Protective effect of luteolin on cigarette smoke extract-induced cellular toxicity and apoptosis in normal human bronchial epithelial cells via the Nrf2 pathway

Oncology Reports

Volumn 31, Issue 4, 2014, Pages 1855-1862

  Tan, Xiaobin ^a   Jin, Ping ^a,b   Feng, Liang ^a   Song, Jie ^a   Sun, E ^a   Liu, Wenbo ^a   Shu, Luan ^a   Jia, Xiaobin ^a  

^a Key Laboratory of New Drug Delivery System of Chinese Materia Medica Jiangsu Provincial Academy of Chinese Medicine ^*  (China)

^b HUAIHUA MEDICAL COLLEGE   (China)

Author keywords

Apoptosis; Chemoprevention; Cigarette smoking; Lung cancer; Luteolin; NF E2 related factor 2

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; CIGARETTE SMOKE; GLUTATHIONE; HEME OXYGENASE 1; LUTEOLIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE) 1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BRONCHUS MUCOSA; CELL DAMAGE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVATION; EPITHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTIOXIDANTS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE; EPITHELIAL CELLS; FLOW CYTOMETRY; HUMANS; LUTEOLIN; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RESPIRATORY MUCOSA; SMOKE; TOBACCO;

EID: 84908129695     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2014.3007     Document Type: Article

References (43)

