Apoptosis in lung injury and fibrosis

European Respiratory Journal

Volumn 32, Issue 6, 2008, Pages 1631-1638

  Drakopanagiotakis, F ^a   Xifteri, A ^a   Polychronopoulos, V ^a   Bouros, D ^b,c  

^a SISMANOGLIO HOSPITAL   (Greece)

^b DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^c DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

Author keywords

Apoptosis; Epithelium; Fibroblast; Mechanisms; Pathogenesis; Pulmonary fibrosis

Indexed keywords

CYTOKINE; DEATH RECEPTOR; MATRIX METALLOPROTEINASE; PROCOAGULANT; TRANSFORMING GROWTH FACTOR BETA1; VASOCONSTRICTOR AGENT;

APOPTOSIS; CELL TYPE; CYTOKINE PRODUCTION; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROSING ALVEOLITIS; HUMAN; HYPOXIA; INFLAMMATION; INFLAMMATORY CELL; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROSIS; LUNG INJURY; MACROPHAGE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW;

AGING; ANOXIA; APOPTOSIS; DNA; FIBROBLASTS; HUMANS; INFLAMMATION; LUNG INJURY; MACROPHAGES; MODELS, BIOLOGICAL; NEUTROPHILS; PULMONARY FIBROSIS; REACTIVE OXYGEN SPECIES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 58849086670     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00176807     Document Type: Review

References (86)

