, 112, 93-101.
27. Hebestreit, H.; Dibbert, B.; Balatti, I.; Braun, D.; Schapowal, A.; Blaser, K.; Simon, H. U. Disruption of fas receptor signaling by nitric oxide in eosinophils. J. Exp. Med. 1998, 187, 415-425.
28. Oliveira, M. S.; de O Barreto, E.; Zamuner, S.; Pires, A. L.; Ferreira, T. P.; Cordeiro, R. S.; Lagente, V.; Martins, M. A.; Wallace, J. L.; e Silva, P. M. Suppressive effects of nitric oxide-releasing prednisolone NCX-1015 on the allergic pleural eosinophil recruitment in rats. Clin. Exp. Allergy 2008, 38, 1830-1837.
29. Feder, L. S.; Stelts, D.; Chapman, R. W.; Manfra, D.; Crawley, Y.; Jones, H.; Minnicozzi, M.; Fernandez, X.; Paster, T.; Egan, R. W.; et al. Role of nitric oxide on eosinophilic lung inflammation in allergic mice. Am. J. Respir. Cell Mol. Biol. 1997, 17, 436-442.
30. Lehtimaki, L.; Kankaanranta, H.; Saarelainen, S.; Hahtola, P.; Jarvenpaa, R.; Koivula, T.; Turjanmaa, V.; Moilanen, E. Extended exhaled NO measurement differentiates between alveolar and bronchial inflammation. Am. J. Respir. Crit. Care Med. 2001, 163, 1557-1561.
31. Zhang, X.; Moilanen, E.; Kankaanranta, H. Enhancement of human eosinophil apoptosis by fluticasone propionate, budesonide, and beclomethasone. Eur. J. Pharmacol. 2000, 406, 325-332.
32. Lamas, A. M.; Leon, O. G.; Schleimer, R. P. Glucocorticoids inhibit eosinophil responses to granulocyte-macrophage colony-stimulating factor. J. Immunol. 1991, 147, 254-259.
33. Wallen, N.; Kita, H.; Weiler, D.; Gleich, G. J. Glucocorticoids inhibit cytokine-mediated eosinophil survival. J. Immunol. 1991, 147, 3490-3495.
34. Lee, E.; Robertson, T.; Smith, J.; Kilfeather, S. Leukotriene receptor antagonists and synthesis inhibitors reverse survival in eosinophils of asthmatic individuals. Am. J. Respir. Crit. Care Med. 2000, 161, 1881-1886.
35. Yasui, K.; Hu, B.; Nakazawa, T.; Agematsu, K.; Komiyama, A. Theophylline accelerates human granulocyte apoptosis not via phosphodiesterase inhibition. J. Clin. Investig. 1997, 100, 1677-1684.
36. Ilmarinen, P.; Kankaanranta, H. Eosinophil apoptosis as a therapeutic target in allergic asthma. Basic Clin. Pharmacol. Toxicol. 2013, 114, 109-117.
37. Woolley, K. L.; Gibson, P. G.; Carty, K.; Wilson, A. J.; Twaddell, S. H.; Woolley, M. J. Eosinophil apoptosis and the resolution of airway inflammation in asthma. Am. J. Respir. Crit. Care Med. 1996, 154, 237-243.
38. Druilhe, A.; Wallaert, B.; Tsicopoulos, A.; Lapa e Silva, J. R.; Tillie-Leblond, I.; Tonnel, A. B.; Pretolani, M. Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am. J. Respir. Cell Mol. Biol. 1998, 19, 747-757.
39. Vignola, A. M.; Chanez, P.; Chiappara, G.; Siena, L.; Merendino, A.; Reina, C.; Gagliardo, R.; Profita, M.; Bousquet, J.; Bonsignore, G. Evaluation of apoptosis of eosinophils, macrophages, and T lymphocytes in mucosal biopsy specimens of patients with asthma and chronic bronchitis. J. Allergy Clin. Immunol. 1999, 103, 563-573.
