The role of Bcl-2 family proteins in pulmonary fibrosis

European Journal of Pharmacology

Volumn 741, Issue , 2014, Pages 281-289

  Safaeian, Leila ^a   Abed, Alireza ^a   Vaseghi, Golnaz ^b  

^a ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Apoptosis; Bcl 2 family proteins; Pulmonary fibrosis

Indexed keywords

PROTEIN BCL 2;

ANIMAL; APOPTOSIS; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); HUMAN; LUNG FIBROSIS; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CLINICAL TRIALS AS TOPIC; HUMANS; PROTO-ONCOGENE PROTEINS C-BCL-2; PULMONARY FIBROSIS;

EID: 84907081285     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.07.029     Document Type: Review

References (102)

1. K.M. Antoniou, A. Pataka, D. Bouros, and N.M. Siafakas Pathogenetic pathways and novel pharmacotherapeutic targets in idiopathic pulmonary fibrosis Pulm. Pharmacol. Ther. 20 2007 453 461
2. A.L. Baptista, E.R. Parra, J.V. Filho, R.A. Kairalla, C.R. de Carvalho, and V.L. Capelozzi Structural features of epithelial remodeling in usual interstitial pneumonia histologic pattern Lung 184 2006 239 244
3. R.S. Bridges, D. Kass, K. Loh, C. Glackin, A.C. Borczuk, and S. Greenberg Gene expression profiling of pulmonary fibrosis identifies Twist1 as an antiapoptotic molecular "rectifier" of growth factor signaling Am. J. Pathol. 175 2009 2351 2361
4. G.R. Budinger, G.M. Mutlu, J. Eisenbart, A.C. Fuller, A.A. Bellmeyer, C.M. Baker, M. Wilson, K. Ridge, T.A. Barrett, V.Y. Lee, and N.S. Chandel Proapoptotic Bid is required for pulmonary fibrosis Proc. Natl. Acad. Sci. 103 2006 4604 4609
5. F. Bühling, A. Wille, C. Röcken, O. Wiesner, A. Baier, I. Meinecke, T. Welte, and T. Pap Altered expression of membrane-bound and soluble CD95/Fas contributes to the resistance of fibrotic lung fibroblasts to FasL induced apoptosis Respir. Res. 6 2005 37
6. A. Burlacu Regulation of apoptosis by Bcl-2 family proteins J. Cell Mol. Med. 7 2003 249 257
7. H.S. Chand, J.F. Harris, Y. Mebratu, Y. Chen, P.S. Wright, S.H. Randell, and Y. Tesfaigzi Intracellular insulin-like growth factor-1 induces Bcl-2 expression in airway epithelial cells J. Immunol. 188 2012 4581 4589
8. J.E. Chipuk, T. Moldoveanu, F. Llambi, M.J. Parsons, and D.R. Green The BCL-2 family reunion Mol. Cell 37 2010 299 310
9. R.G. Crystal, P.B. Bitterman, B. Mossman, M.I. Schwarz, D. Sheppard, L. Almasy, H.A. Chapman, S.L. Friedman, T.E. King Jr., L.A. Leinwand, L. Liotta, G.R. Martin, D.A. Schwartz, G.S. Schultz, C.R. Wagner, and R.A. Musson Future research directions in idiopathic pulmonary fibrosis Am. J. Respir. Crit. Care Med. 166 2002 236 246
10. O.M. de Brito, and L. Scorrano An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship EMBO J. 29 2010 2715 2723
11. G. Dewson, and R. Kluck Bcl-2 family-regulated apoptosis in health and disease Cell Health Cytoskelet. 2 2010 9 22
12. F. Drakopanagiotakis, A. Xifteri, E. Tsiambas, A. Karameris, K. Tsakanika, N. Karagiannidis, D. Mermigkis, V. Polychronopoulos, and D. Bouros Decreased apoptotic rate of alveolar macrophages of patients with idiopathic pulmonary fibrosis Pulm. Med. 2012 2012 981730
