Cigarette smoke extract stimulates epithelial-mesenchymal transition through Src activation

Free Radical Biology and Medicine

Volumn 52, Issue 8, 2012, Pages 1437-1442

  Zhang, Hongqiao ^a   Liu, Honglei ^a   Borok, Zea ^b   Davies, Kelvin J A ^a,c   Ursini, Fulvio ^d   Forman, Henry Jay ^a,e  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cigarette smoke; Epithelial mesenchymal transition; Free radicals; N acetylcysteine; Redox; Src

Indexed keywords

ACETYLCYSTEINE; ACROLEIN; CATALASE; CIGARETTE SMOKE; NERVE CELL ADHESION MOLECULE; PROTEIN TYROSINE KINASE; UVOMORULIN; VIMENTIN;

ARTICLE; CARCINOMA CELL; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACETYLCYSTEINE; ACROLEIN; CATALASE; CELL LINE, TUMOR; ENZYME ACTIVATION; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; SMOKE; SRC-FAMILY KINASES; TOBACCO;

BOVINAE;

EID: 84862781190     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.01.024     Document Type: Article

References (76)

1. Willis, B. C.; Borok, Z. TGF-β-induced EMT: mechanisms and implications for fibrotic lung disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 293:L525-L534; 2007.
2. Gharaee-Kermani, M., et al. Recent advances in molecular targets and treatment of idiopathic pulmonary fibrosis: focus on TGFβ signaling and the myofibroblast. Curr. Med. Chem. 16:1400-1417; 2009.
3. Yauch, R. L., et al. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin. Cancer Res. 11:8686-8698; 2005.
4. Soltermann, A., et al. Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer. Clin. Cancer Res. 14:7430-7437; 2008.
5. Baumgartner, K. B., et al. Cigarette smoking: a risk factor for idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 155:242-248; 1997.
6. Biesalski, H. K., et al. European Consensus Statement on Lung Cancer: risk factors and prevention. Lung Cancer Panel. CA Cancer J. Clin. 48:167-176 discussion 164-166; 1998.
7. Besaratinia, A.; Pfeifer, G. P. Second-hand smoke and human lung cancer. Lancet Oncol. 9:657-666; 2008.
8. Asomaning, K., et al. Second hand smoke, age of exposure and lung cancer risk. Lung Cancer 61:13-20; 2008.
9. Cooley, M. E., et al. Smoking cessation is challenging even for patients recovering from lung cancer surgery with curative intent. Lung Cancer 66:218-225; 2009.
10. Burke, L., et al. Smoking behaviors among cancer survivors: an observational clinical study. J. Oncol. Pract. 5:6-9; 2009.
11. Walker, M. S., et al. Smoking relapse during the first year after treatment for early-stage non-small-cell lung cancer. Cancer Epidemiol. Biomarkers Prev. 15: 2370-2377; 2006.
12. Liu, Y.; Gao, W.; Zhang, D. Effects of cigarette smoke extract on A549 cells and human lung fibroblasts treated with transforming growth factor-β1 in a coculture system. Clin. Exp. Med. 10:159-167; 2010.
13. Sohal, S. S., et al. Reticular basement membrane fragmentation and potential epithelial mesenchymal transition is exaggerated in the airways of smokers with chronic obstructive pulmonary disease. Respirology 15:930-938; 2010.
14. Kasai, H., et al. TGF-β1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir. Res. 6:56; 2005.
15. Willis, B. C., et al. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-β1: potential role in idiopathic pulmonary fibrosis. Am. J. Pathol. 166:1321-1332; 2005.
16. Rodier, J. M., et al. pp 60c-src is a positive regulator of growth factor-induced cell scattering in a rat bladder carcinoma cell line. J. Cell Biol. 131:761-773; 1995.
17. Kong, D., et al. miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 27: 1712-1721; 2009.
18. Higgins, D. F., et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J. Clin. Invest. 117:3810-3820; 2007.
19. Nawshad, A., et al. Transforming growth factor-β signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs 179:11-23; 2005.
20. Cannito, S., et al. Epithelial-mesenchymal transition: from molecular mechanisms, redox regulation to implications in human health and disease. Antioxid. Redox Signaling 12:1383-1430; 2010.
21. Torres, M.; Forman, H. J. Activation of several MAP kinases upon stimulation of rat alveolar macrophages: role of the NADPH oxidase. Arch. Biochem. Biophys. 366: 231-239; 1999.
22. Lee, Y. J.; Han, H. J. Troglitazone ameliorates high glucose-induced EMT and dysfunction of SGLTs through PI3K/Akt, GSK-3β, Snail1, and β-catenin in renal proximal tubule cells. Am. J. Physiol. Renal Physiol. 298:F1263-F1275; 2010.
