Study on the Critical Roles of Apoptosis in Asthma Disease
Abstract
Inflammation, and remodeling in airways are the two crucial characteristics of asthma, a common respiratory disease. In asthma pathophysiology, the recruitment of granulocytes finally results in inflammation, leading to lung damage. In this regard, failure to clear inflammatory cells by programmed cell death, apoptosis will cause the prolongation of inflammation. On the other hand, in airway epithelial cells, apoptosis may occur, resulting in airway remodeling. Hence, dysregulation of apoptosis has been suggested to contribute to the development of asthma. Importantly, knowledge of the factors related to apoptotic cascade seems vital to explore various pharmacological interventions for the treatment of asthma. In this review, we highlight several important apoptotic and anti-apoptotic factors contributing either to inflammatory cells or airway epithelial cells involved in asthma pathogenesis.
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2. Ashe PC, Berry MD. Apoptotic signaling cascades. Prog Neuropsychopharmacol Biol Psychiatry 2003;27:199-214.
3. Sloviter RS. Apoptosis: a guide for the perplexed. Trends Pharmacol Sci 2002;23:19-24.
4. Ilmarinen P, Moilanen E, Kankaanranta H. Mitochondria in the center of human eosinophil apoptosis and survival. Int J Mol Sci 2014;15:3952-69.
5. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012;19:107-20.
6. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007;87:99-163.
7. Rossi AG, Hallett JM, Sawatzky DA, Teixeira MM, Haslett C. Modulation of granulocyte apoptosis can influence the resolution of inflammation. Biochem Soc Trans 2007;35:288-91.
8. Kianian F, Sadeghipour HR, Karimian SM, M Kadkhodaee, Seifi B. Protective effects of hydrogen sulfide on anxiety in ovalbumin-induced chronic asthma. Physiol Pharmacol 2019;23:208-14.
9. Kianian F, Karimian SM, Kadkhodaee M, Takzaree N, Seifi B, Adeli S, et al. Combination of ascorbic acid and calcitriol attenuates chronic asthma disease by reductions in oxidative stress and inflammation. Respir Physiol Neurobiol 2019;270:103265.
10. Kianian F, Karimian SM, Kadkhodaee M, Takzaree N, Seifi B, Sadeghipour HR. Protective effects of ascorbic acid and calcitriol combination on airway remodelling in ovalbumin-induced chronic asthma. Pharm Biol 2020;58:107-15.
11. Chin AC, Parkos CA. Pathobiology of neutrophil transepithelial migration: implications in mediating epithelial injury. Annu Rev Pathol 2007;2:111-43.
12. Vignola AM, Chanez P, Chiappara G, Siena L, Merendino A, Reina, et al. 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;103:563-73.
13. El‐Gamal Y, Heshmat N, Mahran M, El-Gabbas Z. Expression of the apoptosis inhibitor Bcl‐2 in sputum eosinophils from children with acute asthma. Clin Exp Allergy 2004;34:1701-6.
14. Kianian F, Kadkhodaee M, Sadeghipour HR, Karimian SM, Seifi B. An overview of high-mobility group box 1, a potent pro-inflammatory cytokine in asthma. J Basic Cl Physiol Pharmacol 2020;31.
15. Kianian F, Seifi B, Kadkhodaee M, Sadeghipour HR, Ranjbaran M. Nephroprotection through modifying the apoptotic tnf-α/erk1/2/bax signaling pathway and oxidative stress by long-term sodium hydrosulfide administration in ovalbumin-induced chronic asthma. Immunol Invest 2020;1-7.
16. Kirsch T, Woywodt A, Beese M, Wyss K, Park JK, Erdbruegger U, et al. Engulfment of apoptotic cells by microvascular endothelial cells induce proinflammatory responses. Blood 2007;109:2854-62.
17. Juncadella IJ, Kadl A, Sharma AK, Shim YM, Hochreiter-Hufford A, Borish L, et al. Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 2013;493:547-51.
18. Walsh GM, Sexton DW, Blaylock MG, Convery CM. Resting and cytokine-stimulated human small airway epithelial cells recognize and engulf apoptotic eosinophils. Blood 1999;94:2827-35.