40. Duncan, C. J.; Lawrie, A.; Blaylock, M. G.; Douglas, J. G.; Walsh, G. M. Reduced eosinophil apoptosis in induced sputum correlates with asthma severity. Eur. Respir. J. 2003, 22, 484-490.
41. Montuschi, P.; Peters-Golden, M. L. Leukotriene modifiers for asthma treatment. Clin. Exp. Allergy 2010, 40, 1732-1741.
42. Lim, S.; Tomita, K.; Caramori, G.; Jatakanon, A.; Oliver, B.; Keller, A.; Adcock, I.; Chung, K. F.; Barnes, P. J. Low-dose theophylline reduces eosinophilic inflammation but not exhaled nitric oxide in mild asthma. Am. J. Respir. Crit. Care Med. 2001, 164, 273-276.
43. Jetzek-Zader, M.; Gudowius, S.; Feyen, O.; Stevens, M.; Lipfert, P.; Niehues, T. A single intravenous dose of prednisolone induces phosphatidylserine externalization, loss of surface marker expression and a 24-h net increase in human peripheral blood lymphocytes ex vivo. Rheumatol. Int. 2007, 27, 667-673.
44. Wiegers, G. J.; Knoflach, M.; Bock, G.; Niederegger, H.; Dietrich, H.; Falus, A.; Boyd, R.; Wick, G. CD4(+)CD8(+)TCR(low) thymocytes express low levels of glucocorticoid receptors while being sensitive to glucocorticoid-induced apoptosis. Eur. J. Immunol. 2001, 31, 2293-2301.
45. Leussink, V. I.; Jung, S.; Merschdorf, U.; Toyka, K. V.; Gold, R. High-dose methylprednisolone therapy in multiple sclerosis induces apoptosis in peripheral blood leukocytes. Arch. Neurol. 2001, 58, 91-97.
46. Meagher, L. C.; Cousin, J. M.; Seckl, J. R.; Haslett, C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J. Immunol. 1996, 156, 4422-4428.
47. Zhang, X.; Moilanen, E.; Kankaanranta, H. Beclomethasone, budesonide and fluticasone propionate inhibit human neutrophil apoptosis. Eur. J. Pharmacol. 2001, 431, 365-371.
48. Zhang, X.; Moilanen, E.; Adcock, I. M.; Lindsay, M. A.; Kankaanranta, H. Divergent effect of mometasone on human eosinophil and neutrophil apoptosis. Life Sci. 2002, 71, 1523-1534.
49. Marwick, J. A.; Dorward, D. A.; Lucas, C. D.; Jones, K. O.; Sheldrake, T. A.; Fox, S.; Ward, C.; Murray, J.; Brittan, M.; Hirani, N.; et al. Oxygen levels determine the ability of glucocorticoids to influence neutrophil survival in inflammatory environments. J. Leukoc. Biol. 2013, 94, 1285-1292.
50. Peachman, K. K.; Lyles, D. S.; Bass, D. A. Mitochondria in eosinophils: Functional role in apoptosis but not respiration. Proc. Natl. Acad. Sci. USA 2001, 98, 1717-1722.
51. Dewson, G.; Cohen, G. M.; Wardlaw, A. J. Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 2001, 98, 2239-2247.
52. Gardai, S. J.; Hoontrakoon, R.; Goddard, C. D.; Day, B. J.; Chang, L. Y.; Henson, P. M.; Bratton, D. L. Oxidant-mediated mitochondrial injury in eosinophil apoptosis: Enhancement by glucocorticoids and inhibition by granulocyte-macrophage colony-stimulating factor. J. Immunol. 2003, 170, 556-566.
53. Segal, M.; Niazi, S.; Simons, M. P.; Galati, S. A.; Zangrilli, J. G. Bid activation during induction of extrinsic and intrinsic apoptosis in eosinophils. Immunol. Cell Biol. 2007, 85, 518-524.