13. C.I. Dubreuil, M.J. Winton, and L. McKerracher Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system J. Cell Biol. 162 2003 233 243
14. M.C. Emblom-Callahan, M.K. Chhina, O.A. Shlobin, S. Ahmad, E.S. Reese, E.P. Iyer, D.N. Cox, R. Brenner, N.A. Burton, G.M. Grant, and S.D. Nathan Genomic phenotype of non-cultured pulmonary fibroblasts in idiopathic pulmonary fibrosis Genomics 96 2010 134 145
15. M. Galuppo, R. Di Paola, E. Mazzon, E. Esposito, I. Paterniti, A. Kapoor, C. Thiemermann, and S. Cuzzocrea GW0742, a high affinity PPAR-β/δ agonist reduces lung inflammation induced by bleomycin instillation in mice Int. J. Immunopathol. Pharmacol. 23 2010 1033 1046
16. M. Galuppo, E. Esposito, E. Mazzon, R. Di Paola, I. Paterniti, D. Impellizzeri, and S. Cuzzocrea MEK inhibition suppresses the development of lung fibrosis in the bleomycin model Naunyn Schm. Arch. Pharmacol. 384 2011 21 37
17. A.M. Gressner, B. Lahme, H.G. Mannherz, and B. Polzar TGF-β-mediated hepatocellular apoptosis by rat and human hepatoma cells and primary rat hepatocytes J. Hepatol. 26 1997 1079 1092
18. A. Gross, J.M. McDonnell, and S.J. Korsmeyer BCL-2 family members and the mitochondria in apoptosis Genes Dev. 13 1999 1899 1911
19. D. Guinee, E. Brambilla, M. Fleming, T. Hayashi, M. Rahn, M. Koss, V. Ferrans, and W. Travis The potential role of BAX and BCL-2 expression in diffuse alveolar damage Am. J. Pathol. 151 1997 999 1007
20. R.F. Hamilton, L. Li, T.B. Felder, and A. Holian Bleomycin induces apoptosis in human alveolar macrophages Am. J. Physiol. 269 1995 L318 L325
21. W.D. Huang, J.Z. Wang, Y.Q. Lu, Y.M. Dl, J.K. Jiang, and Q. Zhang Lysine acetylsalicylate ameliorates lung injury in rats acutely exposed to paraquat Chin. Med. J. 124 2011 2496 2501
22. E. Iwai-Kanai, K. Hasegawa, M. Araki, T. Kakita, T. Morimoto, and S. Sasayama alpha- and beta-adrenergic pathways differentially regulate cell type-specific apoptosis in rat cardiac myocytes Circulation 100 1999 305 311
23. J. Jehle, I. Staudacher, F. Wiedmann, P.A. Schweizer, R. Becker, H.A. Katus, and D. Thomas Regulation of apoptosis in HL-1 cardiomyocytes by phosphorylation of the receptor tyrosine kinase EphA2 and protection by lithocholic acid Br. J. Pharmacol. 167 2012 1563 1572
24. A. Jafarian-Dehkordi, M. Rabbani, H. Mir Mohammad Sadeghi, N. Afshar-Moghaddam, S.A. Alavi, F. Mahmoodi, and L. Safaeian Development and time-course of bleomycin-induced pulmonary fibrosis in NMRI mice DARU J. Pharm. Sci. 15 2007 1 6
25. Z. Jin, and W.S. El-Deiry Overview of cell death signaling pathways Cancer Biol. Ther. 4 2005 139 163
26. P.M. Kaan, R.G. Hegele, S. Hayashi, and J.C. Hogg Expression of bcl-2 and Epstein-Barr virus LMP1 in lymphocytic interstitial pneumonia Thorax 52 1997 12 16
27. D.W. Kamp, G. Liu, P. Cheresh, S.J. Kim, A. Mueller, A.P. Lam, H. Trejo, D. Williams, S. Tulasiram, M. Baker, K. Ridge, N.S. Chandel, and R. Beri Asbestos-induced alveolar epithelial cell apoptosis: role of endoplasmic reticulum stress response Am. J. Respir. Cell Mol. Biol. 49 2013 892 901
28. M.H. Kang, and C.P. Reynolds Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy Clin. Cancer Res. 15 2009 1126 1132