19. Grossmann J. Molecular mechanisms of "detachment-induced apoptosis-Anoikis". Apoptosis 2002;7:247-60.
20. Montefort S, Roche WR, Holgate ST. Bronchial epithelial shedding in asthmatics and non-asthmatics. Respir Med 1993;87:9-11.
21. Liu Y, Pu Y, Li D, Zhou L, Wan L. Azithromycin ameliorates airway remodeling via inhibiting airway epithelium apoptosis. Life Sci 2017;170:1-8.
22. Moulding DA, Akgul C, Derouet M, White MR, Edwards SW. BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J Leukoc Biol 2001;70:783-92.
23. Dewson G, Cohen GM, Wardlaw AJ. Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 2001;98:2239-47.
24. Edwards SW, Derouet M, Howse M, Moots RJ. Regulation of neutrophil apoptosis by Mcl-1. Biochem Soc Trans 2004;32:489-92.
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26. Cho IH, Gong JH, Kang MK, Lee EJ, Park JH, Park SJ, et al. Astragalin inhibits airway eotaxin-1 induction and epithelial apoptosis through modulating oxidative stress-responsive MAPK signaling. BMC Pulm Med 2014;14:122.
27. Rehman R, Bhat YA, Panda L, Mabalirajan U. TRPV1 inhibition attenuates IL-13 mediated asthma features in mice by reducing airway epithelial injury. Int Immunopharmacol 2013;15:597-605.
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29. Druilhe A, Wallaert B, Tsicopoulos A, Lepa e Silva JR, Tilie-Leblond I, Tonnel AB, et al. Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am J Respir Cell Mol Biol 1998;19:747-57.
30. Jayaraman S, Castro M, O'Sullivan M, Bragdon MJ, Holtzman MJ. Resistance to Fasmediated T cell apoptosis in asthma. J Immunol 1999;162:1717-22.
31. Holtzman MJ, Look DC, Sampath D, Castro M, Koga T, Walter MJ. Control of epithelial immune-response genes and implications for airway immunity and inflammation. Proc Assoc Am Physicians 1998;110:1-11.
32. Kuwano K, Yoshimi M, Maeyama T, Hamada N, Yamada M, Nakanishi Y. Apoptosis signaling pathways in lung diseases. Med Chem 2005;1:49-56.
33. Gilroy DW, Lawrence T, Perretti M, Rossi AG. Inflammatory resolution: new opportunities for drug discovery. Nat Rev Drug Discov 2004;3:401.
34. Dalton DK, Haynes L, Chu CQ, Swain SL, Wittmer S. Interferon γ eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med 2000;192:117-22.
35. Novelli F, Di Pierro F, Francia di Celle P, Bertini S, Affaticati P, Garotta G, et al. Environmental signals influencing expression of the IFN-gamma receptor on human T cells control whether IFN-gamma promotes proliferation or apoptosis. J Immunol 1994;152:496-504.
36. Tesfaigzi Y, Fischer MJ, Daheshia M, Green FH, De Sanctis GT, Wilder JA. Bax is crucial for IFNg-induced resolution of allergen-induced mucous cell metaplasia. J Immunol 2002;169:5919-25.
37. De Rose V, Cappello P, Sorbello V, Ceccarini B, Gani F, Bosticardo M, et al. IFN‐γ inhibits the proliferation of allergen‐activated T lymphocytes from atopic, asthmatic patients by inducing Fas/FasL‐mediated apoptosis. J Leukoc Biol 2004;76:423-32.
38. Nakao F, Ihara K, Kusuhara K, Sasaki Y, Kinukawa N, Takabayashi A, et al. Association of IFN-γ and IFN regulatory factor 1 polymorphisms with childhood atopic asthma. J Allergy Clin Immunol Pract 2001;107:499-504.
39. Kumar S, Boehm J, Lee JC. p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov 2003;2:717-26.
40. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001;22:153-83.
41. Suzuki K, Hino M, Hato F, Tatsumi N, Kitagawa S. Cytokine-Specific Activation of Distinct Mitogen-Activated Protein Kinase Subtype Cascades in Human Neutrophils Stimulated by Granulocyte Colony-Stimulating Factor, Granulocyte-Macrophage Colony-Stimulating Factor, and Tumor Necrosis Factor-α. Blood 1999;93:341-9.