54. Maret, M.; Ruffie, C.; Letuve, S.; Phelep, A.; Thibaudeau, O.; Marchal, J.; Pretolani, M.; Druilhe, A. A role for Bid in eosinophil apoptosis and in allergic airway reaction. J. Immunol. 2009, 182, 5740-5747.
55. Lee, Y. A.; Shin, M. H. Mitochondrial respiration is required for activation of ERK1/2 and caspase-3 in human eosinophils stimulated with hydrogen peroxide. J. Investig. Allergol. Clin. Immunol. 2009, 19, 188-194.
56. Van Der Vliet, H. J.; Wever, P. C.; van Diepen, F. N.; Yong, S. L.; Ten Berge, I. J. Quantification of Bax/Bcl-2 ratios in peripheral blood lymphocytes, monocytes and granulocytes and their relation to susceptibility to anti-Fas (anti-CD95)-induced apoptosis. Clin. Exp. Immunol. 1997, 110, 324-328.
57. Druilhe, A.; Arock, M.; le Goff, L.; Pretolani, M. Human eosinophils express bcl-2 family proteins: Modulation of Mcl-1 expression by IFN-gamma. Am. J. Respir. Cell Mol. Biol. 1998, 18, 315-322.
58. Shen, Z. J.; Esnault, S.; Schinzel, A.; Borner, C.; Malter, J. S. The peptidyl-prolyl isomerase Pin1 facilitates cytokine-induced survival of eosinophils by suppressing Bax activation. Nat. Immunol. 2009, 10, 257-265.
59. Oh, J.; Malter, J. S. Pin1-FADD interactions regulate Fas-mediated apoptosis in activated eosinophils. J. Immunol. 2013, 190, 4937-4945.
60. Zangrilli, J.; Robertson, N.; Shetty, A.; Wu, J.; Hastie, A.; Fish, J. E.; Litwack, G.; Peters, S. P. Effect of IL-5, glucocorticoid, and Fas ligation on Bcl-2 homologue expression and caspase activation in circulating human eosinophils. Clin. Exp. Immunol. 2000, 120, 12-21.
61. Duffin, R.; Leitch, A. E.; Sheldrake, T. A.; Hallett, J. M.; Meyer, C.; Fox, S.; Alessandri, A. L.; Martin, M. C.; Brady, H. J.; Teixeira, M. M.; et al. The CDK inhibitor, R-roscovitine, promotes eosinophil apoptosis by down-regulation of Mcl-1. FEBS Lett. 2009, 583, 2540-2546.
62. Farahi, N.; Uller, L.; Juss, J. K.; Langton, A. J.; Cowburn, A. S.; Gibson, A.; Foster, M. R.; Farrow, S. N.; Marco-Casanova, P.; Sobolewski, A.; et al. Effects of the cyclin-dependent kinase inhibitor R-roscovitine on eosinophil survival and clearance. Clin. Exp. Allergy 2011, 41, 673-687.
63. Sivertson, K. L.; Seeds, M. C.; Long, D. L.; Peachman, K. K.; Bass, D. A. The differential effect of dexamethasone on granulocyte apoptosis involves stabilization of Mcl-1L in neutrophils but not in eosinophils. Cell. Immunol. 2007, 246, 34-45.
64. Germain, M.; Milburn, J.; Duronio, V. MCL-1 inhibits BAX in the absence of MCL-1/BAX interaction. J. Biol. Chem. 2008, 283, 6384-6392.
65. Saffar, A. S.; Dragon, S.; Ezzati, P.; Shan, L.; Gounni, A. S. Phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase regulate induction of Mcl-1 and survival in glucocorticoid-treated human neutrophils. J. Allergy Clin. Immunol. 2008, 121, 492-498.
66. Dewson, G.; Walsh, G. M.; Wardlaw, A. J. Expression of Bcl-2 and its homologues in human eosinophils. Modulation by interleukin-5. Am. J. Respir. Cell Mol. Biol. 1999, 20, 720-728.
67. Kaasik, A.; Safiulina, D.; Zharkovsky, A.; Veksler, V. Regulation of mitochondrial matrix volume. Am. J. Physiol. Cell Physiol. 2007, 292, C157-C163.