23. Jain, A. K.; Jaiswal, A. K. GSK-3β acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J. Biol. Chem. 282: 16502-16510; 2007.
24. 2-induced transactivation of EGF receptor requires Src and mediates ERK1/2, but not Akt, activation in renal cells. Am. J. Physiol. Renal Physiol. 286:F858-F865; 2004.
25. 2-induced phosphorylation of ERK1/2 and PKB requires tyrosine kinase activity of insulin receptor and c-Src. Antioxid. Redox Signaling 7: 1014-1020; 2005.
26. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogenactivated protein kinase-activated protein kinase-2. Biochem. J. 336:241-246; 1998.
27. Felton, V. M.; Borok, Z.; Willis, B. C. N-acetylcysteine inhibits alveolar epithelial-mesenchymal transition. Am. J. Physiol. Lung Cell. Mol. Physiol. 297:L805-L812; 2009.
28. Ingley, E. Src family kinases: regulation of their activities, levels and identification of new pathways. Biochim. Biophys. Acta 1784:56-65; 2008.
29. Liu, X.; Feng, R. Inhibition of epithelial to mesenchymal transition in metastatic breast carcinoma cells by c-Src suppression. Acta Biochim. Biophys. Sin. (Shanghai) 42:496-501; 2010.
30. Choi, Y. L., et al. LYN is a mediator of epithelial-mesenchymal transition and a target of dasatinib in breast cancer. Cancer Res. 70:2296-2306; 2010.
31. Martinez-Orozco, R., et al. Arachidonic acid promotes epithelial-to-mesenchymal-like transition in mammary epithelial cells MCF10A. Eur. J. Cell Biol. 89:476-488; 2010.
32. Yang, S. Z., et al. HBx protein induces EMT through c-Src activation in SMMC-7721 hepatoma cell line. Biochem. Biophys. Res. Commun. 382:555-560; 2009.
33. Cicchini, C., et al. TGFβ-induced EMT requires focal adhesion kinase (FAK) signaling. Exp. Cell Res. 314:143-152; 2008.
34. Ulianich, L., et al. ER stress is associated with dedifferentiation and an epithelialto- mesenchymal transition-like phenotype in PC Cl3 thyroid cells. J. Cell Sci. 121: 477-486; 2008.
35. Xu, K. P.; Yin, J.; Yu, F. S. SRC-family tyrosine kinases in wound- and ligand-induced epidermal growth factor receptor activation in human corneal epithelial cells. Invest. Ophthalmol. Visual Sci. 47:2832-2839; 2006.
36. Giannoni, E.; Taddei, M. L.; Chiarugi, P. Src redox regulation: again in the front line. Free Radic. Biol. Med. 49:516-527; 2010.
37. Giannoni, E., et al. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol. Cell. Biol. 25:6391-6403; 2005.
38. Meng, D., et al. Insulin-like growth factor-I (IGF-I) induces epidermal growth factor receptor transactivation and cell proliferation through reactive oxygen species. Free Radic. Biol. Med. 42:1651-1660; 2007.
39. Zhang, Y., et al. Mechanical strain-induced RhoA activation requires NADPH oxidase-mediated ROS generation in caveolae. Antioxid. Redox Signaling 13: 959-973; 2010.
40. Yan, S. R.; Berton, G. Regulation of Src family tyrosine kinase activities in adherent human neutrophils: evidence that reactive oxygen intermediates produced by adherent neutrophils increase the activity of the p58c-fgr and p53/56lyn tyrosine kinases. J. Biol. Chem. 271:23464-23471; 1996.
41. Mallozzi, C.; Di Stasi, A. M.; Minetti, M. Activation of src tyrosine kinases by peroxynitrite. FEBS Lett. 456:201-206; 1999.
42. Lee, E. K., et al. Decreased expression of glutaredoxin 1 is required for transforming growth factor-β1-mediated epithelial-mesenchymal transition of EpRas mammary epithelial cells. Biochem. Biophys. Res. Commun. 391:1021-1027; 2010.
43. Rhyu, D. Y., et al. Role of reactive oxygen species in TGF-β1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J. Am. Soc. Nephrol. 16:667-675; 2005.
44. Wu, W. S., et al. Reactive oxygen species mediated sustained activation of protein kinase Cα and extracellular signal-regulated kinase for migration of human hepatoma cell Hepg2. Mol. Cancer Res. 4:747-758; 2006.
45. Cannito, S., et al. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis 29:2267-2278; 2008.
46. Wu, W. S. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 25:695-705; 2006.
47. Tollefson, A. K., et al. Endogenous enzymes (NOX and ECSOD) regulate smoke-induced oxidative stress. Free Radic. Biol. Med. 49:1937-1946; 2010.
48. Hanke, J. H., et al. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor: study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:695-701; 1996.
49. Bain, J., et al. The specificities of protein kinase inhibitors: an update. Biochem. J. 371:199-204; 2003.
50. Dasgupta, P., et al. Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int. J. Cancer 124:36-45; 2009.