42. Alvarado-Kristensson M, Melander F, Leandersson K, Rönnstrand L, Wernstedt C, Andersson T. p38-MAPK signals survival by phosphorylation of caspase-8 and caspase-3 in human neutrophils. J Exp Med 2004;199:449-58.
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44. Hawkins PT, Anderson KE, Davidson K, Stephens LR. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 2006;34:647-62.
45. Szefler SJ. Airway remodeling: therapeutic target or not? Am J Respir Crit Care Med 2005;171:672-3.
46. Feder LS, Stelts D, Chapman RW, Manfra D, Crawley Y, Jones H, et al. Role of nitric oxide on eosinophilic lung inflammation in allergic mice. Am J Respir Cell Mol Biol 1997;17:436-42.
47. Castellano I, Ercolesi E, Palumbo A. Nitric oxide affects ERK signaling through downregulation of MAP kinase phosphatase levels during larval development of the ascidian Ciona intestinalis. PLoS One 2014;9:e102907.
48. Cowburn AS, Deighton J, Walmsley SR, Chilvers ER. The survival effect of TNF‐α in human neutrophils is mediated via NF‐κB‐dependent IL‐8 release. Eur J Immunol 2004;34:1733-43.
49. Mirza AZ, Althagafi II, Shamshad H. Role of PPAR receptor in different diseases and their ligands: Physiological importance and clinical implications. Eur J Med Chem 2019;166:502-13.
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51. Nutku E, Aizawa H, Hudson SA, Bochner BS. Ligation of Siglec-8: a selective mechanism for induction of human eosinophil apoptosis. Blood 2003;101:5014-20.
52. Bochner BS. Siglec‐8 on human eosinophils and mast cells, and Siglec‐F on murine eosinophils, are functionally related inhibitory receptors. Clin Exp Allergy 2009;39:317-24.
53. Kiwamoto T, Katoh T, Tiemeyer M, Bochner BS. The Role of lung epithelial ligands for Siglec-8 and Siglec-F in eosinophilic inflammation. Curr Opin Allergy Clin Immunol 2013;13:106-11.
54. Nutku E, Hudson SA, Bochner BS. Mechanism of Siglec-8-induced human eosinophil apoptosis: Role of caspases and mitochondrial injury. Biochem Biophys Res Commun 2005;336:918-24.
55. Mohammadian M, Sadeghipour HR, Jahromi GP, Jafari M, Nejad AK, Khamse S, et al. Simvastatin and bone marrow-derived mesenchymal stem cells (BMSCs) affects serum IgE and lung cytokines levels in sensitized mice. Cytokine 2019;113:83-8.
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57. James AJ, Penrose JF, Cazaly AM, Holgate ST, Sampson AP. Human bronchial fibroblasts express the 5-lipoxygenase pathway. Respir Res 2006;7:102.
58. Kiwamoto T, Ishii Y, Morishima Y, Yoh K, Maeda A, Ishizaki K, et al. Transcription factors T-bet and GATA-3 regulate development of airway remodeling. Am J Respir Crit Care Med 2006;174:142-51.
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2. Ashe PC, Berry MD. Apoptotic signaling cascades. Prog Neuropsychopharmacol Biol Psychiatry 2003;27:199-214.
3. Sloviter RS. Apoptosis: a guide for the perplexed. Trends Pharmacol Sci 2002;23:19-24.
4. Ilmarinen P, Moilanen E, Kankaanranta H. Mitochondria in the center of human eosinophil apoptosis and survival. Int J Mol Sci 2014;15:3952-69.
5. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012;19:107-20.
6. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007;87:99-163.
7. Rossi AG, Hallett JM, Sawatzky DA, Teixeira MM, Haslett C. Modulation of granulocyte apoptosis can influence the resolution of inflammation. Biochem Soc Trans 2007;35:288-91.
8. Kianian F, Sadeghipour HR, Karimian SM, M Kadkhodaee, Seifi B. Protective effects of hydrogen sulfide on anxiety in ovalbumin-induced chronic asthma. Physiol Pharmacol 2019;23:208-14.
