Grape seed proanthocyanidins inhibit cigarette smoke condensate-induced lung cancer cell migration through inhibition of NADPH oxidase and reduction in the binding of p22phox and p47phox proteins

Molecular Carcinogenesis

Volumn 54, Issue S1, 2015, Pages E61-E71

  Vaid, Mudit ^a   Katiyar, Santosh K ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Cancer cell migration; Cigarette smoke condensate; Lung cancer cells; NADPH oxidase; Oxidative stress; Proanthocyanidins

Indexed keywords

CIGARETTE SMOKE CONDENSATE; PROANTHOCYANIDIN; PROTEIN P22; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; CYBA PROTEIN, HUMAN; GRAPE SEED EXTRACT; GRAPE SEED PROANTHOCYANIDINS; NEUTROPHIL CYTOSOLIC FACTOR 1; PROTEIN BINDING; SMOKE;

A549 CELL LINE; ARTICLE; ASSAY; CELL MIGRATION; CONTROLLED STUDY; ENZYME INHIBITION; GRAPE; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG CANCER CELL LINE; OXIDATIVE STRESS; PLANT SEED; PRIORITY JOURNAL; PROTEIN BINDING; SMOKING; ADVERSE EFFECTS; ANTAGONISTS AND INHIBITORS; CELL MOTION; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; LUNG TUMOR; METABOLISM; NEOPLASM METASTASIS; NON SMALL CELL LUNG CANCER; PATHOLOGY; SMOKE; TOBACCO; TUMOR CELL LINE;

VITACEAE;

CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; GRAPE SEED EXTRACT; HUMANS; LUNG NEOPLASMS; NADPH OXIDASE; NEOPLASM METASTASIS; OXIDATIVE STRESS; PROANTHOCYANIDINS; PROTEIN BINDING; SMOKE; TOBACCO;

EID: 84931031336     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22173     Document Type: Article

References (39)

