Mitochondrial reactive oxygen species mediates nicotine-induced hypoxia-inducible factor-1α expression in human non-small cell lung cancer cells

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 6, 2012, Pages 852-861

  Guo, Lili ^a   Li, Lin ^a   Wang, Weiqiang ^a   Pan, Zhenhua ^a   Zhou, Qinghua ^a   Wu, Zhihao ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Hypoxia inducible factor 1 ; Lung cancer metastasis; Mitochondria; Nicotine; Reactive oxygen species

Indexed keywords

CATALASE; DIHYDRO BETA ERYTHROIDINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINE; NICOTINIC RECEPTOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL FUNCTION; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UPREGULATION;

ANOXIA; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DIHYDRO-BETA-ERYTHROIDINE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG NEOPLASMS; MECAMYLAMINE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; NICOTINE; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RECEPTORS, CHOLINERGIC; RNA INTERFERENCE; RNA, SMALL INTERFERING; SMOKING; TRANSCRIPTION, GENETIC;

EID: 84858983379     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.02.004     Document Type: Article

References (45)

1. Tyson L.B. Non-small cell lung cancer: new hope for a chronic illness. Oncol. Nurs. Forum 2007, 34(5):963-970.
2. MacKinnon A.C., Kopatz J., Sethi T. The molecular and cellular biology of lung cancer: identifying novel therapeutic strategies. Br. Med. Bull. 2010, 95:47-61.
3. Pesch B., Kendzia B., Gustavsson P., Jockel K.H., Johnen G., Pohlabeln H., Olsson A., Ahrens W., Gross I.M., Bruske I., et al. Cigarette smoking and lung cancer-relative risk estimates for the major histological types from a pooled analysis of case-control studies. Int. J. Cancer Nov. 2 2011, [Electronic publication ahead of print], doi: 10.1002/ijc.27339.
4. Dasgupta P., Rastogi S., Pillai S., Ordonez-Ercan D., Morris M., Haura E., Chellappan S. Nicotine induces cell proliferation by beta-arrestin-mediated activation of Src and Rb-Raf-1 pathways. J. Clin. Invest. 2006, 116(8):2208-2217.
5. Dasgupta P., Rizwani W., Pillai S., Kinkade R., Kovacs M., Rastogi S., Banerjee S., Carless M., Kim E., Coppola D., et al. Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int. J. Cancer 2009, 124(1):36-45.
6. Yoshino I., Kometani T., Shoji F., Osoegawa A., Ohba T., Kouso H., Takenaka T., Yohena T., Maehara Y. Induction of epithelial-mesenchymal transition-related genes by benzo[a]pyrene in lung cancer cells. Cancer 2007, 110(2):369-374.
7. Thunnissen F.B. Acetylcholine receptor pathway and lung cancer. J. Thorac. Oncol. 2009, 4(8):943-946.
8. Egleton R.D., Brown K.C., Dasgupta P. Nicotinic acetylcholine receptors in cancer: multiple roles in proliferation and inhibition of apoptosis. Trends Pharmacol. Sci. 2008, 29(3):151-158.
9. Yildiz D. Nicotine, its metabolism and an overview of its biological effects. Toxicon 2004, 43(6):619-632.
10. Crowley-Weber C.L., Dvorakova K., Crowley C., Bernstein H., Bernstein C., Garewal H., Payne C.M. Nicotine increases oxidative stress, activates NF-kappaB and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem. Biol. Interact. 2003, 145(1):53-66.
11. Nguyen D.X., Massague J. Genetic determinants of cancer metastasis. Nat. Rev. Genet. 2007, 8(5):341-352.
12. Sullivan R., Graham C.H. Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev. 2007, 26(2):319-331.
13. Brown J.M., Wilson W.R. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. 2004, 4(6):437-447.
14. Dewhirst M.W., Cao Y., Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat. Rev. 2008, 8(6):425-437.
15. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. 2003, 3(10):721-732.
16. Galanis A., Pappa A., Giannakakis A., Lanitis E., Dangaj D., Sandaltzopoulos R. Reactive oxygen species and HIF-1 signalling in cancer. Cancer Lett. 2008, 266(1):12-20.
17. Bell E.L., Emerling B.M., Chandel N.S. Mitochondrial regulation of oxygen sensing. Mitochondrion 2005, 5(5):322-332.
18. Zhang Q., Tang X., Zhang Z.F., Velikina R., Shi S., Le A.D. Nicotine induces hypoxia-inducible factor-1alpha expression in human lung cancer cells via nicotinic acetylcholine receptor-mediated signaling pathways. Clin. Cancer Res. 2007, 13(16):4686-4694.
19. Wu Z., Lauer T.W., Sick A., Hackett S.F., Campochiaro P.A. Oxidative stress modulates complement factor H expression in retinal pigmented epithelial cells by acetylation of FOXO3. J. Biol. Chem. 2007, 282(31):22414-22425.
20. Mai W., Kawakami K., Shakoori A., Kyo S., Miyashita K., Yokoi K., Jin M., Shimasaki T., Motoo Y., Minamoto T. Deregulated GSK3{beta} sustains gastrointestinal cancer cells survival by modulating human telomerase reverse transcriptase and telomerase. Clin. Cancer Res. 2009, 15(22):6810-6819.