9. Kianian F, Karimian SM, Kadkhodaee M, Takzaree N, Seifi B, Adeli S, et al. Combination of ascorbic acid and calcitriol attenuates chronic asthma disease by reductions in oxidative stress and inflammation. Respir Physiol Neurobiol 2019;270:103265.
10. Kianian F, Karimian SM, Kadkhodaee M, Takzaree N, Seifi B, Sadeghipour HR. Protective effects of ascorbic acid and calcitriol combination on airway remodelling in ovalbumin-induced chronic asthma. Pharm Biol 2020;58:107-15.
11. Chin AC, Parkos CA. Pathobiology of neutrophil transepithelial migration: implications in mediating epithelial injury. Annu Rev Pathol 2007;2:111-43.
12. Vignola AM, Chanez P, Chiappara G, Siena L, Merendino A, Reina, et al. 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;103:563-73.
13. El‐Gamal Y, Heshmat N, Mahran M, El-Gabbas Z. Expression of the apoptosis inhibitor Bcl‐2 in sputum eosinophils from children with acute asthma. Clin Exp Allergy 2004;34:1701-6.
14. Kianian F, Kadkhodaee M, Sadeghipour HR, Karimian SM, Seifi B. An overview of high-mobility group box 1, a potent pro-inflammatory cytokine in asthma. J Basic Cl Physiol Pharmacol 2020;31.
15. Kianian F, Seifi B, Kadkhodaee M, Sadeghipour HR, Ranjbaran M. Nephroprotection through modifying the apoptotic tnf-α/erk1/2/bax signaling pathway and oxidative stress by long-term sodium hydrosulfide administration in ovalbumin-induced chronic asthma. Immunol Invest 2020;1-7.
16. Kirsch T, Woywodt A, Beese M, Wyss K, Park JK, Erdbruegger U, et al. Engulfment of apoptotic cells by microvascular endothelial cells induce proinflammatory responses. Blood 2007;109:2854-62.
17. Juncadella IJ, Kadl A, Sharma AK, Shim YM, Hochreiter-Hufford A, Borish L, et al. Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 2013;493:547-51.
18. Walsh GM, Sexton DW, Blaylock MG, Convery CM. Resting and cytokine-stimulated human small airway epithelial cells recognize and engulf apoptotic eosinophils. Blood 1999;94:2827-35.
19. Grossmann J. Molecular mechanisms of "detachment-induced apoptosis-Anoikis". Apoptosis 2002;7:247-60.
20. Montefort S, Roche WR, Holgate ST. Bronchial epithelial shedding in asthmatics and non-asthmatics. Respir Med 1993;87:9-11.
21. Liu Y, Pu Y, Li D, Zhou L, Wan L. Azithromycin ameliorates airway remodeling via inhibiting airway epithelium apoptosis. Life Sci 2017;170:1-8.
22. Moulding DA, Akgul C, Derouet M, White MR, Edwards SW. BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J Leukoc Biol 2001;70:783-92.
23. Dewson G, Cohen GM, Wardlaw AJ. Interleukin-5 inhibits translocation of Bax to the mitochondria, cytochrome c release, and activation of caspases in human eosinophils. Blood 2001;98:2239-47.
24. Edwards SW, Derouet M, Howse M, Moots RJ. Regulation of neutrophil apoptosis by Mcl-1. Biochem Soc Trans 2004;32:489-92.
25. Bianchi SM, Dockrell DH, Renshaw SA, Sabroe I, Whyte MK. Granulocyte apoptosis in the pathogenesis and resolution of lung disease. Clin Sci (Lond) 2006;110:293-304.
26. Cho IH, Gong JH, Kang MK, Lee EJ, Park JH, Park SJ, et al. Astragalin inhibits airway eotaxin-1 induction and epithelial apoptosis through modulating oxidative stress-responsive MAPK signaling. BMC Pulm Med 2014;14:122.
27. Rehman R, Bhat YA, Panda L, Mabalirajan U. TRPV1 inhibition attenuates IL-13 mediated asthma features in mice by reducing airway epithelial injury. Int Immunopharmacol 2013;15:597-605.
