Cigarette smoke-induced proteostasis imbalance in obstructive lung diseases

Current Molecular Medicine

Volumn 12, Issue 7, 2012, Pages 836-849

  Cantin, A M ^a   Richter, M V ^a  

^a CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

Author keywords

COPD; Epithelium; ER stress; Glutathione; Nrf2; Oxidants; Unfolded protein response; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ANTIOXIDANT; CCAAT ENHANCER BINDING PROTEIN; CIGARETTE SMOKE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE R; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2;

APOPTOSIS; CALCIUM HOMEOSTASIS; CELL CYCLE PROGRESSION; CELL DEATH; CELL SURVIVAL; CHRONIC OBSTRUCTIVE LUNG DISEASE; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; LUNG ALVEOLUS EPITHELIUM; MITOCHONDRION; OXIDATION; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEOSTASIS DEFICIENCY; RESPIRATORY EPITHELIUM; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84863517037     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/156652412801318746     Document Type: Review

References (173)

1. Vital signs: current cigarette smoking among adults aged >or=18 years United States, 2009. MMWR Morb Mortal Wkly Rep 2010; 59: 1135-40.
2. Garrett BE, Dube SR, Trosclair A, Caraballo RS, Pechacek TF. Cigarette Smoking --- United States, 1965--2008. MMWR Surveill Summ 2011; 60: 109-13.
3. Berry CE, Wise RA. Mortality in COPD: causes, risk factors, and prevention. COPD 2010; 7: 375-82.
4. Smoking-attributable mortality, years of potential life lost, and productivity losses-United States, 2000-2004. MMWR Morb Mortal Wkly Rep 2008; 57: 1226-8.
5. Celli BR, MacNee W. Standards for the diagnosis and treatment of patients with COPD: a summary of the ATS/ERS position paper. Eur Respir J 2004; 23: 932-46.
6. Viegi G, Pistelli F, Sherrill DL, Maio S, Baldacci S, Carrozzi L. Definition, epidemiology and natural history of COPD. Eur Respir J 2007; 30: 993-1013.
7. Hogg JC, Timens W. The pathology of chronic obstructive pulmonary disease. Annu Rev Pathol 2009; 4: 435-59.
8. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science 2008; 319: 916-9.
9. Gidalevitz T, Prahlad V, Morimoto RI. The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb Perspect Biol 2011; 3: a009704.
10. Herning RI, Jones RT, Bachman J, Mines AH. Puff volume increases when low-nicotine cigarettes are smoked. Br Med J (Clin Res Ed) 1981; 283: 187-9.
11. Church DF, Pryor WA. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 1985; 64: 111-26.
12. Zang LY, Stone K, Pryor WA. Detection of free radicals in aqueous extracts of cigarette tar by electron spin resonance. Free Radic Biol Med 1995; 19: 161-7.
13. Halliwell B, Gutteridge JMC. Reactive species can be poisonous: their role in toxicology. In: Halliwell B, Gutteridge JMC, Eds. Free radicals in biology and medicine; 4th ed. New York: Oxford Uinversity Press 2007; pp. 440-87.
14. Bartalis J, Zhao YL, Flora JW, Paine JB, Wooten JB. Carbon-centered radicals in cigarette smoke: acyl and alkylaminocarbonyl radicals. Anal Chem 2009; 81: 631-41.
15. Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci 1993; 686: 12-27; discussion -8.
16. McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 1969; 244: 6049-55.
17. Halliwell B. Superoxide-dependent formation of hydroxyl radicals in the presence of iron salts. Its role in degradation of hyaluronic acid by a superoxide-generating system. FEBS Lett 1978; 96: 238-42.
18. Mussalo-Rauhamaa H, Leppanen A, Salmela SS, Pyysalo H. Cigarettes as a source of some trace and heavy metals and pesticides in man. Arch Environ Health 1986; 41: 49-55.
