Endoplasmic reticulum stress, a new wrestler, in the pathogenesis of idiopathic pulmonary fibrosis

American Journal of Translational Research

Volumn 9, Issue 2, 2017, Pages 722-735

  Zhang, Lei ^a   Wang, Yi ^a   Pandupuspitasari, Nuruliarizki Shinta ^a   Wu, Guorao ^a   Xiang, Xudong ^b   Gong, Quan ^c   Xiong, Weining ^a   Wang, Cong Yi ^a   Yang, Ping ^a   Ren, Boxu ^c  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c YANGTZE UNIVERSITY   (China)

Author keywords

ER stress; IPF; Pathogenesis; Profibrotic cells; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CALNEXIN; CALRETICULIN; CASPASE 4; CHAPERONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN 70; OXYGEN REGULATED PROTEIN 150; PROTEIN TYROSINE KINASE; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROSING ALVEOLITIS; FIBROSIS; HUMAN; INFLAMMATION; LUNG ALVEOLUS EPITHELIUM CELL; MACROPHAGE; POLARIZATION; PROTEIN MISFOLDING; UNFOLDED PROTEIN RESPONSE;

EID: 85014305470     PISSN: None     EISSN: 19438141     Source Type: Journal    
DOI: None     Document Type: Article

References (116)

1. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, Lynch DA, Ryu JH, Swigris JJ, Wells AU, Ancochea J, Bouros D, Carvalho C, Costabel U, Ebina M, Hansell DM, Johkoh T, Kim DS, King TE Jr, Kondoh Y, Myers J, Muller NL, Nicholson AG, Richeldi L, Selman M, Dud-den RF, Griss BS, Protzko SL and Schunemann HJ. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 2011; 183: 788-824.
2. Raghu G, Anstrom KJ, King TE Jr, Lasky JA and Martinez FJ. Prednisone, azathioprine, and N-acetylcysteine for pulmonary fibrosis. N Engl J Med 2012; 366: 1968-1977.
3. Raghu G, Weycker D, Edelsberg J, Bradford WZ and Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2006; 174: 810-816.
4. Gribbin J, Hubbard RB, Le Jeune I, Smith CJ, West J and Tata LJ. Incidence and mortality of idiopathic pulmonary fibrosis and sarcoidosis in the UK. Thorax 2006; 61: 980-985.
5. Hartert M, Senbaklavacin O, Gohrbandt B, Fischer BM, Buhl R and Vahld CF. Lung transplantation: a treatment option in end-stage lung disease. Dtsch Arztebl Int 2014; 111: 107-116.
6. Back SH, Lee K, Vink E and Kaufman RJ. Cyto-plasmic IRE1 alpha-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress. J Biol Chem 2006; 281: 18691-18706.
7. Asselah T, Bieche I, Mansouri A, Laurendeau I, Cazals-Hatem D, Feldmann G, Bedossa P, Paradis V, Martinot-Peignoux M, Lebrec D, Guich-ard C, Ogier-Denis E, Vidaud M, Tellier Z, Sou-melis V, Marcellin P and Moreau R. In vivo hepatic endoplasmic reticulum stress in patients with chronic hepatitis C. J Pathol 2010; 221: 264-274.
8. Ayala P, Montenegro J, Vivar R, Letelier A, Aran-guiz Urroz P, Copaja M, Pivet D, Humeres C, Troncoso R, Miguel Vicencio J, Lavandero S and Diaz-Araya G. Attenuation of endoplasmic reticulum stress using the chemical chaperone 4-phenylbutyric acid prevents cardiac fibrosis induced by isoproterenol. Exp Mol Pathol 2012; 92: 97-104.
9. Bertolotti A, Zhang YH, Hendershot LM, Harding HP and Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2: 326-332.
10. Bonner JC. Lung fibrotic responses to particle exposure. Toxicol Pathol 2007; 35: 148-153.
11. Bosio A, Knorr C, Janssen U, Gebel S, Hauss-mann HJ and Muller T. Kinetics of gene expression profiling in Swiss 3T3 cells exposed to aqueous extracts of cigarette smoke. Carcinogenesis 2002; 23: 741-748.