28. Mineev VN, Nesterovich II, Trofimov VI, Kashintseva TV, Rybakova MG, Grozov RV. Evaluating the activity of the apoptosis-regulating genes from Bcl-2, Bax expression, and caspase-3 activity in bronchial epithelial cells in patients with asthma. Arkh Patol 2011;73:11-4.
29. Druilhe A, Wallaert B, Tsicopoulos A, Lepa e Silva JR, Tilie-Leblond I, Tonnel AB, et al. Apoptosis, proliferation, and expression of Bcl-2, Fas, and Fas ligand in bronchial biopsies from asthmatics. Am J Respir Cell Mol Biol 1998;19:747-57.
30. Jayaraman S, Castro M, O'Sullivan M, Bragdon MJ, Holtzman MJ. Resistance to Fasmediated T cell apoptosis in asthma. J Immunol 1999;162:1717-22.
31. Holtzman MJ, Look DC, Sampath D, Castro M, Koga T, Walter MJ. Control of epithelial immune-response genes and implications for airway immunity and inflammation. Proc Assoc Am Physicians 1998;110:1-11.
32. Kuwano K, Yoshimi M, Maeyama T, Hamada N, Yamada M, Nakanishi Y. Apoptosis signaling pathways in lung diseases. Med Chem 2005;1:49-56.
33. Gilroy DW, Lawrence T, Perretti M, Rossi AG. Inflammatory resolution: new opportunities for drug discovery. Nat Rev Drug Discov 2004;3:401.
34. Dalton DK, Haynes L, Chu CQ, Swain SL, Wittmer S. Interferon γ eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med 2000;192:117-22.
35. Novelli F, Di Pierro F, Francia di Celle P, Bertini S, Affaticati P, Garotta G, et al. Environmental signals influencing expression of the IFN-gamma receptor on human T cells control whether IFN-gamma promotes proliferation or apoptosis. J Immunol 1994;152:496-504.
36. Tesfaigzi Y, Fischer MJ, Daheshia M, Green FH, De Sanctis GT, Wilder JA. Bax is crucial for IFNg-induced resolution of allergen-induced mucous cell metaplasia. J Immunol 2002;169:5919-25.
37. De Rose V, Cappello P, Sorbello V, Ceccarini B, Gani F, Bosticardo M, et al. IFN‐γ inhibits the proliferation of allergen‐activated T lymphocytes from atopic, asthmatic patients by inducing Fas/FasL‐mediated apoptosis. J Leukoc Biol 2004;76:423-32.
38. Nakao F, Ihara K, Kusuhara K, Sasaki Y, Kinukawa N, Takabayashi A, et al. Association of IFN-γ and IFN regulatory factor 1 polymorphisms with childhood atopic asthma. J Allergy Clin Immunol Pract 2001;107:499-504.
39. Kumar S, Boehm J, Lee JC. p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov 2003;2:717-26.
40. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001;22:153-83.
41. Suzuki K, Hino M, Hato F, Tatsumi N, Kitagawa S. Cytokine-Specific Activation of Distinct Mitogen-Activated Protein Kinase Subtype Cascades in Human Neutrophils Stimulated by Granulocyte Colony-Stimulating Factor, Granulocyte-Macrophage Colony-Stimulating Factor, and Tumor Necrosis Factor-α. Blood 1999;93:341-9.
42. Alvarado-Kristensson M, Melander F, Leandersson K, Rönnstrand L, Wernstedt C, Andersson T. p38-MAPK signals survival by phosphorylation of caspase-8 and caspase-3 in human neutrophils. J Exp Med 2004;199:449-58.
43. Undevia NS, Dorscheid DR, Marroquin BA, Gugliotta WL, Tse R, White SR. Smad and p38-MAPK signaling mediates apoptotic effects of transforming growth factor-β1 in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004;287:L515-24.
44. Hawkins PT, Anderson KE, Davidson K, Stephens LR. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 2006;34:647-62.
45. Szefler SJ. Airway remodeling: therapeutic target or not? Am J Respir Crit Care Med 2005;171:672-3.
46. Feder LS, Stelts D, Chapman RW, Manfra D, Crawley Y, Jones H, et al. Role of nitric oxide on eosinophilic lung inflammation in allergic mice. Am J Respir Cell Mol Biol 1997;17:436-42.