29. H.R. Kang, S.J. Cho, C.G. Lee, R.J. Homer, and J.A. Elias Transforming growth factor (TGF)-beta1 stimulates pulmonary fibrosis and inflammation via a Bax-dependent, bid-activated pathway that involves matrix metalloproteinase-12 J. Biol. Chem. 282 2007 7723 7732
30. M. Kasper, C. Roehlecke, M. Witt, H. Fehrenbach, A. Hofer, T. Miyata, C. Weigert, R.H. Funk, and E.D. Schleicher Induction of apoptosis by glyoxal in human embryonic lung epithelial cell line L132 Am. J. Respir. Cell Mol. Biol. 23 2000 485 491
31. M. Kazufumi, N. Sonoko, K. Masanori, I. Takateru, and O. Akira Expression of bcl-2 protein and APO-1 (Fas antigen) in the lung tissue from patients with idiopathic pulmonary fibrosis Microsc. Res. Tech. 38 1997 480 487
32. H. Kim, H.C. Tu, D. Ren, O. Takeuchi, J.R. Jeffers, G.P. Zambetti, J.J. Hsieh, and E.H. Cheng Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis Mol. Cell 36 2009 487 499
33. Y.C. Kim, and R.M. Day Angiotensin II regulates activation of Bim via Rb/E2F1 during apoptosis: involvement of interaction between AMPKβ1/2 and Cdk4 Am. J. Physiol. Lung Cell. Mol. Physiol. 303 2012 L228 L238
34. M. Konopleva, S. Zhao, Z. Xie, H. Segall, A. Younes, D.F. Claxton, Z. Estrov, S.M. Kornblau, and M. Andreeff Apoptosis: molecules and mechanisms Adv. Exp. Med. Biol. 457 1999 217 236
35. P. Kopiński, K. Sładek, J. Szczeklik, J. Soja, A. Szlubowski, B. Balicka-Slusarczyk, B. Lackowska, M. Plato, and A. Szpechciński Expression of insulin-like growth factor-I (IGF-I) in alveolar macrophages and lymphocytes obtained by bronchoalveolar lavage (BAL) in interstitial lung diseases (ILD). Assessment of IGF-I as a potential local mitogen and antiapoptotic cytokine Folia Histochem. Cytobiol. 44 2006 249 258
36. P. Kopiński, A. Dyczek, J. Chorostowska-Wynimko, A. Marszałek, B. Balicka-Slusarczyk, I. Kubiszewska, K. Szabłowska, E. Półgesek, and A. Szpechciński Higher incidence of alveolar lymphocytes (AL) apoptosis in smokers depends on BCL-2 expression and specific response to tumor necrosis factor alpha (TNFalpha). Bronchoalveolar lavage (BAL) material analysis from selected interstitial lung diseases (ILD) and healthy controls Przegl. Lek. 69 2012 731 736
37. L. Kong, Y.Q. Gao, J.F. Wang, J.Z. Niu, and X.X. Zhang Apoptosis of type II alveolar epithelial cell induced by bleomycin in lung fibrotic rat Zhongguo Yi Xue Ke Xue Yuan Xue Bao 29 2007 782 786
38. S. Krick, B.G. Eul, J. Hänze, R. Savai, F. Grimminger, W. Seeger, and F. Rose Role of hypoxia-inducible factor-1alpha in hypoxia-induced apoptosis of primary alveolar epithelial type II cells Am. J. Respir. Cell Mol. Biol. 32 2005 395 403
39. J.A. Kropski, W.E. Lawson, L.R. Young, and T.S. Blackwell Genetic studies provide clues on the pathogenesis of idiopathic pulmonary fibrosis Dis. Model. Mech. 6 2013 9 17
40. K. Kuwano, N. Hagimoto, T. Tanaka, M. Kawasaki, R. Kunitake, H. Miyazaki, Y. Kaneko, T. Matsuba, T. Maeyama, and N. Hara Expression of apoptosis-regulatory genes in epithelial cells in pulmonary fibrosis in mice J. Pathol. 190 2000 221 229
41. K. Kuwano, N. Hagimoto, T. Maeyama, M. Fujita, M. Yoshimi, I. Inoshima, N. Nakashima, N. Hamada, K. Watanabe, and N. Hara Mitochondria-mediated apoptosis of lung epithelial cells in idiopathic interstitial pneumonias Lab. Invest. 82 2002 1695 1706
