Cigarette smoke-mediated oxidative stress induces apoptosis via the MAPKs/STAT1 pathway in mouse lung fibroblasts

Toxicology Letters

Volumn 240, Issue 1, 2016, Pages 140-148

  Lee, Hanbyeol ^a   Park, Jeong Ran ^a   Kim, Eun Jeong ^a   Kim, Woo Jin ^a   Hong, Seok Ho ^a   Park, Sung Min ^a   Yang, Se Ran ^a  

^a Kangwon National University   (South Korea)

Author keywords

Apoptosis; Cigarette smoke extract; Lung fibroblast; MAPKs; STAT1

Indexed keywords

CASPASE 3; CIGARETTE SMOKE; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PROTEIN BAX; STAT1 PROTEIN; BAX PROTEIN, MOUSE; CASP3 PROTEIN, MOUSE; CYCLOOXYGENASE 2; GLUTATHIONE; PTGS2 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; STAT1 PROTEIN, MOUSE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; ISOLATED LUNG; LUNG FIBROBLAST; LUNG TOXICITY; MOUSE; NEURAL STEM CELL; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIMARY CULTURE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKING; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; CELL PROLIFERATION; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; GENETICS; LUNG; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL PROLIFERATION; CYCLOOXYGENASE 2; FIBROBLASTS; GLUTATHIONE; INTERLEUKIN-6; LUNG; MAP KINASE SIGNALING SYSTEM; MICE; NITRIC OXIDE; OXIDATIVE STRESS; PHOSPHORYLATION; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SMOKING; STAT1 TRANSCRIPTION FACTOR; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84946606829     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.10.030     Document Type: Article

References (49)