19. Dikalov S, Alov P, Rangelova D. Role of iron ion chelation by quinones in their reduction, OH-radical generation and lipid peroxidation. Biochem Biophys Res Commun 1993; 195: 113-9.
20. Winston GW, Church DF, Cueto R, Pryor WA. Oxygen consumption and oxyradical production from microsomal reduction of aqueous extracts of cigarette tar. Arch Biochem Biophys 1993; 304: 371-8.
21. O'Neill CA, Halliwell B, van der Vliet A, et al. Aldehydeinduced protein modifications in human plasma: protection by glutathione and dihydrolipoic acid. J Lab Clin Med 1994; 124: 359-70.
22. Nguyen H, Finkelstein E, Reznick A, Cross C, van der Vliet A. Cigarette smoke impairs neutrophil respiratory burst activation by aldehyde-induced thiol modifications. Toxicology 2001; 160: 207-17.
23. Nardini M, Finkelstein EI, Reddy S, et al. Acrolein-induced cytotoxicity in cultured human bronchial epithelial cells. Modulation by alpha-tocopherol and ascorbic acid. Toxicology 2002; 170: 173-85.
24. Feng Z, Hu W, Hu Y, Tang MS. Acrolein is a major cigaretterelated lung cancer agent: Preferential binding at p53 mutational hotspots and inhibition of DNA repair. Proc Natl Acad Sci USA 2006; 103: 15404-9.
25. Pryor WA, Prier DG, Church DF. Electron-spin resonance study of mainstream and sidestream cigarette smoke: nature of the free radicals in gas-phase smoke and in cigarette tar. Environ Health Perspect 1983; 47: 345-55.
26. Hoidal JR, Fox RB, LeMarbre PA, Takiff HE, Repine JE. Oxidative metabolism of alveolar macrophages from young asymptomatic cigarette smokers. Increased superoxide anion release and its potential consequences. Chest 1980; 77: 270-1.
27. Hoidal JR, Fox RB, LeMarbe PA, Perri R, Repine JE. Altered oxidative metabolic responses in vitro of alveolar macrophages from asymptomatic cigarette smokers. Am Rev Respir Dis 1981; 123: 85-9.
28. Hubbard RC, Ogushi F, Fells GA, et al. Oxidants spontaneously released by alveolar macrophages of cigarette smokers can inactivate the active site of alpha 1- antitrypsin, rendering it ineffective as an inhibitor of neutrophil elastase. J Clin Invest 1987; 80: 1289-95.
29. Gadek JE, Fells GA, Crystal RG. Cigarette smoking induces functional antiprotease deficiency in the lower respiratory tract of humans. Science 1979; 206: 1315-6.
30. Cantin A, Crystal RG. Oxidants, antioxidants and the pathogenesis of emphysema. Eur J Respir Dis Suppl 1985; 139: 7-17.
31. Asami S, Manabe H, Miyake J, et al. Cigarette smoking induces an increase in oxidative DNA damage, 8- hydroxydeoxyguanosine, in a central site of the human lung. Carcinogenesis 1997; 18: 1763-6.
32. Sarir H, Mortaz E, Janse WT, Givi ME, Nijkamp FP, Folkerts G. IL-8 production by macrophages is synergistically enhanced when cigarette smoke is combined with TNFalpha. Biochem Pharmacol 2010; 79: 698-705.
33. Sarir H, Mortaz E, Karimi K, et al. Cigarette smoke regulates the expression of TLR4 and IL-8 production by human macrophages. J Inflamm (Lond) 2009; 6: 12.
34. Hunninghake GW, Gadek JE, Fales HM, Crystal RG. Human alveolar macrophage-derived chemotactic factor for neutrophils. Stimuli and partial characterization. J Clin Invest 1980; 66: 473-83.