68. Ilmarinen-Salo, P.; Moilanen, E.; Kinnula, V. L.; Kankaanranta, H. Nitric oxide-induced eosinophil apoptosis is dependent on mitochondrial permeability transition (mPT), JNK and oxidative stress: Apoptosis is preceded but not mediated by early mPT-dependent JNK activation. Respir. Res. 2012, 13, doi: 10. 1186/1465-9921-13-73.
69. Letuve, S.; Druilhe, A.; Grandsaigne, M.; Aubier, M.; Pretolani, M. Critical role of mitochondria, but not caspases, during glucocorticosteroid-induced human eosinophil apoptosis. Am. J. Respir. Cell Mol. Biol. 2002, 26, 565-571.
70. Garcia-Perez, C.; Roy, S. S.; Naghdi, S.; Lin, X.; Davies, E.; Hajnoczky, G. Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling. Proc. Natl. Acad. Sci. USA 2012, 109, 4497-4502.
71. Petronilli, V.; Penzo, D.; Scorrano, L.; Bernardi, P.; di Lisa, F. The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J. Biol. Chem. 2001, 276, 12030-12034.
72. Ichas, F.; Jouaville, L. S.; Mazat, J. P. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 1997, 89, 1145-1153.
73. Bernardi, P.; Petronilli, V. The permeability transition pore as a mitochondrial calcium release channel: A critical appraisal. J. Bioenerg. Biomembr. 1996, 28, 131-138.
74. 2+ responses to physiological stimuli in adult neurons. Eur. J. Neurosci. 2011, 33, 831-842.
75. 2+ release channel: New answers to an old question. Cell Calcium 2012, 52, 22-27.
76. Zorov, D. B.; Juhaszova, M.; Sollott, S. J. Mitochondrial ROS-induced ROS release: An update and review. Biochim. Biophys. Acta 2006, 1757, 509-517.
77. Ma, Q.; Fang, H.; Shang, W.; Liu, L.; Xu, Z.; Ye, T.; Wang, X.; Zheng, M.; Chen, Q.; Cheng, H. Superoxide flashes: Early mitochondrial signals for oxidative stress-induced apoptosis. J. Biol. Chem. 2011, 286, 27573-27581.
78. Wedi, B.; Straede, J.; Wieland, B.; Kapp, A. 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 1999, 94, 2365-2373.
79. Martinez-Losa, M.; Cortijo, J.; Juan, G.; Ramon M.; Sanz M. J.; Morcillo E. J. Modulatory effects of N-acetyl-L-cysteine on human eosinophil apoptosis. Eur. Respir. J. 2007, 30, 436-442.
80. Nissim Ben Efraim, A. H.; Eliashar, R.; Levi-Schaffer, F. Hypoxia modulates human eosinophil function. Clin. Mol. Allergy 2010, 8, doi: 10. 1186/1476-7961-8-10.
81. Kano, G.; Almanan, M.; Bochner, B. S.; Zimmermann, N. Mechanism of siglec-8-mediated cell death in IL-5-activated eosinophils: Role for reactive oxygen species-enhanced MEK/ERK activation. J. Allergy Clin. Immunol. 2013, 132, 437-445.
82. Orrenius, S.; Gogvadze, V.; Zhivotovsky, B. Mitochondrial oxidative stress: Implications for cell death. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 143-183.
83. Cadenas, E.; Davies, K. J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 2000, 29, 222-230.
84. Gough, D. R.; Cotter, T. G. Hydrogen peroxide: A Jekyll and Hyde signalling molecule. Cell Death Dis. 2011, 2, e213.
85. Kankaanranta, H.; Giembycz, M. A.; Barnes, P. J.; Haddad, El.-B.; Saarelainen, S.; Zhang, X.; Moilanen, E.; Lindsay, M. A. Hydrogen peroxide reverses IL-5 afforded eosinophil survival and promotes constitutive human eosinophil apoptosis. Int. Arch. Allergy Immunol. 2002, 127, 73-78.