42. K. Kuwno, N. Hagimoto, and N. Hara Molecular mechanisms of pulmonary fibrosis and current treatment Curr. Mol. Med. 1 2001 551 573
43. K. Kuwno, R. Kunitake, T. Maeyama, N. Hagimoto, M. Kawasaki, T. Matsuba, M. Yoshimi, I. Inoshima, K. Yoshida, and N. Hara Attenuation of bleomycin-induced peneumopathy in mice by a caspase inhibitor Am. J. Physiol. Lung Cell. Mol. Physiol. 280 2001 L316 L325
44. K. Kuwano, N. Hagimoto, M. Yoshimi, T. Maeyama, and Y. Nakanishi Apoptosis signaling pathways as therapeutic targets in lung injury Lett. Drug Des. Discov. 1 2004 263 268
45. T. Landes, and J.C. Martinou Mitochondrial outer membrane permeabilization during apoptosis: the role of mitochondrial fission Biochim. Biophys. Acta 1813 2011 540 545
46. V.Y. Lee, C. Schroedl, J.K. Brunelle, L.J. Buccellato, O.I. Akinci, H. Kaneto, C. Snyder, J. Eisenbart, G.R. Budinger, and N.S. Chandel Bleomycin induces alveolar epithelial cell death through JNK-dependent activation of the mitochondrial death pathway Am. J. Physiol. Lung Cell. Mol. Physiol. 289 2005 L521 L528
47. C.G. Lee, H.R. Kang, R.J. Homer, G. Chupp, and J.A. Elias Transgenic modeling of transforming growth factor-b1: role of apoptosis in fibrosis and alveolar remodeling Proc. Am. Thorac. Soc. 3 2006 418 423
48. Y.H. Lee, O. Mungunsukh, R.L. Tutino, A.P. Marquez, and R.M. Day Angiotensin-II-induced apoptosis requires regulation of nucleolin and Bcl-xL by SHP-2 in primary lung endothelial cells J. Cell Sci. 123 2010 1634 1643
49. X. Li, H. Rayford, and B.D. Uhal Essential roles for angiotensin receptor AT1a in bleomycin-induced apoptosis and lung fibrosis in mice Am. J. Pathol. 163 2003 2523 2530
50. J. Lindsay, M.D. Eaposti, and A.P. Gilmore Bcl-2 proteins and mitochondria-specificity in membrane targeting for death Biochim. Biophys. Acta 1813 2011 532 539
51. F. Llambi, and D.R. Green Apoptosis and oncogenesis: give and take in the BCL-2 family Curr. Opin. Genet. Dev. 21 2011 12 20
52. T. Maeyama, K. Kuwano, M. Kawasaki, R. Kunitake, N. Hagimoto, T. Matsuba, M. Yoshimi, I. Inoshima, K. Yoshida, and N. Hara Upregulation of Fas signaling molecules in lung epithelial cells from patients with idiopathicpulmonary fibrosis Eur. Respir. J. 17 2001 180 189
53. M. Machtay, A. Scherpereel, J. Santiago, J. Lee, J. McDonough, P. Kinniry, E. Arguiri, V.V. Shuvaev, J. Sun, K. Cengel, C.C. Solomides, and M. Christofidou-Solomidou Systemic polyethylene glycol-modified (PEGylated) superoxide dismutase and catalase mixture attenuates radiation pulmonary fibrosis in the C57/bl6 mouse Radiother. Oncol. 81 2006 196 205
54. R.P. Marshall, P. Gohlke, R.C. Chambers, D.C. Howell, S.E. Bottoms, T. Unger, R.J. McAnulty, and G.J. Laurent Angiotensin II and the fibroproliferative response to acute lung injury Am. J. Physiol. Lung Cell. Mol. Physiol. 286 2004 L156 L164
55. P. Meier, A. Finch, and G. Evan Apoptosis in development Nature 407 2000 796 801
56. C.M. Mermigkis, K. Tsakanika, V. Polychronopoulos, N. Karagianidis, D. Mermigkis, and D. Bouros Expression of bcl-2 protein in bronchoalveolar lavage cell populations from patients with idiopathic pulmonary fibrosis Acta Cytol. 45 2001 914 918