1. Iyer S, Roughley A, Rider A, Taylor-Stokes G. The symposium burden of non-small cell lung cancer in the USA: A real-world cross-sectional study. Support Care Cancer 2014; 22:181-187.
2. Ferrigno D, Buccheri G. Second-line chemotherapy for recurrent non-small cell lung cancer: Do new agents make a difference? Lung Cancer 2000; 29:91-104.
3. Blot WJ, Fraumeni JF Jr. Cancers of the lung and pleura. In: Schottenfeld D, Fraumeni J Jr, editors. Cancer epidemiology and prevention. New York (NY): Oxford University Press; 1996. pp. 637-665.
4. Surgeon General. Reducing the health consequences of smoking: 25 years of progress. Washington (DC): U.S. Gov Print Off; 1989.
5. Shopland DR. Tobacco use and its contribution to early cancer mortality with a special emphasis on cigarette smoking. Environ Health Perspect 1995; 103:131-142.
6. Rodgman A, Perfetti TA. The chemical compounds of tobacco and tobacco smoke. Boca Raton, London, NY: CRC Press; 2009.
7. Nakayama T, Kaneko M, Kodama M, Nagata C. Cigarette smoke induces DNA single-strand breaks in human cells. Nature 1985; 314:462-464.
8. Müller T, Haussmann HJ, Schepers G. Evidence for peroxynitrite as an oxidative stress-inducing compound of aqueous cigarette smoke fractions. Carcinogenesis 1997; 18:295-301.
9. Squadrito GL, Pryor WA. Oxidative chemistry of nitric oxide: The roles of superoxide, peroxynitrite, and carbon dioxide. Free Radic Biol Med 1998; 25:392-403.
10. Fang J, Seki T, Maeda H. Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Adv Drug Deliv Rev 2009; 61:290-302.
11. Khandrika L, Kumar B, Koul S, Maroni P, Koul HK. Oxidative stress in prostate cancer. Cancer Lett 2009; 282:125-136.
12. Danno K, Horio T, Takigawa M, Imamura S. Role of oxygen intermediates in UV-induced epidermal cell injury. J Invest Dermatol 1984; 83:166-168.
13. Punnonen K, Autio P, Kiistala U, Ahotupa M. In-vivo effects of solar-simulated ultraviolet irradiation on antioxidant enzymes and lipid peroxidation in human epidermis. Br J Dermatol 1991; 125:18-20.
14. Visconti R, Grieco D. New insights on oxidative stress in cancer. Curr Opin Drug Discov Devel 2009; 12:240-245.
15. Nagathihalli NS, Massion PP, Gonzalez AL, Lu P, Datta PK. Smoking induces epithelial-to-mesenchymal transition in non-small cell lung cancer through HDAC-mediated downregulation of E-cadherin. Mol Cancer Ther 2012; 11:2362-2372.
16. Zhao Y, Xu Y, Li Y, et al. NF-κB-mediated inflammation leading to EMT via miR-200c is involved in cell transformation induced by cigarette smoke extract. Toxicol Sci 2013; 135:265-276.
17. Zhang H, Liu H, Borok Z, Davies KJA, Ursini F, Forman HJ. Cigarette smoke extract stimulates epithelial-mesenchymal transition through Src activation. Free Radic Biol Med 2012; 52:1437-1442.
18. Maffei-Facino R, Carini M, Aldini G, et al. Procyanidines from Vitis vinifera seeds protect rabbit heart from ischemia/reperfusion injury: Antioxidant intervention and/or iron and copper sequestering ability. Planta Med 1996; 62:495-502.
19. Bagchi D, Garg A, Krohn RL, Bagchi M, Tran MX, Stohs SJ. Oxygen free radical scavenging abilities of vitamin C and E and a grape seed proanthocyanidin extract in vitro. Res Commun Mol Pathol Pharmacol 1997; 95:179-189.
20. Sharma SD, Meeran SM, Katiyar SK. Dietary grape seed proanthocyanidins inhibit UVB-induced oxidative stress and activation of mitogen-activated protein kinases and nuclear factor-κB signaling in in vivo SKH-1 hairless mice. Mol Cancer Ther 2007; 6:995-1005.
21. Mittal A, Elmets CA, Katiyar SK. Dietary feeding of proanthocyanidins from grape seeds prevents photocarcinogenesis in SKH-1 hairless mice: Relationship to decreased fat and lipid peroxidation. Carcinogenesis 2003; 24:1379-1388.
22. Sharma SD, Meeran SM, Katiyar SK. Proanthocyanidins inhibit in vitro and in vivo growth of human non-small cell lung cancer cells by inhibiting the prostaglandin E(2) and prostaglandin E(2) receptors. Mol Cancer Ther 2010; 3:569-580.
23. Akhtar S, Meeran SM, Katiyar N, Katiyar SK. Grape seed proanthocyanidins inhibit the growth of human non-small cell lung cancer xenografts by targeting insulin-like growth factor binding protein-3, tumor cell proliferation, and angiogenic factors. Clin Cancer Res 2009; 3:821-831.
24. Punathil T, Katiyar SK. Inhibition of non-small cell lung cancer cell migration by grape seed proanthocyanidins is mediated through the inhibition of nitric oxide, guanylate cyclase, and ERK1/2. Mol Carcinog 2009; 3:232-242.
25. Mai Y, Higashi T, Terada K, et al. Nicotine- and tar-free cigarette smoke extract induces cell injury via intracellular Ca2+-dependent subtype-specific protein kinase C activation. J Pharmacol Sci 2012; 120:310-314.
26. Asano H, Horinouchi T, Mai Y, et al. Nicotine- and tar-free cigarette smoke induces cell damage through reactive oxygen species newly generated by PKC-dependent activation of NADPH oxidase. J Pharmacol Sci 2012; 118:275-287.
27. Roemer E, Schramke H, Weiler H, et al. Mainstream smoke chemistry and in vitro and in vivo toxicity of the reference cigarettes 3R4F and 2R4F. Beitr Tabakforsch Int 2012; 25:316-335.
28. Liu C, Feng S, van Heemst J, McAdam KG. New insights into the formation of volatile compounds in mainstream cigarette smoke. Anal Bioanal Chem 2010; 396:1817-1830.
29. Lee TJ, Kim EJ, Kim S, et al. Caspase-dependent and caspase-independent apoptosis induced by evodiamine in human leukemic U937 cells. Mol Cancer Ther 2006; 9:2398-2407.
30. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2′, 7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992; 5:227-231.
31. phox binding. J Biol Chem 2010; 285:2959-2967.
32. Nauseef WM. Assembly of the phagocyte NADPH oxidase. Histochem Cell Biol 2004; 122:277-291.
33. Thiery JP. Epithelial-mesenchymal transitions in tumor progression. Nat Rev Cancer 2002; 2:442-454.
34. Sun Q, Prasad R, Rosenthal E, Katiyar SK. Grape seed proanthocyanidins inhibit the invasive potential of human HNSCC cells by targeting EGFR and the epithelial-to-mesenchymal transition. PLoS ONE 2012; 7:e31093.
35. IARC. Tobacco smoke and involuntary smoking. In: IARC monographs on the evaluation of carcinogenic risks to humans. Lyon: IARC Press; 2004, Vol. 83, pp 53-119.
36. Hecht SS. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 1999; 91:1194-1210.
37. Ilonen IK, Räsänen JV, Sihvo EI, et al. Oxidative stress in non-small cell lung cancer: Role of nicotinamide adenine dinucleotide phosphate oxidase and glutathione. Acta Oncol 2009; 48:1054-1061.
38. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJ, Banerjee A, Silliman CC. Structural organization of the neutrophil NADPH oxidase: Phosphorylation and translocation during priming and activation. J Leukoc Biol 2005; 78:1025-1042.
39. Cannito S, Novo E, di Bonzo LV, Busletta C, Colombatto S, Parola M. Epithelial-mesenchymal transition: From molecular mechanisms, redox regulation to implications in human health and disease. Antioxid Redox Signal 2010; 12:1383-1430.