35. Gadek JE, Hunninghake GW, Zimmerman RL, Crystal RG. Regulation of the release of alveolar macrophage-derived neutrophil chemotactic factor. Am Rev Respir Dis 1980; 121: 723-33.
36. Hunninghake G, Gadek J, Crystal R. Mechanism by which cigarette smoke attracts polymorphonuclear leukocytes to lung. Chest 1980; 77: 273.
37. Snelgrove RJ, Jackson PL, Hardison MT, et al. A critical role for LTA4H in limiting chronic pulmonary neutrophilic inflammation. Science 2010; 330: 90-4.
38. Braber S, Koelink PJ, Henricks PA, et al. Cigarette smokeinduced lung emphysema in mice is associated with prolyl endopeptidase, an enzyme involved in collagen breakdown. Am J Physiol Lung Cell Mol Physiol 2011; 300: L255-65.
39. Wallaert B, Gressier B, Marquette CH, et al. Inactivation of alpha 1-proteinase inhibitor by alveolar inflammatory cells from smoking patients with or without emphysema. Am Rev Respir Dis 1993; 147: 1537-43.
40. Rochelle LG, Fischer BM, Adler KB. Concurrent production of reactive oxygen and nitrogen species by airway epithelial cells in vitro. Free Radic Biol Med 1998; 24: 863-8.
41. Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2- related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci USA 1994; 91: 9926-30.
42. Itoh K, Chiba T, Takahashi S, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 1997; 236: 313-22.
43. Marklund SL. Human copper-containing superoxide dismutase of high molecular weight. Proc Natl Acad Sci USA 1982; 79: 7634-8.
44. Marklund SL. Extracellular superoxide dismutase and other superoxide dismutase isoenzymes in tissues from nine mammalian species. Biochem J 1984; 222: 649-55.
45. Meister A. Glutathione metabolism. Methods Enzymol 1995; 251: 3-7.
46. Meister A. Glutathione biosynthesis and its inhibition. Methods Enzymol 1995; 252: 26-30.
47. Dickinson DA, Levonen AL, Moellering DR, et al. Human glutamate cysteine ligase gene regulation through the electrophile response element. Free Radic Biol Med 2004; 37: 1152-9.
48. Lu SC. Regulation of glutathione synthesis. Mol Aspects Med 2009; 30: 42-59.
49. Rahman I, Bel A, Mulier B, et al. Transcriptional regulation of gamma-glutamylcysteine synthetase-heavy subunit by oxidants in human alveolar epithelial cells. Biochem Biophys Res Commun 1996; 229: 832-7.
50. Rahman I, Smith CA, Lawson MF, Harrison DJ, MacNee W. Induction of gamma-glutamylcysteine synthetase by cigarette smoke is associated with AP-1 in human alveolar epithelial cells. FEBS Lett 1996; 396: 21-5.
51. Lee TD, Yang H, Whang J, Lu SC. Cloning and characterization of the human glutathione synthetase 5'- flanking region. Biochem J 2005; 390: 521-8.
52. Hayes JD, Chanas SA, Henderson CJ, et al. The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochem Soc Trans 2000; 28: 33-41.
53. Homolya L, Varadi A, Sarkadi B. Multidrug resistanceassociated proteins: Export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 2003; 17: 103-14.
54. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol 2005; 45: 51-88.
55. Maher JM, Dieter MZ, Aleksunes LM, et al. Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 2007; 46: 1597-610.
56. Rahman I, MacNee W. Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease. Am J Physiol 1999; 277: L1067-88.
57. van der Toorn M, Smit-de Vries MP, Slebos DJ, et al. Cigarette smoke irreversibly modifies glutathione in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2007; 293: L1156-62.
58. Cantin AM, North SL, Hubbard RC, Crystal RG. Normal alveolar epithelial lining fluid contains high levels of glutathione. J Appl Physiol 1987; 63: 152-7.