57. J. Meunier, and T. Hayashi Sigma-1 receptors regulate Bcl-2 expression by reactive oxygen species-dependent transcriptional regulation of nuclear factor kappaB J. Pharmacol. Exp. Ther. 332 2010 388 397
58. Y.P. Moodley, N.L. Misso, A.K. Scaffidi, M. Fogel-Petrovic, R.J. McAnulty, G.J. Laurent, P.J. Thompson, and D.A. Knight Inverse effects of interleukin-6 on apoptosis of fibroblasts from pulmonary fibrosis and normal lungs Am. J. Respir. Cell Mol. Biol. 29 2003 490 498
59. O. Mungunsukh, A.J. Griffin, Y.H. Lee, and R.M. Day Bleomycin induces the extrinsic apoptotic pathway in pulmonary endothelial cells Am. J. Physiol. Lung Cell. Mol. Physiol. 298 2010 L696 L703
60. H.F. Nadrous, J.H. Ryu, W.W. Douglas, P.A. Decker, and E.J. Olson Impact of angiotensin-converting enzyme inhibitors and statins on survival in idiopathic pulmonary fibrosis Chest 126 2004 438 446
61. N. Nakashima, K. Kuwano, T. Maeyama, N. Hagimoto, M. Yoshimi, N. Hamada, M. Yamada, and Y. Nakanishi The p53-Mdm2 associationin epithelial cells in idiopathic pulmonary fibrosis and non-specific interstitial pneumonia J. Clin. Pathol. 58 2005 583 589
62. Y. Nambu, N. Ohya, A. Satoh, H. Hayakawa, K. Oida, and Y. Kobashi Expression of bc1-2 protein in collagen vascular diseases with pulmonary interstitial involvement Nihon Kyobu Shikkan Gakkai Zasshi 33 Suppl. 1995 S284 S290
63. Y. Nishimura, T. Nishiike-Wada, Y. Wada, Y. Miura, T. Otsuki, and H. Iguchi Long-lasting production of TGF-beta1 by alveolar macrophages exposed to low doses of asbestos without apoptosis Int. J. Immunopathol. Pharmacol. 20 2007 661 671
64. Z.N. Oltvai, C.L. Milliman, and S.J. Korsmeyer Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death Cell 74 1999 609 619
65. V. Panduri, S.A. Weitzman, N. Chandel, and D.W. Kamp The mitochondria-regulated death pathway mediates asbestos-induced alveolar epithelial cell apoptosis Am. J. Respir. Cell Mol. Biol. 28 2003 241 248
66. V. Panduri, S. Surapureddi, S. Soberanes, S.A. Weitzman, N. Chandel, and D.W. Kamp P53 mediates amosite asbestos-induced alveolar epithelial cell mitochondria-regulated apoptosis Am. J. Respir. Cell Mol. Biol. 34 2006 443 452
67. A. Pardo, and M. Selman Molecules in focus Idiopathic pulmonary fibrosis: new insights in its pathogenesis Int. J. Biochem. Cell Biol. 34 2002 1534 1538
68. M. Plataki, A.V. Koutsopoulos, K. Darivianaki, G. Delides, N.M. Siafakas, and D. Bouros Expression of apoptotic and antiapoptotic markers in epithelial cells in idiopathic pulmonary fibrosis Chest 127 2005 266 274
69. V.A. Polnovsky, B. Chen, C. Henke, D. Snover, C. Wendt, D.H. Ingbar, and P.B. Bitterman Role of mesenchymal cell death in lung remodeling after injury J. Clin. Invest. 92 1993 388 397
70. G. Raghu, F. Nyberg, and G. Morgan The epidemiology of interstitial lung disease and its association with lung cancer Br. J. Cancer 91 2004 S3 S10
71. Ricci, A., Cherubini, E., Scozzi, D., Pietrangeli, V., Tabbì, L., Raffa, S., Leone, L., Visco, V., Torrisi, M.R., Bruno, P., Mancini, R., Ciliberto, G., Terzano, C., Mariotta, S., 2013. Decreased expression of autophagic Beclin 1 protein in idiopathic pulmonary fibrosis fibroblasts. J. Cell. Physiol. 228, 1516-1524.