86. Serradell, M. C.; Guasconi, L.; Masih, D. T. Involvement of a mitochondrial pathway and key role of hydrogen peroxide during eosinophil apoptosis induced by excretory-secretory products from Fasciola hepatica. Mol. Biochem. Parasitol. 2009, 163, 95-106.
87. Tonomura, N.; McLaughlin, K.; Grimm, L.; Goldsby, R. A.; Osborne, B. A. Glucocorticoid-induced apoptosis of thymocytes: requirement of proteasome-dependent mitochondrial activity. J. Immunol. 2003, 170, 2469-2478.
88. Tome, M. E.; Baker, A. F.; Powis, G.; Payne, C. M.; Briehl, M. M. Catalase-overexpressing thymocytes are resistant to glucocorticoid-induced apoptosis and exhibit increased net tumor growth. Cancer Res. 2001, 61, 2766-2773.
89. Andreyev, A. Y.; Kushnareva, Y. E.; Starkov, A. A. Mitochondrial metabolism of reactive oxygen species. Biochemistry 2005, 70, 200-214.
90. Simon, N.; Jolliet, P.; Morin, C.; Zini, R.; Urien, S.; Tillement, J. P. Glucocorticoids decrease cytochrome c oxidase activity of isolated rat kidney mitochondria. FEBS Lett. 1998, 435, 25-28.
91. Morin, C.; Zini, R.; Simon, N.; Charbonnier, P.; Tillement, J. P.; le Louet, H. Low glucocorticoid concentrations decrease oxidative phosphorylation of isolated rat brain mitochondria: An additional effect of dexamethasone. Fundam. Clin. Pharmacol. 2000, 14, 493-500.
92. Mutsaers, H. A.; Tofighi, R. Dexamethasone enhances oxidative stress-induced cell death in murine neural stem cells. Neurotox. Res. 2012, 22, 127-137.
93. Korhonen, R.; Moilanen, E. MAP kinase phosphatase-1 as an inflammatory factor and drug target. Basic Clin. Pharmacol. Toxicol. 2014, 114, 24-36.
94. Raman, M.; Chen, W.; Cobb, M. H. Differential regulation and properties of MAPKs. Oncogene 2007, 26, 3100-3112.
95. Wancket, L. M.; Frazier, W. J.; Liu, Y. Mitogen-activated protein kinase phosphatase (MKP)-1 in immunology, physiology, and disease. Life Sci. 2012, 90, 237-248.
96. Yin, H.; Shi, Z.; Jiao, S.; Chen, C.; Wang, W.; Greene, M. I.; Zhou, Z. Germinal center kinases in immune regulation. Cell. Mol. Immunol. 2012, 9, 439-445.
97. McCubrey, J. A.; Lahair, M. M.; Franklin, R. A. Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid. Redox Signal. 2006, 8, 1775-1789.
98. Hasala, H.; Zhang, X.; Saarelainen, S.; Moilanen, E.; Kankaanranta, H. c-Jun N-terminal kinase mediates constitutive human eosinophil apoptosis. Pulm. Pharmacol. Ther. 2007, 20, 580-587.
99. Kankaanranta, H.; Zhang, X.; Tumelius, R.; Ruotsalainen, M.; Haikala, H.; Nissinen, E.; Moilanen, E. Antieosinophilic activity of simendans. J. Pharmacol. Exp. Ther. 2007, 323, 31-38.
100. Hasala, H.; Moilanen, E.; Janka-Junttila, M.; Giembycz, M. A.; Kankaanranta, H. First-generation antihistamines diphenhydramine and chlorpheniramine reverse cytokine-afforded eosinophil survival by enhancing apoptosis. Allergy Asthma Proc. 2007, 28, 79-86.
101. Kankaanranta, H.; Ilmarinen, P.; Zhang, X.; Nissinen, E.; Moilanen, E. Antieosinophilic activity of orazipone. Mol. Pharmacol. 2006, 69, 1861-1870.