59. Carolan BJ, Harvey BG, Hackett NR, O'Connor TP, Cassano PA, Crystal RG. Disparate oxidant gene expression of airway epithelium compared to alveolar macrophages in smokers. Respir Res 2009; 10: 111.
60. Rangasamy T, Cho CY, Thimmulappa RK, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smokeinduced emphysema in mice. J Clin Invest 2004; 114: 1248-59.
61. Cullinan SB, Diehl JA. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem 2004; 279: 20108-17.
62. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 2006; 38: 317-32.
63. Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 2005; 7: 385-94.
64. Boutten A, Goven D, Boczkowski J, Bonay M. Oxidative stress targets in pulmonary emphysema: focus on the Nrf2 pathway. Expert Opin Ther Targets 2010; 14: 329-46.
65. Wild AC, Moinova HR, Mulcahy RT. Regulation of gammaglutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J Biol Chem 1999; 274: 33627-36.
66. Moinova HR, Mulcahy RT. Up-regulation of the human gamma-glutamylcysteine synthetase regulatory subunit gene involves binding of Nrf-2 to an electrophile responsive element. Biochem Biophys Res Commun 1999; 261: 661-8.
67. Goven D, Boutten A, Lecon-Malas V, et al. Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema. Thorax 2008; 63: 916-24.
68. Suzuki M, Betsuyaku T, Ito Y, et al. Down-regulated NF-E2- related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2008; 39: 673-82.
69. Kinumi T, Kimata J, Taira T, Ariga H, Niki E. Cysteine-106 of DJ-1 is the most sensitive cysteine residue to hydrogen peroxide-mediated oxidation in vivo in human umbilical vein endothelial cells. Biochem Biophys Res Commun 2004; 317: 722-8.
70. Malhotra D, Thimmulappa R, Navas-Acien A, et al. Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am J Respir Crit Care Med 2008; 178: 592-604.
71. Dinkova-Kostova AT, Liby KT, Stephenson KK, et al. Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc Natl Acad Sci USA 2005; 102: 4584-9.
72. Molckovsky A, Siu LL. First-in-class, first-in-human phase I results of targeted agents: Highlights of the 2008 American Society of Clinical Oncology meeting. J Hematol Oncol 2008; 1: 20.
73. Sussan TE, Rangasamy T, Blake DJ, et al. Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc Natl Acad Sci USA 2009; 106: 250-5.
74. Li G, Scull C, Ozcan L, Tabas I. NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis. J Cell Biol 2010; 191: 1113-25.
75. Ezzi SA, Urushitani M, Julien JP. Wild-type superoxide dismutase acquires binding and toxic properties of ALSlinked mutant forms through oxidation. J Neurochem 2007; 102: 170-8.
76. Cumming RC, Schubert D. Amyloid-beta induces disulfide bonding and aggregation of GAPDH in Alzheimer's disease. Faseb J 2005; 19: 2060-2.
77. Simmen T, Lynes EM, Gesson K, Thomas G. Oxidative protein folding in the endoplasmic reticulum: tight links to the mitochondria-associated membrane (MAM). Biochim Biophys Acta 2010; 1798: 1465-73.
78. Enyedi B, Varnai P, Geiszt M. Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid Redox Signal 2010; 13: 721-9.
79. Gonzalez A, Granados MP, Salido GM, Pariente JA. H2O2- induced changes in mitochondrial activity in isolated mouse pancreatic acinar cells. Mol Cell Biochem 2005; 269: 165-73.
80. Hu Q, Zheng G, Zweier JL, Deshpande S, Irani K, Ziegelstein RC. NADPH oxidase activation increases the sensitivity of intracellular Ca2+ stores to inositol 1,4,5-trisphosphate in human endothelial cells. J Biol Chem 2000; 275: 15749-57.
81. Powell GM, Green GM. Investigation on the effects of cigarette smoke on rabbit alveolar macrophages. Biochem J 1971; 124: 26P-7P.