47. Castellano I, Ercolesi E, Palumbo A. Nitric oxide affects ERK signaling through downregulation of MAP kinase phosphatase levels during larval development of the ascidian Ciona intestinalis. PLoS One 2014;9:e102907.
48. Cowburn AS, Deighton J, Walmsley SR, Chilvers ER. The survival effect of TNF‐α in human neutrophils is mediated via NF‐κB‐dependent IL‐8 release. Eur J Immunol 2004;34:1733-43.
49. Mirza AZ, Althagafi II, Shamshad H. Role of PPAR receptor in different diseases and their ligands: Physiological importance and clinical implications. Eur J Med Chem 2019;166:502-13.
50. Benayoun L, Letuve S, Druilhe A, Boczkowski J, Dombret MC, Mechighel P, et al. Regulation of peroxisome proliferator-activated receptor gamma expression in human asthmatic airways: relationship with proliferation, apoptosis, and airway remodeling. Am J Respir Crit Care Med 2001;164:1487-94.
51. Nutku E, Aizawa H, Hudson SA, Bochner BS. Ligation of Siglec-8: a selective mechanism for induction of human eosinophil apoptosis. Blood 2003;101:5014-20.
52. Bochner BS. Siglec‐8 on human eosinophils and mast cells, and Siglec‐F on murine eosinophils, are functionally related inhibitory receptors. Clin Exp Allergy 2009;39:317-24.
53. Kiwamoto T, Katoh T, Tiemeyer M, Bochner BS. The Role of lung epithelial ligands for Siglec-8 and Siglec-F in eosinophilic inflammation. Curr Opin Allergy Clin Immunol 2013;13:106-11.
54. Nutku E, Hudson SA, Bochner BS. Mechanism of Siglec-8-induced human eosinophil apoptosis: Role of caspases and mitochondrial injury. Biochem Biophys Res Commun 2005;336:918-24.
55. Mohammadian M, Sadeghipour HR, Jahromi GP, Jafari M, Nejad AK, Khamse S, et al. Simvastatin and bone marrow-derived mesenchymal stem cells (BMSCs) affects serum IgE and lung cytokines levels in sensitized mice. Cytokine 2019;113:83-8.
56. Panettieri RA Jr. Airway smooth muscle: immunomodulatory cells that modulate airway remodeling? Respir Physiol Neurobiol 2003;137:277-93.
57. James AJ, Penrose JF, Cazaly AM, Holgate ST, Sampson AP. Human bronchial fibroblasts express the 5-lipoxygenase pathway. Respir Res 2006;7:102.
58. Kiwamoto T, Ishii Y, Morishima Y, Yoh K, Maeda A, Ishizaki K, et al. Transcription factors T-bet and GATA-3 regulate development of airway remodeling. Am J Respir Crit Care Med 2006;174:142-51.
59. Minshall EM, Leung DY, Martin RJ, Song YL, Cameron L, Ernst P, et al. Eosinophil associated TGF-beta1 mRNA expression and airways fibrosis in bronchial asthma. Am J Respir Cell Mol Biol 1997;17:326-33.
60. Humbles AA, Lloyd CM, McMillan SJ, Friend DS, Xanthou G, McKenna EE, et al. A critical role for eosinophils in allergic airways remodeling. Science 2004;305:1776-9.
61. Chen G, Grotendorst G, Eichholtz T, Khalil N. GM-CSF increases airway smooth muscle cell connective tissue expression by inducing TGF-beta receptors. Am J Physiol Lung Cell Mol Physiol 2003;284:L548-56.
62. Yanagisawa K, Osada H, Masuda A, Kondo M, Saito T, Yatabe Y, et al. Induction of apoptosis by Smad3 and down-regulation of Smad3 expression in response to TGF-beta in human normal lung epithelial cells. Oncogene 1998;17:1743-7.
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| Files | ||
| Issue | Vol 59, No 9 (2021) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/acta.v59i9.7551 | |
| Keywords | ||
| Inflammation Airway remodeling Programmed cell death Apoptosis Asthma | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Kianian F, Kadkhodaee M, Sadeghipour HR, Seifi B. Study on the Critical Roles of Apoptosis in Asthma Disease. Acta Med Iran. 2021;59(9):516-523.