12. Selman M, King TE and Pardo A. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 2001; 134: 136-151.
13. Wilson MS and Wynn TA. Pulmonary fibrosis: pathogenesis, etiology and regulation. Mucosal Immunol 2009; 2: 103-121.
14. Knipe RS, Tager AM and Liao JK. The Rho kinases: critical mediators of multiple profibrotic processes and rational targets for new therapies for pulmonary fibrosis. Pharmacol Rev 2015; 67: 103-117.
15. Wolters PJ, Collard HR and Jones KD. Pathogenesis of idiopathic pulmonary fibrosis. Annu Rev Pathol 2014; 9: 157-179.
16. Aoki Y, Maeno T, Aoyagi K, Ueno M, Aoki F, Aoki N, Nakagawa J, Sando Y, Shimizu Y, Suga T, Arai M and Kurabayashi M. Pioglitazone, a per- oxisome proliferator-activated receptor gamma ligand, suppresses bleomycin-induced acute lung injury and fibrosis. Respiration 2009; 77: 311-319.
17. Armanios MY, Chen JJ, Cogan JD, Alder JK, In-gersoll RG, Markin C, Lawson WE, Xie M, Vulto I, Phillips JA 3rd, Lansdorp PM, Greider CW and Loyd JE. Telomerase mutations in families with idiopathic pulmonary fibrosis. N Engl J Med 2007; 356: 1317-1326.
18. Wynn TA and Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 2012; 18: 1028-1040.
19. Kage H and Borok Z. EMT and interstitial lung disease: a mysterious relationship. Curr Opin Pulm Med 2012; 18: 517-523.
20. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D and Chapman HA. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci U S A 2006; 103: 13180-13185.
21. Ho YY, Lagares D, Tager AM and Kapoor M. Fi-brosis--a lethal component of systemic sclerosis. Nat Rev Rheumatol 2014; 10: 390-402.
22. Strieter RM, Keeley EC, Hughes MA, Burdick MD and Mehrad B. The role of circulating mesenchymal progenitor cells (fibrocytes) in the pathogenesis of pulmonary fibrosis. J Leukoc Biol 2009; 86: 1111-1118.
23. Maharaj SS, Baroke E, Gauldie J and Kolb MR. Fibrocytes in chronic lung disease--facts and controversies. Pulm Pharmacol Ther 2012; 25: 263-267.
24. Lin JH, Walter P and Yen TS. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol 2008; 3: 399-425.
25. Schroder M and Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74: 739-789.
26. Sevier CS and Kaiser CA. Formation and transfer of disulphide bonds in living cells. Nat Rev Mol Cell Biol 2002; 3: 836-847.
27. Tu BP and Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 2004; 164: 341-346.
28. Saibil H. Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 2013; 14: 630-642.
29. Bi MX, Naczki C, Koritzinsky M, Fels D, Blais J, Hu NP, Harding H, Novoa I, Varia M, Raleigh J, Scheuner D, Kaufman RJ, Bell J, Ron D, Wout-ers BG and Koumenis C. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. Embo J 2005; 24: 3470-3481.
30. Bialik S and Kimchi A. DAP-kinase as a target for drug design in cancer and diseases associ- ated with accelerated cell death. Semin Cancer Biol 2004; 14: 283-294.
31. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, Lavail MM and Walter P. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007; 318: 944-949.
32. Song B, Scheuner D, Ron D, Pennathur S and Kaufman RJ. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008; 118: 3378-3389.
33. Qiu Y, Mao T, Zhang Y, Shao M, You J, Ding Q, Chen Y, Wu D, Xie D, Lin X, Gao X, Kaufman RJ, Li W and Liu Y. A crucial role for RACK1 in the regulation of glucose-stimulated IRE1alpha activation in pancreatic beta cells. Sci Signal 2010; 3: ra7.
34. Bettigole SE, Lis R, Adoro S, Lee AH, Spencer LA, Weller PF and Glimcher LH. The transcription factor XBP1 is selectively required for eosinophil differentiation. Nat Immunol 2015; 16: 829-837.
35. Korennykh AV, Egea PF, Korostelev AA, Finer-Moore J, Zhang C, Shokat KM, Stroud RM and Walter P. The unfolded protein response signals through high-order assembly of Ire1. Nature 2009; 457: 687-693.