1. Selman M, King TE, Pardo A. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 2001; 134: 136-151.
2. Antoniou KM, Pataka A, Bouros D, Siafakas NM. Pathogenetic pathways and novel pharmacotherapeutic targets in idiopathic pulmonary fibrosis. Pulm Pharmacol Ther 2007; 20: 453-461.
3. Vandivier RW, Henson PM, Douglas IS. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest 2006; 129: 1673-1682.
4. Moore BB, Hogaboam CM. Murine models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008; 294: L152-L160.
5. Martin TR, Hagimoto N, Nakamura M, Matute-Bello G. Apoptosis and epithelial injury in the lungs. Proc Am Thorac Soc 2005; 2: 214-220.
6. Beere HM. Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 2005; 115: 2633-2639.
7. Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol 2002; 192: 131-137.
8. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397: 441-446.
9. Russell JH, Ley TJ. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol 2002; 20: 323-370.
10. Hagimoto N, Kuwano K, Nomoto Y, Kunitake R, Hara N. Apoptosis and expression of Fas/Fas ligand mRNA in bleomycin-induced pulmonary fibrosis in mice. Am J Respir Cell Mol Biol 1997; 16: 91-101.
11. Hagimoto N, Kuwano K, Miyazaki H, et al. Induction of apoptosis and pulmonary fibrosis in mice in response to ligation of Fas antigen. Am J Respir Cell Mol Biol 1997; 17: 272-278.
12. Golan-Gerstl R, Wallach-Dayan SB, Amir G, Breuer R. Epithelial cell apoptosis by fas ligand-positivemyofibroblasts in lung fibrosis. Am J Respir Cell Mol Biol 2007; 36: 270-275.
13. Kuwano K, Hagimoto N, Kawasaki M, et al. Essential roles of the Fas-Fas ligand pathway in the development of pulmonary fibrosis. J Clin Invest 1999; 104: 13-19.
14. Kuwano K, Kunitake R, Maeyama T, et al. Attenuation of bleomycin-induced pneumopathy in mice by a caspase inhibitor. Am J Physiol Lung Cell Mol Physiol 2001; 280: L316-L325.
15. Kuwano K, Kunitake R, Kawasaki M, et al. P21Waf1/Cip1/Sdi1 and p53 expression in association with DNA strand breaks in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 1996; 154: 477-483.
16. Uhal BD, Joshi I, Hughes WF, Ramos C, Pardo A, Selman M. Alveolar epithelial cell death adjacent to underlying myofibroblasts in advanced fibrotic human lung. Am J Physiol 1998; 275: L1192-L1199.
17. Nakashima N, Kuwano K, Maeyama T, et al. The p53-Mdm2 association in epithelial cells in idiopathic pulmonary fibrosis and non-specific interstitial pneumonia. J Clin Pathol 2005; 58: 583-589.
18. Inoshima I, Kuwano K, Hamada N, et al. Induction of CDK inhibitor p21 gene as a new therapeutic strategy against pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2004; 286: L727-L733.
19. Plataki M, Koutsopoulos AV, Darivianaki K, Delides G, Siafakas NM, Bouros D. Expression of apoptotic and antiapoptotic markers in epithelial cells in idiopathic pulmonary fibrosis. Chest 2005; 127: 266-274.
20. Desmouliere A. Factors influencing myofibroblast differentiation during wound healing and fibrosis. Cell Biol Int 1995; 19: 471-476.
21. Moodley YP, Caterina P, Scaffidi AK, et al. Comparison of the morphological and biochemical changes in normal human lung fibroblasts and fibroblasts derived from lungs of patients with idiopathic pulmonary fibrosis during FasL-induced apoptosis. J Pathol 2004; 202: 486-495.
22. Tanaka T, Yoshimi M, Maeyama T, Hagimoto N, Kuwano K, Hara N. Resistance to Fas-mediated apoptosis in human lung fibroblast. Eur Respir J 2002; 20: 359-368.
23. Buhling F, Wille A, Röcken C, et al. Altered expression of membrane-bound and soluble CD95/Fas contributes to the resistance of fibrotic lung fibroblasts to FasL induced apoptosis. Respir Res 2005; 6: 37.
24. Avivi-Green C, Singal M, Vogel WF. Discoidin domain receptor 1-deficient mice are resistant to bleomycin-induced lung fibrosis. Am J Respir Crit Care Med 2006; 174: 420-427.
25. Horowitz JC, Rogers DS, Sharma V, et al. Combinatorial activation of FAK and AKT by transforming growth factor-beta1 confers an anoikis-resistant phenotype to myofibroblasts. Cell Signal 2007; 19: 761-771.
26. Sanders YY, Kumbla P, Hagood JS. Enhanced myofibroblastic differentiation and survival in Thy-1- lung fibroblasts. Am J Respir Cell Mol Biol 2007; 36: 226-235.
27. Young LR, Pasula R, Gulleman PM, Deutsch GH, McCormack FX. Susceptibility of Hermansky-Pudlak mice to bleomycin-induced type II cell apoptosis and fibrosis. Am J Respir Cell Mol Biol 2007; 37: 67-74.
28. Hamilton RF Jr, Li L, Felder TB, Holian A. Bleomycin induces apoptosis in human alveolar macrophages. Am J Physiol 1995; 269: L318-L325.
29. Zhao HW, Hu SY, Barger MW, Ma JK, Castranova V, Ma JY. Time-dependent apoptosis of alveolar macrophages from rats exposed to bleomycin: involvement of TNF receptor 2. J Toxicol Environ Health A 2004; 67: 1391-1406.
30. Wang L, Antonini JM, Rojanasakul Y, Castranova V, Scabilloni JF, Mercer RR. Potential role of apoptotic macrophages in pulmonary inflammation and fibrosis. J Cell Physiol 2003; 194: 215-224.