21. Hu R., Kim B.R., Chen C., Hebbar V., Kong A.N. The roles of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cells. Carcinogenesis 2003, 24(8):1361-1367.
22. Steiner R.C., Heath C.J., Picciotto M.R. Nicotine-induced phosphorylation of ERK in mouse primary cortical neurons: evidence for involvement of glutamatergic signaling and CaMKII. J. Neurochem. 2007, 103(2):666-678.
23. Gao N., Ding M., Zheng J.Z., Zhang Z., Leonard S.S., Liu K.J., Shi X., Jiang B.H. Vanadate-induced expression of hypoxia-inducible factor 1 alpha and vascular endothelial growth factor through phosphatidylinositol 3-kinase/Akt pathway and reactive oxygen species. J. Biol. Chem. 2002, 277(35):31963-31971.
24. Wu Z., Rogers B., Kachi S., Hackett S.F., Sick A., Campochiaro P.A. Reduction of p66Shc suppresses oxidative damage in retinal pigmented epithelial cells and retina. J. Cell. Physiol. 2006, 209(3):996-1005.
25. Carter W.O., Narayanan P.K., Robinson J.P. Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J. Leukoc. Biol. 1994, 55(2):253-258.
26. Lu H., Dalgard C.L., Mohyeldin A., McFate T., Tait A.S., Verma A. Reversible inactivation of HIF-1 prolyl hydroxylases allows cell metabolism to control basal HIF-1. J. Biol. Chem. 2005, 280(51):41928-41939.
27. Wang G., Hazra T.K., Mitra S., Lee H.M., Englander E.W. Mitochondrial DNA damage and a hypoxic response are induced by CoCl(2) in rat neuronal PC12 cells. Nucleic Acids Res. 2000, 28(10):2135-2140.
28. Brunelle J.K., Bell E.L., Quesada N.M., Vercauteren K., Tiranti V., Zeviani M., Scarpulla R.C., Chandel N.S. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 2005, 1(6):409-414.
29. Schriner S.E., Linford N.J., Martin G.M., Treuting P., Ogburn C.E., Emond M., Coskun P.E., Ladiges W., Wolf N., Van Remmen H., et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005, 308(5730):1909-1911. New York, NY.
30. Brognard J., Clark A.S., Ni Y., Dennis P.A. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res. 2001, 61(10):3986-3997.
31. Liao D., Corle C., Seagroves T.N., Johnson R.S. Hypoxia-inducible factor-1alpha is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res. 2007, 67(2):563-572.
32. Gort E.H., Groot A.J., van der Wall E., van Diest P.J., Vooijs M.A. Hypoxic regulation of metastasis via hypoxia-inducible factors. Curr. Mol. Med. 2008, 8(1):60-67.
33. Bos R., Zhong H., Hanrahan C.F., Mommers E.C., Semenza G.L., Pinedo H.M., Abeloff M.D., Simons J.W., van Diest P.J., van der Wall E. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J. Natl. Cancer Inst. 2001, 93(4):309-314.
34. Birner P., Schindl M., Obermair A., Plank C., Breitenecker G., Oberhuber G. Overexpression of hypoxia-inducible factor 1alpha is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Res. 2000, 60(17):4693-4696.
35. Mansfield K.D., Guzy R.D., Pan Y., Young R.M., Cash T.P., Schumacker P.T., Simon M.C. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab. 2005, 1(6):393-399.
36. Guzy R.D., Hoyos B., Robin E., Chen H., Liu L., Mansfield K.D., Simon M.C., Hammerling U., Schumacker P.T. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005, 1(6):401-408.
37. Sanjuan-Pla A., Cervera A.M., Apostolova N., Garcia-Bou R., Victor V.M., Murphy M.P., McCreath K.J. A targeted antioxidant reveals the importance of mitochondrial reactive oxygen species in the hypoxic signaling of HIF-1alpha. FEBS Lett. 2005, 579(12):2669-2674.
38. Wetscher G.J., Bagchi M., Bagchi D., Perdikis G., Hinder P.R., Glaser K., Hinder R.A. Free radical production in nicotine treated pancreatic tissue. Free Radic. Biol. Med. 1995, 18(5):877-882.
39. Loft S., Astrup A., Buemann B., Poulsen H.E. Oxidative DNA damage correlates with oxygen consumption in humans. FASEB J. 1994, 8(8):534-537.
40. Gvozdjakova A., Kucharska J., Gvozdjak J. Effect of smoking on the oxidative processes of cardiomyocytes. Cardiology 1992, 81(2-3):81-84.
41. Bruin J.E., Petre M.A., Lehman M.A., Raha S., Gerstein H.C., Morrison K.M., Holloway A.C. Maternal nicotine exposure increases oxidative stress in the offspring. Free Radic. Biol. Med. 2008, 44(11):1919-1925.
42. West K.A., Brognard J., Clark A.S., Linnoila I.R., Yang X., Swain S.M., Harris C., Belinsky S., Dennis P.A. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J. Clin. Invest. 2003, 111(1):81-90.
43. Zheng Y., Ritzenthaler J.D., Roman J., Han S. Nicotine stimulates human lung cancer cell growth by inducing fibronectin expression. Am. J. Respir. Cell Mol. Biol. 2007, 37(6):681-690.
44. Peng X.H., Karna P., Cao Z., Jiang B.H., Zhou M., Yang L. Cross-talk between epidermal growth factor receptor and hypoxia-inducible factor-1alpha signal pathways increases resistance to apoptosis by up-regulating survivin gene expression. J. Biol. Chem. 2006, 281(36):25903-25914.
45. Gao P., Zhang H., Dinavahi R., Li F., Xiang Y., Raman V., Bhujwalla Z.M., Felsher D.W., Cheng L., Pevsner J., et al. HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell 2007, 12(3):230-238.