36. Harding HP, Zhang Y and Ron D. Protein translation and folding are coupled by an endoplas-mic-reticulum-resident kinase. Nature 1999; 397: 271-274.
37. Tashiro E, Hironiwa N, Kitagawa M, Futamura Y, Suzuki S, Nishio M and Imoto M. Trierixin, a novel Inhibitor of ER stress-induced XBP1 activation from Streptomyces sp. 1. Taxonomy, fermentation, isolation and biological activities. J Antibiot (Tokyo) 2007; 60: 547-553.
38. Isler JA, Skalet AH and Alwine JC. Human cyto-megalovirus infection activates and regulates the unfolded protein response. J Virol 2005; 79: 6890-6899.
39. Wang M and Kaufman RJ. Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature 2016; 529: 326-335.
40. Bertolotti A, Zhang Y, Hendershot LM, Harding HP and Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2: 326-332.
41. Tanjore H, Lawson WE and Blackwell TS. Endoplasmic reticulum stress as a pro-fibrotic stimulus. Biochim Biophys Acta 2013; 1832: 940-947.
42. Grootjans J, Kaser A, Kaufman RJ and Blum-berg RS. The unfolded protein response in immunity and inflammation. Nat Rev Immunol 2016; 16: 469-484.
43. Tessitore A, del P Martin M, Sano R, Ma Y, Mann L, Ingrassia A, Laywell ED, Steindler DA, Am J Transl Res 2017;9(2):722-735 Hendershot LM and d’Azzo A. GM1-ganglio-side-mediated activation of the unfolded protein response causes neuronal death in a neu-rodegenerative gangliosidosis. Mol Cell 2004; 15: 753-766.
44. Hitomi J, Katayama T, Eguchi Y, Kudo T, Tanigu-chi M, Koyama Y, Manabe T, Yamagishi S, Bando Y, Imaizumi K, Tsujimoto Y and Tohyama M. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol 2004; 165: 347-356.
45. Krishnamoorthy T, Pavitt GD, Zhang F, Dever TE and Hinnebusch AG. Tight binding of the phosphorylated alpha subunit of initiation factor 2 (eIF2 alpha) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol Cell Biol 2001; 21: 5018-5030.
46. Lawson WE, Crossno PF, Polosukhin VV, Roldan J, Cheng DS, Lane KB, Blackwell TR, Xu C, Markin C, Ware LB, Miller GG, Loyd JE and Blackwell TS. Endoplasmic reticulum stress in alveolar epithelial cells is prominent in IPF: association with altered surfactant protein processing and herpesvirus infection. Am J Physiol Lung Cell Mol Physiol 2008; 294: L1119-L1126.
47. Lee AH, Iwakoshi NN and Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003; 23: 7448-7459.
48. Yoshida H, Haze K, Yanagi H, Yura T and Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 1998; 273: 33741-33749.
49. Tanjore H, Blackwell TS and Lawson WE. Emerging evidence for endoplasmic reticulum stress in the pathogenesis of idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2012; 302: L721-729.
50. Fehrenbach H. Alveolar epithelial type II cell: defender of the alveolus revisited. Respir Res 2001; 2: 33-46.
51. Rozycki HJ. Potential contribution of type I alveolar epithelial cells to chronic neonatal lung disease. Front Pediatr 2014; 2: 45.
52. Cao Z, Lis R, Ginsberg M, Chavez D, Shido K, Rabbany SY, Fong GH, Sakmar TP, Rafii S and Ding BS. Targeting of the pulmonary capillary vascular niche promotes lung alveolar repair and ameliorates fibrosis. Nat Med 2016; 22: 154-162.
53. Mulugeta S, Nureki S and Beers MF. Lost after translation: insights from pulmonary surfac- tant for understanding the role of alveolar epithelial dysfunction and cellular quality control in fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2015; 309: L507-525.
54. Plataki M, Koutsopoulos AV, Darivianaki K, Delides G, Siafakas NM and Bouros D. Expression of apoptotic and antiapoptotic markers in epithelial cells in idiopathic pulmonary fibrosis. Chest 2005; 127: 266-274.