31. Wang L, Scabilloni JF, Antonini JM, Rojanasakul Y, Castranova V, Mercer RR. Induction of secondary apoptosis, inflammation, and lung fibrosis after intratracheal instillation of apoptotic cells in rats. Am J Physiol Lung Cell Mol Physiol 2006; 290: L695-L702.
32. Kuwano K, Hagimoto N, Tanaka T, et al. Expression of apoptosis-regulatory genes in epithelial cells in pulmonary fibrosis in mice. J Pathol 2000; 190: 221-229.
33. Kuwano K, Miyazaki H, Hagimoto N, et al. The involvement of Fas-Fas ligand pathway in fibrosing lung diseases. Am J Respir Cell Mol Biol 1999; 20: 53-60.
34. Mermigkis CM, Tsakanika K, Polychronopoulos V, Karagianidis N, Mermigkis G, Bouros D. Expression of bcl-2 protein in bronchoalveolar lavage cell populations from patients with idiopathic pulmonary fibrosis. Acta Cytol 2001; 45: 914-918.
35. Baran CP, Opalek JM, McMaken S, et al. Important roles for M-CSF, CCL2 and mononuclear phagocytes in the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 2007; 176: 78-89.
36. Wynes MW, Frankel SK, Riches DW. IL-4-induced macrophage-derived IGF-I protects myofibroblasts from apoptosis following growth factor withdrawal. J Leukoc Biol 2004; 76: 1019-1027.
37. 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.
38. Turner-Warwick M, Haslam PL. The value of serial bronchoalveolar lavages in assessing the clinical progress of patients with cryptogenic fibrosing alveolitis. Am Rev Respir Dis 1987; 135: 26-34.
39. Li HP, Li X, He GJ, Yi XH, Kaplan AP. The influence of dexamethasone on the proliferation and apoptosis of pulmonary inflammatory cells in bleomycin-induced pulmonary fibrosis in rats. Respirology 2004; 9: 25-32.
40. Watters LC, Schwarz MI, Cherniack RM, et al. Idiopathic pulmonary fibrosis. Pretreatment bronchoalveolar lavage cellular constituents and their relationships with lung histopathology and clinical response to therapy. Am Rev Respir Dis 1987; 135: 696-704.
41. Thrall RS, Phan SH, McCormick JR, Ward PA. The development of bleomycin-induced pulmonary fibrosis in neutrophil-depleted and complement-depleted rats. Am J Pathol 1981; 105: 76-81.
42. Maher TM, Wells AU, Laurent GJ. Idiopathic pulmonary fibrosis: multiple causes and multiple mechanisms? Eur Respir J 2007; 30: 835-839.
43. McWhinnie R, Pechkovsky DV, Zhou D, et al. Endothelin-1 induces hypertrophy and inhibits apoptosis in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2007; 292: L278-L286.
44. Jain R, Shaul PW, Borok Z, Willis BC. Endothelin-1 induces alveolar epithelial-mesenchymal transition through endothelin type A receptor-mediated production of TGF-beta1. Am J Respir Cell Mol Biol 2007; 37: 38-47.
45. Li X, Molina-Molina M, Abdul-Hafez A, et al. Extravascular sources of lung angiotensin peptide synthesis in idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2006; 291: L887-L895.
46. Wang R, Ramos C, Joshi I, et al. Human lung myofibroblast-derived inducers of alveolar epithelial apoptosis identified as angiotensin peptides. Am J Physiol 1999; 277: L1158-L1164.
47. Wang R, Zagariya A, Ang E, Iburra-Sunga O, Uhal BD. Fas-induced apoptosis of alveolar epithelial cells requires ANG II generation and receptor interaction. Am J Physiol 1999; 277: L1245-1250.
48. Uhal BD, Gidea C, Bargout R, et al. Captopril inhibits apoptosis in human lung epithelial cells: a potential antifibrotic mechanism. Am J Physiol 1998; 275: L1013-L1017.
49. Li X, Rayford H, Uhal BD. Essential roles for angiotensin receptor AT1a in bleomycin-induced apoptosis and lung fibrosis in mice. Am J Pathol 2003; 163: 2523-2530.
50. Li X, Zhuang J, Rayford H, Zhang H, Shu R, Uhal BD. Attenuation of bleomycin-induced pulmonary fibrosis by intratracheal administration of antisense oligonucleotides against angiotensinogen mRNA. Curr Pharm Des 2007; 13: 1257-1268.
51. Kuwano K, Nakashima N, Inoshima I, et al. Oxidative stress in lung epithelial cells from patients with idiopathic interstitial pneumonias. Eur Respir J 2003; 21: 232-240.
52. Waghray M, Cui Z, Horowitz JC, et al. Hydrogen peroxide is a diffusible paracrine signal for the induction of epithelial cell death by activated myofibroblasts. FASEB J 2005; 19: 854-856.
53. Wallach-Dayan SB, Izbicki G, Cohen PY, Gerstl-Golan R, Fine A, Breuer R. Bleomycin initiates apoptosis of lung epithelial cells by ROS but not by Fas/FasL pathway. Am J Physiol Lung Cell Mol Physiol 2006; 290: L790-L796.
54. Psathakis K, Mermigkis D, Papatheodorou G, et al. Exhaled markers of oxidative stress in idiopathic pulmonary fibrosis. Eur J Clin Invest 2006; 36: 362-367.
55. Davis DW, Weidner DA, Holian A, McConkey DJ. Nitric oxide-dependent activation of p53 suppresses bleomycin-induced apoptosis in the lung. J Exp Med 2000; 192: 857-869.
56. Takahashi A, Aoshiba K, Nagai A. Apoptosis of wound fibroblasts induced by oxidative stress. Exp Lung Res 2002; 28: 275-284.