72. S.J. Riedl, and G.S. Salvesen The apoptosome: signalling platform of cell death Nat. Rev. Mol. Cell Biol. 8 2007 405 413
73. K. Sugino, T. Ito, Y. Muramatsu, K. Sato, S. Sakamoto, and S. Homma Comparison of the clinical features of idiopathic pulmonary fibrosis in Japan and the U.S.A., based on disease severity Nihon. Kokyuki. Gakkai. Zasshi. 48 2010 892 897
74. L. Safaeian, A. Jafarian, M. Rabbani, H.M. Sadeghi, N. Afshar-Moghaddam, and S. Sarahroodi Comparison of bleomycin-induced pulmonary apoptosis between NMRI mice and C57BL/6 mice Res. Pharm. Sci. 8 2013 43 50
75. L. Safaeian, A. Jafarian, M. Rabbani, H.M. Sadeghi, N. Torabinia, and S.A. Alavi The effect of AT1 receptor blockade on bax and bcl-2 expression in bleomycin-induced pulmonary fibrosis DARU J. Pharm. Sci. 17 2009 53 59
76. L. Safaeian, A. Jafarian, M. Rabbani, H.M. Sadeghi, N. Torabiniaand, and S.A. Alavi The role of strain variation in BAX and BCL-2 expression in murine bleomycin-induced pulmonary fibrosis Pak. J. Biol. Sci. 11 2008 2606 2612
77. G.S. Salvesen, and C.S. Duckett IAP proteins: blocking the road to death's door Nat. Rev. Mol. Cell Biol. 3 2002 401 410
78. Y.Y. Sanders, H. Liu, X. Zhang, L. Hecker, K. Bernard, L. Desai, G. Liu, and V.J. Thannickal Histone modifications in senescence-associated resistance to apoptosis by oxidative stress Redox. Biol. 1 2013 8 16
79. Y. Satomi, K. Sakaguchi, Y. Kasahara, and F. Akahori Novel and extensive aspects of paraquat-induced pulmonary fibrogenesis: comparative and time-course microarray analyses in fibrogenic and non-fibrogenic rats J. Toxicol. Sci. 32 2007 529 553
80. M.J. Segel, R. Aqeilan, K. Zilka, H. Lorberboum-Galski, S.B. Wallach-Dayan, M.W. Conner, T.G. Christensen, and R. Breuer Effect of IL-2-Bax, a novel interleukin-2-receptor-targeted chimeric protein, on bleomycin lung injury Int. J. Exp. Pathol. 86 2005 279 288
81. H.J. Shin, K.K. Park, B.H. Lee, C.K. Moon, and M.O. Lee Identification of genes that are induced after cadmium exposure by suppression subtractive hybridization Toxicology 191 2003 121 131
82. S. Skwarna, I. Henneke, W. Seeger, A. Guenther, and C. Ruppert Relative role of hepatocyte growth factor in mediating epithelial cell-protective effects in lung fibrosis - a role of Bcl-xL induction Pneumologie 65- 2011 A59
83. D. Sorescu, W.E. Lawson, T.S. Blackwell, M. Rojas, and A.L. Mora Role of endoplasmic reticulum stress in age-related susceptibility to lung fibrosis Am. J. Respir. Cell Mol. Biol. 46 2012 748 756
84. J. Strausz, J. Muller-Quernheim, H. Steppling, and R. Ferlinz Oxygen radicalproduction by alveolar inflammatory cells in idiopathic pulmonaryfibrosis Am. Rev. Respir. Dis. 141 1990 124 128
85. T. Tanaka, M. Yoshimi, T. Maeyama, N. Hagimoto, K. Kuwano, and N. Hara Resistance to Fas-mediated apoptosis in human lung fibroblast Eur. Respir. J. 20 2002 359 368
86. V.J. Thannickal, and J.C. Horowitz Evolving concepts of apoptosis in idiopathic pulmonary fibrosis Am. Thorac. Soc. 3 2006 350 356