55. Gunther A, Lubke N, Ermert M, Schermuly RT, Weissmann N, Breithecker A, Markart P, Ruppert C, Quanz K, Ermert L, Grimminger F and Seeger W. Prevention of bleomycin-induced lung fibrosis by aerosolization of heparin or urokinase in rabbits. Am J Respir Crit Care Med 2003; 168: 1358-1365.
56. Kuwano K. Involvement of epithelial cell apoptosis in interstitial lung diseases. Intern Med 2008; 47: 345-353.
57. Cheresh P, Kim SJ, Tulasiram S and Kamp DW. Oxidative stress and pulmonary fibrosis. Biochim Biophys Acta 2013; 1832: 1028-1040.
58. Cui Y, Robertson J, Maharaj S, Waldhauser L, Niu J, Wang J, Farkas L, Kolb M and Gauldie J. Oxidative stress contributes to the induction and persistence of TGF-beta 1 induced pulmonary fibrosis. Int J Biochem Cell Biol 2011; 43: 1122-1133.
59. Lekkerkerker AN, Aarbiou J, van Es T and Janssen RA. Cellular players in lung fibrosis. Curr Pharm Des 2012; 18: 4093-4102.
60. Lawson WE, Cheng DS, Degryse AL, Tanjore H, Polosukhin VV, Xu XC, Newcomb DC, Jones BR, Roldan J, Lane KB, Morrisey EE, Beers MF, Yull FE and Blackwell TS. Endoplasmic reticulum stress enhances fibrotic remodeling in the lungs. Proc Natl Acad Sci U S A 2011; 108: 10562-10567.
61. Mulugeta S, Maguire JA, Newitt JL, Russo SJ, Kotorashvili A and Beers MF. Misfolded BRICHOS SP-C mutant proteins induce apoptosis via caspase-4- and cytochrome c-related mechanisms. Am J Physiol Lung Cell Mol Physiol 2007; 293: L720-L729.
62. Mulugeta S, Nguyen V, Russo SJ, Muniswamy M and Beers MF. A surfactant protein C precursor protein BRICHOS domain mutation causes endoplasmic reticulum stress, proteasome dysfunction, and caspase 3 activation. Am J Respir Cell Mol Biol 2005; 32: 521-530.
63. Maitra M, Wang Y, Gerard RD, Mendelson CR and Garcia CK. Surfactant protein A2 mutations associated with pulmonary fibrosis lead to protein instability and endoplasmic reticulum stress. J Biol Chem 2010; 285: 22103-22113.
64. Korfei M, Ruppert C, Mahavadi P, Henneke I, Markart P, Koch M, Lang G, Fink L, Bohle RM, Seeger W, Weaver TE and Guenther A. Epithe- lial endoplasmic reticulum stress and apoptosis in sporadic idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2008; 178: 838-846.
65. Lawson WE, Crossno PF, Polosukhin VV, Roldan J, Cheng DS, Lane KB, Blackwell TR, Xu C, Markin C, Ware LB, Miller GG, Loyd JE and Blackwell TS. Endoplasmic reticulum stress in alveolar epithelial cells is prominent in IPF: association with altered surfactant protein processing and herpesvirus infection. Am J Physiol Lung Cell Mol Physiol 2008; 294: L1119-1126.
66. Lawson WE, Cheng DS, Degryse AL, Tanjore H, Polosukhin VV, Xu XC, Newcomb DC, Jones BR, Roldan J, Lane KB, Morrisey EE, Beers MF, Yull FE and Blackwell TS. Endoplasmic reticulum stress enhances fibrotic remodeling in the lungs. Proc Natl Acad Sci U S A 2011; 108: 10562-10567.
67. Mahavadi P, Henneke I, Ruppert C, Knudsen L, Venkatesan S, Liebisch G, Chambers RC, Ochs M, Schmitz G, Vancheri C, Seeger W, Korfei M and Guenther A. Altered surfactant homeostasis and alveolar epithelial cell stress in amiod-arone-induced lung fibrosis. Toxicol Sci 2014; 142: 285-297.
68. Kamp DW, Liu G, Cheresh P, Kim SJ, Mueller A, Lam AP, Trejo H, Williams D, Tulasiram S, Baker M, Ridge K, Chandel NS and Beri R. Asbestos-induced alveolar epithelial cell apoptosis. The role of endoplasmic reticulum stress response. Am J Respir Cell Mol Biol 2013; 49: 892-901.