82. Tarze A, Deniaud A, Le Bras M, et al. GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene 2007; 26: 2606-20.
83. Nakajima H, Amano W, Fujita A, Fukuhara A, Azuma YT, Hata F, et al. The active site cysteine of the proapoptotic protein glyceraldehyde-3-phosphate dehydrogenase is essential in oxidative stress-induced aggregation and cell death. J Biol Chem 2007; 282: 26562-74.
84. Patterson RL, van Rossum DB, Kaplin AI, Barrow RK, Snyder SH. Inositol 1,4,5-trisphosphate receptor/GAPDH complex augments Ca2+ release via locally derived NADH. Proc Natl Acad Sci USA 2005; 102: 1357-9.
85. MacNee W, Donaldson K. Mechanism of lung injury caused by PM10 and ultrafine particles with special reference to COPD. Eur Respir J Suppl 2003; 40: 47s-51s.
86. McConkey DJ, Nutt LK. Calcium flux measurements in apoptosis. Methods in cell biology 2001; 66: 229-46.
87. Hovnanian A. SERCA pumps and human diseases. Subcellular biochemistry 2007; 45: 337-63.
88. Brini M. Plasma membrane Ca(2+)-ATPase: from a housekeeping function to a versatile signaling role. Pflugers Arch 2008; 457(3): 657-64.
89. Ulianich L, Garbi C, Treglia AS, et al. ER stress is associated with dedifferentiation and an epithelial-to-mesenchymal transition-like phenotype in PC Cl3 thyroid cells. J Cell Sci 2008; 121: 477-86.
90. Dremina ES, Sharov VS, Davies MJ, Schoneich C. Oxidation and inactivation of SERCA by selective reaction of cysteine residues with amino acid peroxides. Chem Res Toxicol 2007; 20: 1462-9.
91. Zaidi A, Barron L, Sharov VS, Schoneich C, Michaelis EK, Michaelis ML. Oxidative inactivation of purified plasma membrane Ca2+-ATPase by hydrogen peroxide and protection by calmodulin. Biochemistry 2003; 42: 12001-10.
92. Sharov VS, Dremina ES, Galeva NA, Williams TD, Schoneich C. Quantitative mapping of oxidation-sensitive cysteine residues in SERCA in vivo and in vitro by HPLCelectrospray-tandem MS: selective protein oxidation during biological aging. Biochem J 2006; 394: 605-15.
93. Nguyen T, Rubinstein NA, Vijayasarathy C, et al. Effect of chronic obstructive pulmonary disease on calcium pump ATPase expression in human diaphragm. J Appl Physiol 2005; 98: 2004-10.
94. Green HJ, Burnett M, Duhamel TA, et al. Abnormal sarcoplasmic reticulum Ca2+-sequestering properties in skeletal muscle in chronic obstructive pulmonary disease. Am J Physiol Cell Physiol 2008; 295: C350-7.
95. Taraseviciene-Stewart L, Voelkel NF. Molecular pathogenesis of emphysema. J Clin Invest 2008; 118: 394-402.
96. Cantin AM. Cellular response to cigarette smoke and oxidants: adapting to survive. Proc Am Thorac Soc 2010; 7: 368-75.
97. MacNee W, Rahman I. Is oxidative stress central to the pathogenesis of chronic obstructive pulmonary disease? Trends Mol Med 2001; 7: 55-62.
98. Louhelainen N, Rytila P, Haahtela T, Kinnula VL, Djukanovic R. Persistence of oxidant and protease burden in the airways after smoking cessation. BMC Pulm Med 2009; 9: 25.
99. Rahman I, van Schadewijk AA, Crowther AJ, et al. 4- Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2002; 166: 490-5.
100. Malhotra D, Thimmulappa R, Vij N, et al. Heightened endoplasmic reticulum stress in the lungs of patients with chronic obstructive pulmonary disease: the role of Nrf2- regulated proteasomal activity. Am J Respir Crit Care Med 2009; 180: 1196-207.