1. Ahmad A., et al. Altered oxidant-antioxidant levels in the disease prognosis of chronic obstructive pulmonary disease. Int. J. Tuberc. Lung Dis. 2013, 17(8):1104-1109.
2. Aoshiba K., Nagai A. Chronic lung inflammation in aging mice. FEBS Lett. 2007, 581(18):3512-3516.
3. Barnes P.J. New anti-inflammatory targets for chronic obstructive pulmonary disease. Nat. Rev. Drug Discov. 2013, 12(7):543-559.
4. Cantin A.M., et al. Normal alveolar epithelial lining fluid contains high levels of glutathione. J. Appl. Physiol. 1987, 63(1):152-157.
5. Cao Z.H., et al. STAT1- mediated down-regulation of Bcl-2 expression is involved in IFN-gamma/TNF-alpha- induced apoptosis in NIT-1 cells. PLoS One 2015, 10(3):e0120921.
6. Carnevali S., et al. Cigarette smoke extract induces oxidative stress and apoptosis in human lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 284(6):L955-L963.
7. Deslee G., et al. Cigarette smoke induces nucleic-acid oxidation in lung fibroblasts. Am. J. Respir. Cell Mol. Biol. 2010, 43(5):576-584.
8. Di Stefano A., et al. Innate immunity but not NLRP3 inflammasome activation correlates with severity of stable COPD. Thorax 2014, 69(6):516-524.
9. Fischer B.M., et al. Pathogenic triad in COPD: oxidative stress, protease-antiprotease imbalance, and inflammation. Int. J. Chronic Obstruct. Pulmon. Dis. 2011, 6:413-421.
10. Flouris A.D., et al. Biological evidence for the acute health effects of secondhand smoke exposure. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 298(1):L3-12.
11. Gu W., et al. Mesenchymal stem cells alleviate airway inflammation and emphysema in COPD through down- regulation of cyclooxygenase-2 via p38 and ERK MAPK pathways. Sci. Rep. 2015, 5:8733.
12. Hogan B.L., et al. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell 2014, 15(2):123-138.
13. Holz O., et al. Lung fibroblasts from patients with emphysema show a reduced proliferation rate in culture. Eur. Respir. J. 2004, 24(4):575-579.
14. Houghton A.M. Mechanistic links between COPD and lung cancer. Nat. Rev. Cancer 2013, 13(4):233-245.
15. Hwang J.W., et al. Cigarette smoke-induced autophagy is regulated by SIRT1-PARP-1- dependent mechanism: implication in pathogenesis of COPD. Arch. Biochem. Biophys. 2010, 500(2):203-209.
16. Ibuki Y., et al. Cigarette sidestream smoke induces histone H3 phosphorylation via JNK and PI3K/Akt pathways, leading to the expression of proto-oncogenes. Carcinogenesis 2014, 35(6):1228-1237.
17. Kanaji N., et al. Fibroblasts that resist cigarette smoke-induced senescence acquire profibrotic phenotypes. Am. J. Physiol. Lung Cell. Mol. Physiol. 2014, 307(5):L364-L373.
18. Kim S.Y., et al. Mesenchymal stem cell-conditioned media recovers lung fibroblasts from cigarette smoke-induced damage. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 302(9):L891-908.
19. Kovarik P., et al. Stress-induced phosphorylation of STAT1 at Ser727 requires p38 mitogen-activated protein kinase whereas IFN-gamma uses a different signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(24):13956-13961.
20. Lavrentiadou S.N., et al. Ceramide-mediated apoptosis in lung epithelial cells is regulated by glutathione. Am. J. Respir. Cell Mol. Biol. 2001, 25(6):676-684.
21. Lee H., et al. Nicotine inhibits the proliferation by upregulation of nitric oxide and increased HDAC1 in mouse neural stem cells. In Vitro Cell. Dev. Biol. Anim. 2014, 50(8):731-739.
22. Lee J., et al. Is the aging process accelerated in chronic obstructive pulmonary disease?. Curr. Opin. Pulm. Med. 2011, 17(2):90-97.
23. Leonard W.J., O'Shea J.J. Jaks and STATs: biological implications. Annu. Rev. Immunol. 1998, 16:293-322.
24. Li L., et al. Nitric oxide upregulation of caspase-8 mRNA expression in lung endothelial cells: role of JAK2/STAT-1 signaling. Mol. Cell. Biochem. 2007, 305(1-2):71-77.
25. Malhotra D., et al. Expression of concern: 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(12):1196-1207.
26. Nathan C. Is iNOS beginning to smoke?. Cell 2011, 147(2):257-258.
27. Park S.Y., et al. Nicotine inhibits bFGF-induced neurite outgrowth through suppression of NO synthesis in H19-7 cells. Neurochem. Res. 2007, 32(3):481-488.
28. Park J.W., et al. Extracellular signal-regulated kinase (ERK) inhibition attenuates cigarette smoke extract (CSE) induced-death inducing signaling complex (DISC) formation in human lung fibroblasts (MRC-5) cells. J. Toxicol. Sci. 2010, 35(1):33-39.
29. Park J.W., et al. The phosphodiesterase 4 inhibitor rolipram protects against cigarette smoke extract-induced apoptosis in human lung fibroblasts. Eur. J. Pharmacol. 2013, 706(1-3):76-83.
30. Plantier L., et al. Defect of alveolar regeneration in pulmonary emphysema: role of lung fibroblasts. Int. J. Chronic Obstruct. Pulm. Dis. 2007, 2(4):463-469.
31. Plantier L., et al. Dysregulation of elastin expression by fibroblasts in pulmonary emphysema: role of cellular retinoic acid binding protein 2. Thorax 2008, 63(11):1012-1017.
32. Profita M., et al. Acetylcholine leads to signal transducer and activator of transcription 1 (STAT-1) mediated oxidative/nitrosative stress in human bronchial epithelial cell line. Biochim. Biophys. Acta 2013, 1832(12):1949-1958.
33. Rahman I., et al. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 2006, 1(6):3159-3165.
34. Ravid T., et al. Ceramide accumulation precedes caspase-3 activation during apoptosis of A549 human lung adenocarcinoma cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 284(6):L1082-L1092.
35. Rossi A., et al. Mechanisms, assessment and therapeutic implications of lung hyperinflation in COPD. Respir. Med. 2015, 109(7):785-802.
36. Roy Chowdhury S., et al. Bacterial fucose-rich polysaccharide stabilizes MAPK-mediated Nrf2/Keap1 signaling by directly scavenging reactive oxygen species during hydrogen peroxide-induced apoptosis of human lung fibroblast cells. PLoS One 2014, 9(11):e113663.
37. Salazar L.M., Herrera A.M. Fibrotic response of tissue remodeling in COPD. Lung 2011, 189(2):101-109.
38. Seimetz M., et al. Inducible NOS inhibition reverses tobacco-smoke-induced emphysema and pulmonary hypertension in mice. Cell 2011, 147(2):293-305.
39. Stephanou A., Latchman D.S. STAT-1: a novel regulator of apoptosis. Int. J. Exp. Pathol. 2003, 84(6):239-244.
40. Ueno M., et al. Alendronate inhalation ameliorates elastase-induced pulmonary emphysema in mice by induction of apoptosis of alveolar macrophages. Nat. Commun. 2015, 6:6332.
41. Wang W., et al. Lyn regulates cytotoxicity in respiratory epithelial cells challenged by cigarette smoke extracts. Curr. Mol. Med. 2014, 14(5):663-672.
42. Warburton D., Bellusci S. The molecular genetics of lung morphogenesis and injury repair. Paediatr. Respir. Rev. 2004, 5(Suppl. A):S283-S287.
43. Xu X., et al. Cigarette smoke exposure reveals a novel role for the MEK/ERK1/2 MAPK pathway in regulation of CFTR. Biochim. Biophys. Acta 2015, 1850(6):1224-1232.
44. Yang S.R., et al. RelB is differentially regulated by IkappaB kinase-alpha in B cells and mouse lung by cigarette smoke. Am. J. Respir. Cell Mol. Biol. 2009, 40(2):147-158.
45. Yang H., et al. 1alpha,25- Dihydroxyvitamin D3 induces neutrophil apoptosis through the p38 MAPK signaling pathway in chronic obstructive pulmonary disease patients. PLoS One 2015, 10(4):e0120515.
46. Zeng H., et al. Apoptosis and Bcl-2 family proteins, taken to chronic obstructive pulmonary disease. Eur. Rev. Med. Pharmacol. Sci. 2012, 16(6):711-727.
47. Zeng K.W., et al. Anti- neuroinflammatory effect of MC13, a novel coumarin compound from condiment murraya, through inhibiting lipopolysaccharide-induced TRAF6-TAK1-NF-kappaB, P38/ERK MAPKS and Jak2-Stat1/Stat3 pathways. J. Cell. Biochem. 2015, 116(7):1286-1299.
48. Zhang X., et al. Carbon monoxide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during anoxia-reoxygenation injury. J. Biol. Chem. 2005, 280(10):8714-8721.
49. Zuo L., et al. Interrelated role of cigarette smoking, oxidative stress, and immune response in COPD and corresponding treatments. Am. J. Physiol. Lung Cell. Mol. Physiol. 2014, 307(3):L205-L218.