69. Leers MPG, Kolgen W, Bjorklund V, Bergman T, Tribbick G, Persson B, Bjorklund P, Ramaekers FC, Bjorklund B, Nap M, Jornvall H and Schutte B. Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis. J Pathol 1999; 187: 567-572.
70. Cha SI, Ryerson CJ, Lee JS, Kukreja J, Barry SS, Jones KD, Elicker BM, Kim DS, Papa FR, Collard HR and Wolters PJ. Cleaved cytokeratin-18 is a mechanistically informative biomarker in idiopathic pulmonary fibrosis. Respir Res 2012; 13: 105.
71. Uhal BD, Li X, Xue A, Gao X and Abdul-Hafez A. Regulation of alveolar epithelial cell survival by the ACE-2/angiotensin 1-7/Mas axis. Am J Physiol Lung Cell Mol Physiol 2011; 301: L269-L274.
72. Uhal BD, Nguyen H, Dang M, Gopallawa I, Jiang J, Dang V, Ono S and Morimoto K. Abrogation of ER stress-induced apoptosis of alveolar epithelial cells by angiotensin 1-7. Am J Physiol Lung Cell Mol Physiol 2013; 305: L33-41.
73. Winters CJ, Koval O, Murthy S, Allamargot C, Sebag SC, Paschke JD, Jaffer OA, Carter AB and Grumbach IM. CaMKII inhibition in type II pneumocytes protects from bleomycin-induced pulmonary fibrosis by preventing Ca2+-depen-dent apoptosis. Am J Physiol Lung Cell Mol Physiol 2016; 310: L86-94.
74. Nakajima F, Aratani S, Fujita H, Yagishita N, Ichinose S, Makita K, Setoguchi Y and Nakajima T. Synoviolin inhibitor LS-102 reduces endoplasmic reticulum stress-induced collagen secretion in an in vitro model of stress-related interstitial pneumonia. Int J Mol Med 2015; 35: 110-116.
75. Kato A, Okura T, Hamada C, Miyoshi S, Katayama H, Higaki J and Ito R. Cell stress induces upregulation of osteopontin via the ERK pathway in type II alveolar epithelial cells. PLoS One 2014; 9: e100106.
76. Willis BC and Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007; 293: L525-534.
77. Willis BC, duBois RM and Borok Z. Epithelial origin of myofibroblasts during fibrosis in the lung. Proc Am Thorac Soc 2006; 3: 377-382.
78. Saika S, Ikeda K, Yamanaka O, Flanders KC, Ohnishi Y, Nakajima Y, Muragaki Y and Ooshi-ma A. Adenoviral gene transfer of BMP-7, Id2, or Id3 suppresses injury-induced epithelial-to-mesenchymal transition of lens epithelium in mice. Am J Physiol Cell Physiol 2006; 290: C282-289.
79. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F and Kalluri R. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 2003; 9: 964-968.
80. Moon RT, Kohn AD, De Ferrari GV and Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat Rev Genet 2004; 5: 691-701.
81. Ulianich L, Garbi C, Treglia AS, Punzi D, Miele C, Raciti GA, Beguinot F, Consiglio E and Di Jeso B. ER stress is associated with dedifferen-tiation and an epithelial-to-mesenchymal tran-sition-like phenotype in PC Cl3 thyroid cells. J Cell Sci 2008; 121: 477-486.
82. Tanjore H, Cheng DS, Degryse AL, Zoz DF, Ab-dolrasulnia R, Lawson WE and Blackwell TS. Alveolar epithelial cells undergo epithelial-to-mesenchymal transition in response to endoplasmic reticulum stress. J Biol Chem 2015; 290: 3277.
83. Zhong Q, Zhou B, Ann DK, Minoo P, Liu Y, Ban-falvi A, Krishnaveni MS, Dubourd M, Demaio L, Willis BC, Kim KJ, duBois RM, Crandall ED, Beers MF and Borok Z. Role of endoplasmic reticulum stress in epithelial-mesenchymal transition of alveolar epithelial cells: effects of misfolded surfactant protein. Am J Respir Cell Mol Biol 2011; 45: 498-509.