101. Jorgensen E, Stinson A, Shan L, Yang J, Gietl D, Albino AP. Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 2008; 8: 229.
102. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74: 739-89.
103. Yoshida H, Haze K, Yanagi H, Yura T, 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: 33741-9.
104. Tirasophon W, Welihinda AA, Kaufman RJ. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev 1998; 12: 1812-24.
105. Brewer JW, Diehl JA. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Natl Acad Sci USA 2000; 97: 12625-30.
106. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 2003; 23: 7198-209.
107. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999; 397: 271-4.
108. Haas IG, Wabl M. Immunoglobulin heavy chain binding protein. Nature 1983; 306: 387-9.
109. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2: 326-32.
110. Kelsen SG, Duan X, Ji R, Perez O, Liu C, Merali S. Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am J Respir Cell Mol Biol 2008; 38: 541-50.
111. Gewandter JS, Staversky RJ, O'Reilly MA. Hyperoxia augments ER-stress-induced cell death independent of BiP loss. Free Radic Biol Med 2009; 47: 1742-52.
112. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-29.
113. Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 2004; 101: 11269-74.
114. Hengstermann A, Muller T. Endoplasmic reticulum stress induced by aqueous extracts of cigarette smoke in 3T3 cells activates the unfolded-protein-response-dependent PERK pathway of cell survival. Free Radic Biol Med 2008; 44: 1097-107.
115. Geraghty P, Wallace A, D'Armiento JM. Induction of the unfolded protein response by cigarette smoke is primarily an activating transcription factor 4-C/EBP homologous protein mediated process. Int J Chron Obstruct Pulmon Dis 2011; 6: 309-19.
116. Miyamoto N, Izumi H, Miyamoto R, et al. Transcriptional regulation of activating transcription factor 4 under oxidative stress in retinal pigment epithelial ARPE-19/HPV-16 cells. Invest Ophthalmol Vis Sci 2011; 52: 1226-34.
117. Harding HP, Zhang Y, Zeng H, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003; 11: 619-33.
118. Raven JF, Baltzis D, Wang S, et al. PKR and PKR-like endoplasmic reticulum kinase induce the proteasomedependent degradation of cyclin D1 via a mechanism requiring eukaryotic initiation factor 2alpha phosphorylation. J Biol Chem 2008; 283: 3097-108.
119. Raven JF, Koromilas AE. PERK and PKR: old kinases learn new tricks. Cell Cycle 2008; 7: 1146-50.
120. Yamamoto K, Yoshida H, Kokame K, Kaufman RJ, Mori K. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. Journal of biochemistry 2004; 136: 343-50.
121. Groenendyk J, Michalak M. Endoplasmic reticulum quality control and apoptosis. Acta Biochim Pol 2005; 52: 381-95.
122. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454: 455-62.
123. Pierrou S, Broberg P, O'Donnell RA, et al. Expression of genes involved in oxidative stress responses in airway epithelial cells of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2007; 175: 577-86.
124. Sohal SS, Reid D, Soltani A, et al. Reticular basement membrane fragmentation and potential epithelial mesenchymal transition is exaggerated in the airways of smokers with chronic obstructive pulmonary disease. Respirology (Carlton, Vic) 2010; 15: 930-8.
125. Min T, Bodas M, Mazur S, Vij N. Critical role of proteostasisimbalance in pathogenesis of COPD and severe emphysema. J Mol Med 2011; 89(6): 577-93.
126. Rabe KF, Hurd S, Anzueto A, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 2007; 176: 532-55.
127. Vij N. AAA ATPase p97/VCP: cellular functions, disease and therapeutic potential. J Cell Mol Med 2008; 12: 2511-8.
128. Janssen-Heininger YM, Poynter ME, Baeuerle PA. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic Biol Med 2000; 28: 1317-27.