57. Krick S, Eul BG, Hänze J, et al. Role of hypoxia-inducible factor-1a in hypoxia-induced apoptosis of primary alveolar epithelial type II cells. Am J Respir Cell Mol Biol 2005; 32: 395-403.
58. Tzouvelekis A, Harokopos V, Paparountas T, et al. Comparative expression profiling in pulmonary fibrosis suggests a role of hypoxia-inducible factor-1alpha in disease pathogenesis. Am J Respir Crit Care Med 2007; 176: 1108-1119.
59. Kim KK, Kugler MC, Wolters PJ, et al. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 2006; 103: 13180-13185.
60. Zhu YK, Umino T, Liu XD, et al. Contraction of fibroblast-containing collagen gels: initial collagen concentration regulates the degree of contraction and cell survival. In Vitro Cell Dev Biol Anim 2001; 37: 10-16.
61. Hadden HL, Henke CA. Induction of lung fibroblast apoptosis by soluble fibronectin peptides. Am J Respir Crit Care Med 2000; 162: 1553-1560.
62. Farias E, Lu M, Li X, Schnapp LM. Integrin α8b1-fibronectin interactions promote cell survival via PI3 kinase pathway. Biochem Biophys Res Commun 2005; 329: 305-311.
63. Antoniou KM, Alexandrakis MG, Siafakas NM, Bouros D. Cytokine network in the pathogenesis of idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis 2005; 22: 91-104.
64. Hagimoto N, Kuwano K, Inoshima I, et al. TGF-β1 as an enhancer of Fas-mediated apoptosis of lung epithelial cells. J Immunol 2002; 168: 6470-6478.
65. Yamada M, Kuwano K, Maeyama T, et al. Gene transfer of soluble transforming growth factor type II receptor by in vivo electroporation attenuates lung injury and fibrosis. J Clin Pathol, 2007; 60: 916-920.
66. Budinger GR, Mutlu GM, Eisenbart J, et al. Proapoptotic Bid is required for pulmonary fibrosis. Proc Natl Acad Sci USA 2006; 103: 4604-4609.
67. Kang HR, Cho SJ, Lee CG, Homer RJ, Elias JA. Transforming growth factor (TGF)-β1 stimulates pulmonary fibrosis and inflammation via a Bax-dependent, Bid-activated pathway that involves matrix metalloproteinase-12. J Biol Chem 2007; 282: 7723-7732.
68. Yamasaki M, Kang HR, Homer RJ, et al. P21 regulates TGF-β1-induced pulmonary responses via a TNF-α signaling pathway. Am J Respir Cell Mol Biol 2008; 38: 346-353.
69. Kapoun AM, Gaspar NJ, Wang Y, et al. Transforming growth factor-β receptor type 1 (TGFβRI) kinase activity but not p38 activation is required for TGFβRI-induced myofibroblast differentiation and profibrotic gene expression. Mol Pharmacol 2006; 70: 518-531.
70. Frankel SK, Cosgrove GP, Cha SI, et al. TNF-alpha sensitizes normal and fibrotic human lung fibroblasts to Fas-induced apoptosis. Am J Respir Cell Mol Biol 2006; 34: 293-304.
71. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature 1997; 390: 350-351.
72. Gao Y, Herndon JM, Zhang H, Griffith TS, Ferguson TA. Antiinflammatory effects of CD95 ligand (FasL)-induced apoptosis. J Exp Med 1998; 188: 887-896.
73. Brown SB, Savill J. Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J Immunol 1999; 162: 480-485.
74. Gregory CD, Devitt A. The macrophage and the apoptotic cell: an innate immune interaction viewed simplistically? Immunology 2004; 113: 1-14.
75. Chambers RC. Procoagulant signalling mechanisms in lung inflammation and fibrosis: novel opportunities for pharmacological intervention? Br J Pharmacol 2008; 153: Suppl. 1, S367-S378.
76. Kubo H, Nakayama K, Yanai M, et al. Anticoagulant therapy for idiopathic pulmonaryfibrosis. Chest 2005; 128: 1475-1482.
77. Suzuki T, Moraes TJ, Vachon E, et al. Proteinase-activated receptor-1 mediates elastase-induced apoptosis of human lung epithelial cells. Am J Respir Cell Mol Biol 2005; 33: 231-247.
78. 6 integrin-dependent TGF-β activation and promotes acute lung injury. J Clin Invest 2006; 116: 1606-1614.
79. Brantly M, Avila NA, Shotelersuk V, Lucero C, Huizing M, Gahl WA. Pulmonary function and high-resolution CT findings in patients with an inherited form of pulmonary fibrosis, Hermansky-Pudlak syndrome, due to mutations in HPS-1. Chest 2000; 117: 129-136.
80. Campisi J. Senescent cells, tumour suppression, and organismal aging: good citizens, bad neighbors. Cell 2005; 120: 513-522.
81. Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, Choi AM. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol 1996; 14: 556-568.
82. Marcotte R, Lacelle C, Wang E. Senescent fibroblasts resist apoptosis by downregulating caspase-3. Mech Ageing Dev 2004; 125: 777-783.
83. Blasco MA. Telomere length, stem cells and aging. Nat Chem Biol 2007; 3: 640-649.
84. Tsakiri KD, Cronkhite JT, Kuan PJ, et al. Adult-onset pulmonary fibrosis caused by mutations in telomerase. Proc Natl Acad Sci USA 2007; 104: 7552-7557.
85. Fridlender ZG, Cohen PY, Golan O, Arish N, Wallach-Dayan S, Breuer R. Telomerase activity in bleomycin-induced epithelial cell apoptosis and lung fibrosis. Eur Respir J 2007; 30: 205-213.
86. Liu T, Chung MJ, Ullenbruch M, et al. Telomerase activity is required for bleomycin-induced pulmonary fibrosis in mice. J Clin Invest 2007; 117: 3800-3809.