84. Mo XT, Zhou WC, Cui WH, Li DL, Li LC, Xu L, Zhao P and Gao J. Inositol-requiring protein 1 -X-box-binding protein 1 pathway promotes epithelial-mesenchymal transition via mediating snail expression in pulmonary fibrosis. Int J Biochem Cell Biol 2015; 65: 230-238.
85. Lee MR, Lee GH, Lee HY, Kim DS, Chung MJ, Lee YC, Kim HR and Chae HJ. BAX inhibitor-1-associated V-ATPase glycosylation enhances collagen degradation in pulmonary fibrosis. Cell Death Dis 2014; 5: e1113.
86. Reimers K, Choi CY, Bucan V and Vogt PM. The Bax Inhibitor-1 (BI-1) family in apoptosis and tumorigenesis. Curr Mol Med 2008; 8: 148-156.
87. Zhao H, Qin HY, Cao LF, Chen YH, Tan ZX, Zhang C and Xu DX. Phenylbutyric acid inhibits epithelial-mesenchymal transition during bleomycin-induced lung fibrosis. Toxicol Lett 2015; 232: 213-220.
88. Zhao H, Wu QQ, Cao LF, Qing HY, Zhang C, Chen YH, Wang H, Liu RY and Xu DX. Melatonin inhibits endoplasmic reticulum stress and epithelial-mesenchymal transition during bleomycin-induced pulmonary fibrosis in mice. PLoS One 2014; 9: e97266.
89. Varin A and Gordon S. Alternative activation of macrophages: immune function and cellular biology. Immunobiology 2009; 214: 630-641.
90. Byrne AJ, Mathie SA, Gregory LG and Lloyd CM. Pulmonary macrophages: key players in the innate defence of the airways. Thorax 2015; 70: 1189-1196.
91. Byrne AJ, Maher TM and Lloyd CM. Pulmonary macrophages: A new therapeutic pathway in fibrosing lung disease? Trends Mol Med 2016; 22: 303-316.
92. Sica A and Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122: 787-795.
93. Mills CD. M1 and M2 macrophages: Oracles of health and disease. Crit Rev Immunol 2012; 32: 463-488.
94. Rhee I. Diverse macrophages polarization in tumor microenvironment. Arch Pharm Res 2016; 39: 1588-1596.
95. Ryan AJ, Larson-Casey JL, He C, Murthy S and Carter AB. Asbestos-induced disruption of calcium homeostasis induces endoplasmic reticulum stress in macrophages. J Biol Chem 2014; 289: 33391-33403.
96. Ono M, Ohkouchi S, Kanehira M, Tode N, Kobayashi M, Ebina M, Nukiwa T, Irokawa T, Oga-wa H, Akaike T, Okada Y, Kurosawa H, Kikuchi T and Ichinose M. Mesenchymal stem cells correct inappropriate epithelial-mesenchyme relation in pulmonary fibrosis using stanniocal-cin-1. Mol Ther 2015; 23: 549-560.
97. Tao B, Jin W, Xu J, Liang Z, Yao J, Zhang Y, Wang K, Cheng H, Zhang X and Ke Y. Myeloid-specific disruption of tyrosine phosphatase Shp2 promotes alternative activation of macrophages and predisposes mice to pulmonary fibrosis. J Immunol 2014; 193: 2801-2811.
98. Gharib SA, Johnston LK, Huizar I, Birkland TP, Hanson J, Wang Y, Parks WC and Manicone AM. MMP28 promotes macrophage polarization toward M2 cells and augments pulmonary fibrosis. J Leukoc Biol 2014; 95: 9-18.
99. Wynn TA, Chawla A and Pollard JW. Macrophage biology in development, homeostasis and disease. Nature 2013; 496: 445-455.
100. Martinez FO, Helming L and Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009; 27: 451-483.
101. Lawrence T and Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 2011; 11: 750-761.
102. Brombacher F, Arendse B, Peterson R, Holscher A and Holscher C. Analyzing classical and alternative macrophage activation in macrophage/ neutrophil-specific IL-4 receptor-alpha-defici-ent mice. Methods Mol Biol 2009; 531: 225-252.