51. Zhong, Q., et al. Role of endoplasmic reticulum stress in epithelial-mesenchymal transition of alveolar epithelial cells: effects of misfolded surfactant protein. Am. J. Respir. Cell Mol. Biol. 45:498-509; 2011.
52. Lambert, C., et al. Acrolein in cigarette smoke inhibits T-cell responses. J. Allergy Clin. Immunol. 116:916-922; 2005.
53. Eiserich, J. P., et al. Dietary antioxidants and cigarette smoke-induced biomolecular damage: a complex interaction. Am. J. Clin. Nutr. 62 (6 Suppl.):1490S-1500S; 1995.
54. Aoshiba, K., et al. Immunohistochemical evaluation of oxidative stress in murine lungs after cigarette smoke exposure. Inhalation Toxicol. 15:1029-1038; 2003.
55. Kirkham, P. A., et al. Cigarette smoke triggers macrophage adhesion and activation: role of lipid peroxidation products and scavenger receptor. Free Radic. Biol. Med. 35:697-710; 2003.
56. Rahman, I., 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. 166:490-495; 2002.
57. Mandal, M., et al. Epithelial to mesenchymal transition in head and neck squamous carcinoma: association of Src activation with E-cadherin down-regulation, vimentin expression, and aggressive tumor features. Cancer 112:2088-2100; 2008.
58. Forman, H. J., et al. The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal. Arch. Biochem. Biophys. 477:183-195; 2008.
59. Schmitt, J. M.; Stork, P. J. Gα and Gβγ require distinct Src-dependent pathways to activate Rap1 and Ras. J. Biol. Chem. 277:43024-43032; 2002.
60. Pierce, K. L., et al. Epidermal growth factor (EGF) receptor-dependent ERK activation by G protein-coupled receptors: a co-culture system for identifying intermediates upstream and downstream of heparin-binding EGF shedding. J. Biol. Chem. 276:23155-23160; 2001.
61. Touyz, R. M., et al. Increased angiotensin II-mediated Src signaling via epidermal growth factor receptor transactivation is associated with decreased C-terminal Src kinase activity in vascular smooth muscle cells from spontaneously hypertensive rats. Hypertension 39:479-485; 2002.
62. Bobe, R., et al. Evidence for ERK1/2 activation by thrombin that is independent of EGFR transactivation. Am. J. Physiol. Heart Circ. Physiol. 285:H745-H754; 2003.
63. Scapoli, L., et al. Src-dependent ERK5 and Src/EGFR-dependent ERK1/2 activation is required for cell proliferation by asbestos. Oncogene 23:805-813; 2004.
64. Li, Z., et al. Src tyrosine kinase inhibitor PP2 suppresses ERK1/2 activation and epidermal growth factor receptor transactivation by X-irradiation. Biochem. Biophys. Res. Commun. 341:363-368; 2006.
65. Cuevas, B., et al. SHP-1 regulates Lck-induced phosphatidylinositol 3-kinase phosphorylation and activity. J. Biol. Chem. 274:27583-27589; 1999.
66. Li, Y., et al. The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3β and β-catenin. J. Biol. Chem. 276: 6061-6064; 2001.
67. Fukazawa, H.; Mizuno, S.; Uehara, Y. Effects of herbimycin A and various SHreagents on p60v-src kinase activity in vitro. Biochem. Biophys. Res. Commun. 173:276-282; 1990.
68. Akhand, A. A., et al. Nitric oxide controls src kinase activity through a sulfhydryl group modification-mediated Tyr-527-independent and Tyr-416-linked mechanism. J. Biol. Chem. 274:25821-25826; 1999.
69. Krasnowska, E. K., et al. N-acetyl-L-cysteine fosters inactivation and transfer to endolysosomes of c-Src. Free Radic. Biol. Med. 45:1566-1572; 2008.
70. Oo, M. L., et al. Cysteine residues in the C-terminal lobe of Src: their role in the suppression of the Src kinase. Oncogene 22:1411-1417; 2003.
71. Cheng, S. E., et al. Cigarette smoke extract regulates cytosolic phospholipase A2 expression via NADPH oxidase/MAPKs/AP-1 and p300 in human tracheal smooth muscle cells. Free Radic. Biol. Med. 46:948-996; 2009.
72. Kemble, D. J.; Sun, G. Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation. Proc. Natl. Acad. Sci. USA 106:5070-5075; 2009.
73. 2+ influx following store depletion in HEK 293 cells. Cell Calcium 40:1-10; 2006.
74. 2 regulates the activation of distinct MAPK pathways. Free Radic. Biol. Med. 33:1121-1132; 2002.
75. Boivin, B., et al. A modified cysteinyl-labeling assay reveals reversible oxidation of protein tyrosine phosphatases in angiomyolipoma cells. Proc. Natl. Acad. Sci. USA 105:9959-9964; 2008.
76. Mills, J. E., et al. A novel disulfide bond in the SH2 domain of the C-terminal Src kinase controls catalytic activity. J. Mol. Biol. 365:1460-1468; 2007.