1. Jemal A, Bray F, Center MM, et al: Global cancer statistics. CA Cancer J Clin 61: 69-90, 2011.
2. Siegel R, Naishadham D and Jemal A: Cancer statistics 2013. CA Cancer J Clin 63: 11-30, 2013.
3. Nakayama T, Kaneko M, Kodama M and Nagata C: Cigarette smoke induces DNA single-strand breaks in human cells. Nature 314: 462-464, 1985.
4. Nyunoya T, Monick MM, Klingelhutz A, et al: Cigarette smoke induces cellular senescence. Am J Respir Cell Mol Biol 35: 681-688, 2006.
5. Carnevali S, Petruzzelli S, Longoni B, et al: Cigarette smoke extract induces oxidative stress and apoptosis in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 284: L955-L963, 2003.
6. Baglole CJ, Bushinsky SM, Garcia TM, et al: Differential induction of apoptosis by cigarette smoke extract in primary human lung fibroblast strains: implications for emphysema. Am J Physiol Lung Cell Mol Physiol 291: L19-L29, 2006.
7. Kensler TW, Wakabayashi N and Biswal S: Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
8. So HS, Kim HJ, Lee JH, et al: Flunarizine induces Nrf2-mediated transcriptional activation of heme oxygenase-1 in protection of auditory cells from cisplatin. Cell Death Differ 13: 1763-1775, 2006.
9. Leiser SF and Miller RA: Nrf2 signaling a mechanism for cellular stress resistance in long-lived mice. Mol Cell Biol 30: 871-884, 2010.
10. Thimmulappa RK, Mai KH, Srisuma S, et al: Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62: 5196-5203, 2002.
11. Hayashi A, Suzuki H, Itoh K, et al: Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance- associated protein 1 in mouse embryo fibroblasts. Biochem Biophys Res Commun 310: 824-829, 2003.
12. Ko WG, Kang TH, Lee SJ, et al: Effects of luteolin on the inhibition of proliferation and induction of apoptosis in human myeloid leukaemia cells. Phytother Res 16: 295-298, 2002.
13. Lee HZ, Wu CH and Chang SP: Release of nucleophosmin from the nucleus: involvement in aloe-emodin-induced human lung non small carcinoma cell apoptosis. Int J Cancer 113: 971-976, 2005.
14. Huang YT, Hwang JJ, Lee PP, et al: Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on cell growth and metastasis-associated properties in A43 cells over expressing epidermal growth factor receptor. Br J Pharmacol 128: 999-1010, 1999.
15. Leung HW, Wu CH, Lin CH and Lee HZ: Luteolin induced DNA damage leading to human lung squamous carcinoma CH27 cell apoptosis. Eur J Pharmacol 508: 77-83, 2005.
16. Bagli E, Stefaniotou M, Morbidelli L, et al: Luteolin inhibits vascular endothelial growth factor-induced angiogenesis; inhibition of endothelial cell survival and proliferation by targeting phosphatidylinositol 3′-kinase activity. Cancer Res 64: 7936-7946, 2004.
17. Lin Y, Shi R, Wang X and Shen HM: Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr Cancer Drug Targets 8: 634-646, 2008.
18. Tang X, Wang H, Fan L, et al: Luteolin inhibits Nrf2 leading to negative regulation of the Nrf2/ARE pathway and sensitization of human lung carcinoma A549 cells to therapeutic drugs. Free Radic Biol Med 50: 1599-1609, 2011.
19. Balamurugan K and Karthikeyan J: Evaluation of luteolin in the prevention of N-nitrosodiethylamine-induced hepatocellular carcinoma using animal model system. Indian J Clin Biochem 27: 157-163, 2012.
20. Smelter DF, Sathish V, Thompson MA, et al: Thymic stromal lymphopoietin in cigarette smoke-exposed human airway smooth muscle. J Immunol 185: 3035-3040, 2010.
21. Hudy MH, Traves SL, Wiehler S and Proud D: Cigarette smoke modulates rhinovirus induced airway epithelial chemokine production. Eur Respir J 35: 1256-1263, 2010.
22. Albino AP, Huang X, Jorgensen ED, et al: Induction of DNA double-strand breaks in A549 and normal human pulmonary epithelial cells by cigarette smoke is mediated by free radicals. Int J Oncol 28: 1491-1505, 2006.
23. Cheng SE, Lee IT, Lin CC, et al: Cigarette smoke particle-phase extract induces HO-1 expression in human tracheal smooth muscle cells: role of the c-Src/NADPH oxidase/MAPK/Nrf2 signaling pathway. Free Radic Biol Med 48: 1410-1422, 2010.
24. Pryor WA and Stone K: Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann NY Acad Sci 686: 12-27, 1993.
25. Newcomb PA and Carbone PP: The health consequences of smoking. Cancer Med Clin North Am 76: 305-311, 1992.
26. Thun MJ, Henley SJ and Calle EE: Tobacco use and cancer: an epidemiologic perspective for geneticists. Oncogene 21: 7307-7325, 2002.
27. Poulsen HE, Prieme H and Loft S: Role of oxidative DNA damage in cancer initiation and promotion. Eur J Cancer Prev 7: 9-16, 1998.
28. Prasad KN and Edwards-Prasad J: Vitamin E and cancer prevention: recent advances and future potentials. J Am Coll Nutr 11: 487-500, 1992.
29. Banerjee S, Chattopadhyay R, Ghosh A, et al: Cellular and molecular mechanisms of cigarette smoke-induced lung damage and prevention by vitamin C. J Inflamm 11: 5-21, 2008.
30. Lannan S, Donaldson K, Brown D, et al: Effects of cigarette smoke and its condensates on alveolar epithelial cell injury in vitro. Am J Physiol 266: 92-100, 1994.
31. Nakamura Y, Romberger DJ, Tate L, et al: Cigarette smoke inhibits lung fibroblast proliferation and chemotaxis. Am J Respir Crit Care Med 151: 1497-1503, 1995.
32. van der Vaart H, Postma DS, Timens W and ten Hacken NH: Acute effects of cigarette smoke on inflammation and oxidative stress: a review. Thorax 59: 713-721, 2004.
33. Deslee G, Adair-Kirk TL, Betsuyaku T, et al: Cigarette smoke induces nucleic-acid oxidation in lung fibroblasts. Am J Respir Cell Mol Biol 43: 576-584, 2010.
34. Messner B, Frotschnig S, Steinacher-Nigisch A, et al: Apoptosis and necrosis: two different outcomes of cigarette smoke condensate-induced endothelial cell death. Cell Death Dis 3: e424, 2012.
35. Pan J, Zhang Q, Wang Y and You M: 226S proteasome activity is down-regulated in lung cancer stem-like cells propagated in vitro. PLoS One 5: e13298, 2010.
36. Comer DM, Kidney JC, Ennis M and Elborn JS: Airway epithelial cell apoptosis and inflammation in COPD, smokers and nonsmokers. Eur Respir J 41: 1058-1067, 2013.
37. Pandurangan AK, Ananda Sadagopan SK, Dharmalingam P and Ganapasam S: Luteolin, a bioflavonoid inhibits Azoxymethane-induced colorectal cancer through activation of Nrf2 signaling. Toxicol Mech Methods: Oct 7, 2013 (Epub ahead of print).
38. Huang CS, Lii CK, Lin AH, et al: Protection by chrysin, apigenin, and luteolin against oxidative stress is mediated by the Nrf2-dependent up-regulation of heme oxygenase 1 and glutamate cysteine ligase in rat primary hepatocytes. Arch Toxicol 87: 167-178, 2013.
39. Florczyk U, Łoboda A, Stachurska A, et al: Role of Nrf2 transcription factor in cellular response to oxidative stress. Postepy Biochem 56: 147-155, 2010 (In Polish).
40. Su ZY, Shu L, Khor TO, et al: A perspective on dietary phytochemicals and cancer chemoprevention: oxidative stress, nrf2, and epigenomics. Top Curr Chem 329: 133-162, 2013.
41. Shinkai Y, Sumi D, Fukami I, et al: Sulforaphane, an activator of Nrf2, suppresses cellular accumulation of arsenic and its cytotoxicity in primary mouse hepatocytes. FEBS Lett 580: 1771-1774, 2006.
42. Osburn WO and Kensler TW: Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat Res 659: 31-39, 2008.
43. Du Y, Villeneuve NF, Wang XJ, et al: Oridonin confers protection against arsenic-induced toxicity through activation of the Nrf2-mediated defensive response. Environ Health Perspect 116: 1154-1161, 2008.