103. Rauh MJ, Ho V, Pereira C, Sham A, Sly LM, Lam V, Huxham L, Minchinton AI, Mui A and Krystal G. SHIP represses the generation of alternatively activated macrophages. Immunity 2005; 23: 361-374.
104. Oh J, Riek AE, Weng S, Petty M, Kim D, Colonna M, Cella M and Bernal-Mizrachi C. Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J Biol Chem 2012; 287: 11629-11641.
105. Zhang M, Guo Y, Fu H, Hu S, Pan J, Wang Y, Cheng J, Song J, Yu Q, Zhang S, Xu JF, Pei G, Xiang X, Yang P and Wang CY. Chop deficiency prevents UUO-induced renal fibrosis by attenuating fibrotic signals originated from Hmgb1/ TLR4/NFkappaB/IL-1beta signaling. Cell Death Dis 2015; 6: e1847.
106. Tanaka Y, Ishitsuka Y, Hayasaka M, Yamada Y, Miyata K, Endo M, Kondo Y, Moriuchi H, Irikura M, Tanaka K, Mizushima T, Oike Y and Irie T. The exacerbating roles of CCAAT/enhancer-binding protein homologous protein (CHOP) in the development of bleomycin-induced pulmonary fibrosis and the preventive effects of tau-roursodeoxycholic acid (TUDCA) against pulmonary fibrosis in mice. Pharmacol Res 2015; 99: 52-62.
107. Yao Y, Wang Y, Zhang Z, He L, Zhu J, Zhang M, He X, Cheng Z, Ao Q, Cao Y, Yang P, Su Y, Zhao J, Zhang S, Yu Q, Ning Q, Xiang X, Xiong W, Wang CY and Xu Y. Chop deficiency protects mice against bleomycin-induced pulmonary fibrosis by attenuating M2 macrophage production. Mol Ther 2016; 24: 915-925.
108. Ayaub EA, Kolb PS, Mohammed-Ali Z, Tat V, Murphy J, Bellaye PS, Shimbori C, Boivin FJ, Lai R, Lynn EG, Lhotak S, Bridgewater D, Kolb MR, Inman MD, Dickhout JG, Austin RC and Ask K. GRP78 and CHOP modulate macrophage apoptosis and the development of bleomycin-induced pulmonary fibrosis. J Pathol 2016; 239: 411-425.
109. Barron L, Gharib SA and Duffield JS. Lung pericytes and resident fibroblasts: Busy multitask-ers. Am J Pathol 2016; 186: 2519-2531.
110. Lama VN and Phan SH. The extrapulmonary origin of fibroblasts: stem/progenitor cells and beyond. Proc Am Thorac Soc 2006; 3: 373-376.
111. Andersson-Sjoland A, de Alba CG, Nihlberg K, Becerril C, Ramirez R, Pardo A, Westergren-Thorsson G and Selman M. Fibrocytes are a potential source of lung fibroblasts in idiopathic pulmonary fibrosis. Int J Biochem Cell Biol 2008; 40: 2129-2140.
112. Gharaee-Kermani M, Gyetko MR, Hu B and Phan SH. New insights into the pathogenesis and treatment of idiopathic pulmonary fibrosis: a potential role for stem cells in the lung parenchyma and implications for therapy. Pharm Res 2007; 24: 819-841.
113. Scotton CJ and Chambers RC. Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 2007; 132: 1311-1321.
114. Baek HA, Kim DS, Park HS, Jang KY, Kang MJ, Lee DG, Moon WS, Chae HJ and Chung MJ. Involvement of endoplasmic reticulum stress in myofibroblastic differentiation of lung fibroblasts. Am J Respir Cell Mol Biol 2012; 46: 731-739.
115. Tanaka KI, Shirai A, Ito Y, Namba T, Tahara K, Yamakawa N and Mizushima T. Expression of 150-kDa oxygen-regulated protein (ORP150) stimulates bleomycin-induced pulmonary fibrosis and dysfunction in mice. Biochem Biophys Res Commun 2012; 425: 818-824.
116. Zimmerman KA, Graham LV, Pallero MA and Murphy-Ullrich JE. Calreticulin regulates transforming growth factor-beta-stimulated extracellular matrix production. J Biol Chem 2013; 288: 14584-14598.