102. Shrivastava, P.; Pantano, C.; Watkin, R.; McElhinney, B.; Guala, A.; Poynter, M. L.; Persinger, R. L.; Budd, R.; Janssen-Heininger, Y. Reactive nitrogen species-induced cell death requires Fas-dependent activation of c-Jun N-terminal kinase. Mol. Cell. Biol. 2004, 24, 6763-6772.
103. Sanchez-Perez, I.; Murguia, J. R.; Perona, R. Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene 1998, 16, 533-540.
104. Ventura, J. J.; Hubner, A.; Zhang, C.; Flavell, R. A.; Shokat, K. M.; Davis, R. J. Chemical genetic analysis of the time course of signal transduction by JNK. Mol. Cell 2006, 21, 701-710.
105. Lamb, J. A.; Ventura, J. J.; Hess, P.; Flavell, R. A.; Davis, R. J. JunD mediates survival signaling by the JNK signal transduction pathway. Mol. Cell 2003, 11, 1479-1489.
106. Kamata, H.; Honda, S.; Maeda, S.; Chang, L.; Hirata, H.; Karin, M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005, 120, 649-661.
107. Miike, S.; Nakao, A.; Hiraguri, M.; Kurasawa, K.; Saito, Y.; Iwamoto, I. Involvement of JAK2, but not PI 3-kinase/Akt and MAP kinase pathways, in anti-apoptotic signals of GM-CSF in human eosinophils. J. Leukoc. Biol. 1999, 65, 700-706.
108. Kankaanranta, H.; de Souza, P. M.; Barnes, P. J.; Salmon, M.; Giembycz, M. A.; Lindsay, M. A. SB 203580, an inhibitor of p38 mitogen-activated protein kinase, enhances constitutive apoptosis of cytokine-deprived human eosinophils. J. Pharmacol. Exp. Ther. 1999, 290, 621-628.
109. 2-terminal kinase and p38 mitogen-activated protein kinase in human eosinophils. Clin. Exp. Immunol. 2000, 122, 20-27.
110. Baruch-Morgenstern, N. B.; Shik, D.; Moshkovits, I.; Itan, M.; Karo-Atar, D.; Bouffi, C.; Fulkerson, P. C.; Rashkovan, D.; Jung, S.; Rothenberg, M. E.; Munitz, A. Paired immunoglobulin-like receptor A is an intrinsic, self-limiting suppressor of IL-5-induced eosinophil development. Nat. Immunol. 2013, 15, doi: 10. 1038/ni. 2757.
111. Matsumoto, K.; Terakawa, M.; Miura, K.; Fukuda, S.; Nakajima, T.; Saito, H. Extremely rapid and intense induction of apoptosis in human eosinophils by anti-CD30 antibody treatment in vitro. J. Immunol. 2004, 172, 2186-2193.
112. Tsukahara, K.; Nakao, A.; Hiraguri, M.; Miike, S.; Mamura, M.; Saito, Y.; Iwamoto, I. Tumor necrosis factor-alpha mediates antiapoptotic signals partially via p38 MAP kinase activation in human eosinophils. Int. Arch. Allergy Immunol. 1999, 120, 54-59.
113. Wong, C. K.; Hu, S.; Cheung, P. F.; Lam, C. W. Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: Implications in allergic inflammation. Am. J. Respir. Cell Mol. Biol. 2010, 43, 305-315.
114. De Souza, P. M.; Kankaanranta, H.; Michael, A.; Barnes, P. J.; Giembycz, M. A.; Lindsay, M. A. Caspase-catalyzed cleavage and activation of Mst1 correlates with eosinophil but not neutrophil apoptosis. Blood 2002, 99, 3432-3438.
115. Ura, S.; Nishina, H.; Gotoh, Y.; Katada, T. Activation of the c-Jun N-terminal kinase pathway by MST1 is essential and sufficient for the induction of chromatin condensation during apoptosis. Mol. Cell. Biol. 2007, 27, 5514-5522.