129. Fujisawa T, Velichko S, Thai P, Hung LY, Huang F, Wu R. Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-kappaB paradigm. J Immunol 2009; 183: 6236-43.
130. Ito K, Lim S, Caramori G, Chung KF, Barnes PJ, Adcock IM. Cigarette smoking reduces histone deacetylase 2 expression, enhances cytokine expression, and inhibits glucocorticoid actions in alveolar macrophages. Faseb J 2001; 15: 1110-2.
131. Barnes PJ, Adcock IM. Glucocorticoid resistance in inflammatory diseases. Lancet 2009; 373: 1905-17.
132. Barnes PJ. Role of HDAC2 in the pathophysiology of COPD. Annu Rev Physiol 2009; 71: 451-64.
133. Wu CH, Lin HH, Yan FP, Wang CJ. Immunohistochemical detection of apoptotic proteins, p53/Bax and JNK/FasL cascade, in the lung of rats exposed to cigarette smoke. Arch Toxicol 2006; 80: 328-36.
134. Park JW, Ryter SW, Choi AM. Functional significance of apoptosis in chronic obstructive pulmonary disease. COPD 2007; 4: 347-53.
135. Banzet N, Francois D, Polla BS. Tobacco smoke induces mitochondrial depolarization along with cell death: effects of antioxidants. Redox Rep 1999; 4: 229-36.
136. Chen ZH, Lam HC, Jin Y, et al. Autophagy protein microtubule-associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA 2010; 107: 18880-5.
137. Nakagawa T, Zhu H, Morishima N, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403: 98-103.
138. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002; 277: 34287-94.
139. Rao RV, Castro-Obregon S, Frankowski H, et al. Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 2002; 277: 21836-42.
140. Yoneda T, Imaizumi K, Oono K, et al. Activation of caspase- 12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 2001; 276: 13935-40.
141. Ng FW, Nguyen M, Kwan T, et al. p28 Bap31, a Bcl-2/Bcl- XL- and procaspase-8-associated protein in the endoplasmic reticulum. J Cell Biol 1997; 139: 327-38.
142. Rong Y, Distelhorst CW. Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 2008; 70: 73-91.
143. Tagawa Y, Hiramatsu N, Kasai A, et al. Induction of apoptosis by cigarette smoke via ROS-dependent endoplasmic reticulum stress and CCAAT/enhancer-binding protein-homologous protein (CHOP). Free Radic Biol Med 2008; 45: 50-9.
144. Boya P, Cohen I, Zamzami N, Vieira HL, Kroemer G. Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell death and differentiation 2002; 9: 465-7.
145. Li S, Perlman DM, Peterson MS, et al. Translation initiation factor 4E blocks endoplasmic reticulum-mediated apoptosis. J Biol Chem 2004; 279: 21312-7.
146. Wei MC, Zong WX, Cheng EH, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-30.
147. Kasahara Y, Tuder RM, Cool CD, Lynch DA, Flores SC, Voelkel NF. Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. Am J Respir Crit Care Med 2001; 163: 737-44.
148. Tuder RM, Zhen L, Cho CY, et al. Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. Am J Respir Cell Mol Biol 2003; 29: 88-97.
149. Shoshani T, Faerman A, Mett I, et al. Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol Cell Biol 2002; 22: 2283-93.
150. Ellisen LW, Ramsayer KD, Johannessen CM, et al. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol Cell 2002; 10: 995-1005.
151. Yoshida T, Mett I, Bhunia AK, et al. Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smokeinduced pulmonary injury and emphysema. Nat Med 2010; 16: 767-73.
152. Petrache I, Natarajan V, Zhen L, et al. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat Med 2005; 11: 491-8.
153. Petrache I, Medler TR, Richter AT, et al. Superoxide dismutase protects against apoptosis and alveolar enlargement induced by ceramide. Am J Physiol Lung Cell Mol Physiol 2008; 295: L44-53.