87. E. Torres-González, M. Bueno, A. Tanaka, L.T. Krug, D.S. Cheng, V.V. Polosukhin, Y.Y. Sanders, H. Liu, X. Zhang, L. Hecker, K. Bernard, L. Desai, G. Liu, and V.J. Thannickal Histone modifications in senescence-associated resistance to apoptosis by oxidative stress Redox Biol. 1 2013 8 16
88. A.C. Tsamandas, K. Thomopoulos, V. Zolota, T. Kourelis, T. Karatzas, P. Ravazoula, K. Tepetes, T. Petsas, D. Karavias, C. Karatza, D.S. Bonikos, and C. Gogos Potential role of bcl-2 and bax mRNA and protein expression in chronic hepatitis type B and C: a clinicopathologic study Mod. Pathol. 16 2003 1273 1288
89. B.D. Uhal Apoptosis in lung fibrosis and repair Chest 122 2002 293S 298S
90. B.D. Uhal The role of apoptosis in pulmonary fibrosis Eur. Respir. Rev. 17 2008 138 144
91. B.D. Uhal, I. Joshi, A.L. True, S. Mundle, A. Raza, A. Pardo, and M. Selman Fibroblasts isolated after fibrotic lung injury induce apoptosis of alveolar epithelial cells in vitro Am. J. Physiol. 269 1995 L819 L828
92. A.J. Valentijn, N. Zouq, and A.P. Anoikis Gilmore Biochem. Soc. Trans. 32 2007 421 425
93. R. Wang, C. Ramos, I. Joshi, A. Zagariya, A. Pardo, M. Selman, and B.D. Uhal Human lung myofibroblast-derived inducers of alveolar epithelial apoptosis identified as angiotensin peptides Am. J. Physiol. 277 1999 L1158 L1164
94. R. Wang, O. Ibarra-Sunga, L. Verlinski, R. Pick, and B.D. Uhal Abrogation of bleomycin-induced epithelial apoptosis and lung fibrosis by captopril or by a caspase inhibitor Am. J. Physiol. Lung Cell. Mol. Physiol. 279 2000 L143 L151
95. M. Waghray, Z. Cui, J.C. Horowitz, I.M. Subramanian, F.J. Martinez, G.B. Toews, and V.J. Thannickal Hydrogen peroxide is a diffusible paracrine signalfor the induction of epithelial cell death by activated myofibroblasts FASEB J. 19 2005 854 856
96. S.N. Willis, J.I. Fletcher, T. Kaufmann, M.F. van Delft, L. Chen, P.E. Czabotar, H. Ierino, E.F. Lee, W.D. Fairlie, P. Bouillet, A. Strasser, R.M. Kluck, J.M. Adams, and D.C. Huang Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak Science 315 2007 856 859
97. T.A. Wynn Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases J. Clin. Invest. 117 2007 524 529
98. N. Yan, and Y. Shi Mechanisms of apoptosis through structural biology Annu. Rev. Cell Dev. Biol. 21 2005 35 56
99. K. Yanagisawa, H. Osada, A. Masuda, K. Yanagisawa, H. Osada, A. Masuda, M. Kondo, T. Saito, Y. Yatabe, K. Takagi, T. Takahashi, and T. Takahashi Induction of apoptosis by Smad3 and down-regulation of Smad3 expression in response to TGF-β in human normal lung epithelial cells Oncogene 17 1998 1743 1747
100. H. Zhang, W.E. Lawson, V.V. Polosukhin, A. Pozzi, T.S. Blackwell, Y. Litingtung, and C. Chiang Inhibitor of differentiation 1 promotes endothelial survival in a bleomycin model of lung injury in mice Am. J. Pathol. 171 2007 1113 1126
101. H.Y. Zhang, and S.H. Phan Inhibition of myofibroblast apoptosis by transforming growth factor (TGF)-beta(1) Am. J. Respir. Cell Mol. Biol. 21 1999 658 665
102. Y. Zhou, X. Huang, L. Hecker, D. Kurundkar, A. Kurundkar, H. Liu, TH. Jin, L. Desai, K. Bernard, and V.J. Thannickal Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis J. Clin. Invest. 123 2013 1096 1108