154. Diab KJ, Adamowicz JJ, Kamocki K, et al. Stimulation of sphingosine 1-phosphate signaling as an alveolar cell survival strategy in emphysema. Am J Respir Crit Care Med 2010; 181: 344-52.
155. Bodas M, Min T, Mazur S, Vij N. Critical modifier role of membrane-cystic fibrosis transmembrane conductance regulator-dependent ceramide signaling in lung injury and emphysema. J Immunol 2011; 186: 602-13.
156. Teichgraber V, Ulrich M, Endlich N, Riethmuller J, Wilker B, De Oliveira-Munding CC, et al. Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat Med 2008; 14: 382-91.
157. Cowley EA, Linsdell P. Oxidant stress stimulates anion secretion from the human airway epithelial cell line Calu-3: implications for cystic fibrosis lung disease. J Physiol 2002; 543: 201-9.
158. Jung JS, Lee JY, Oh SO, et al. Effect of t-butylhydroperoxide on chloride secretion in rat tracheal epithelia. Pharmacol Toxicol 1998; 82: 236-42.
159. Nguyen TD, Canada AT. Modulation of human colonic T84 cell secretion by hydrogen peroxide. Biochem Pharmacol 1994; 47: 403-10.
160. Tamai H, Kachur JF, Baron DA, Grisham MB, Gaginella TS. Monochloramine, a neutrophil-derived oxidant, stimulates rat colonic secretion. J Pharmacol Exp Ther 1991; 257: 887-94.
161. Cantin AM, Bilodeau G, Ouellet C, Liao J, Hanrahan JW. Oxidant stress suppresses CFTR expression. Am J Physiol Cell Physiol 2006; 290: C262-70.
162. Cantin AM, Hanrahan JW, Bilodeau G, et al. Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am J Respir Crit Care Med 2006; 173: 1139-44.
163. Bartoszewski R, Rab A, Twitty G, et al. The mechanism of cystic fibrosis transmembrane conductance regulator transcriptional repression during the unfolded protein response. J Biol Chem 2008; 283: 12154-65.
164. Rab A, Bartoszewski R, Jurkuvenaite A, Wakefield J, Collawn JF, Bebok Z. Endoplasmic reticulum stress and the unfolded protein response regulate genomic cystic fibrosis transmembrane conductance regulator expression. Am J Physiol Cell Physiol 2007; 292: C756-66.
165. Harrington MA, Kopito RR. Cysteine residues in the nucleotide binding domains regulate the conductance state of CFTR channels. Biophys J 2002; 82: 1278-92.
166. Bodas M, Min T, Vij N. Critical role of CFTR dependent lipidrafts in cigarette smoke induced lung epithelial injury. Am J Physiol Lung Cell Mol Physiol 2011.
167. Ryter SW, Choi AM. Autophagy in the lung. Proc Am Thorac Soc 2010; 7: 13-21.
168. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12: 222-30.
169. Kim HP, Wang X, Chen ZH, et al. Autophagic proteins regulate cigarette smoke-induced apoptosis: protective role of heme oxygenase-1. Autophagy 2008; 4: 887-95.
170. Chen ZH, Kim HP, Sciurba FC, et al. Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS One 2008; 3: e3316.
171. Ryter SW, Lam HC, Chen ZH, Choi AM. Deadly triplex: Smoke, autophagy, and apoptosis. Autophagy 2011; 7.
172. Richens TR, Linderman DJ, Horstmann SA, Lambert C, Xiao YQ, Keith RL, et al. Cigarette smoke impairs clearance of apoptotic cells through oxidant-dependent activation of RhoA. Am J Respir Crit Care Med 2009; 179: 1011-21.
173. Hodge S, Matthews G, Mukaro V, et al. Cigarette smokeinduced changes to alveolar macrophage phenotype and function are improved by treatment with procysteine. Am J Respir Cell Mol Biol 2011; 44: 673-81.