Benzo(a)pyrene induced lung cancer: Role of dietary phytochemicals in chemoprevention

Pharmacological Reports

Volumn 67, Issue 5, 2015, Pages 996-1009

  Kasala, Eshvendar Reddy ^a   Bodduluru, Lakshmi Narendra ^a   Barua, Chandana C ^b   Sriram, Chandra Shekhar ^a   Gogoi, Ranadeep ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

^b ASSAM AGRICULTURAL UNIVERSITY   (India)

Author keywords

Benzo(a)pyrene; Chemoprevention; Dietary phytochemicals; Lung cancer

Indexed keywords

BENZO[A]PYRENE; PLANT MEDICINAL PRODUCT; TOBACCO SMOKE; ANTINEOPLASTIC AGENT; CARCINOGEN;

CHEMOPROPHYLAXIS; DIET SUPPLEMENTATION; DNA ADDUCT; HUMAN; LUNG CANCER; LUNG CARCINOGENESIS; MICROENVIRONMENT; NONHUMAN; REVIEW; TUMOR GROWTH; TUMOR PROMOTION; ANIMAL; CHEMICALLY INDUCED; DIET; LUNG NEOPLASMS; PATHOLOGY;

ANIMALS; ANTICARCINOGENIC AGENTS; BENZO(A)PYRENE; CARCINOGENS; CHEMOPREVENTION; DIET; HUMANS; LUNG NEOPLASMS; PHYTOCHEMICALS;

EID: 84940024091     PISSN: 22995684     EISSN: 22995684     Source Type: Journal    
DOI: 10.1016/j.pharep.2015.03.004     Document Type: Review

References (131)

1. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J Clin 61 2011 69 90
2. J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, and et al. GLOBOCAN 2012 v1.0, cancer incidence and mortality worldwide: IARC Cancer Base No. 11 2013 International Agency for Research on Cancer Lyon, France [accessed 03.11.14]
3. World Health Organization Global cancer rates could increase by 50% to 15 million by 2020 2003 World Cancer Report Geneva
4. D. Hoffmann, I. Hoffmann, and K. El-Bayoumy The less harmful cigarette: a controversial issue. A tribute to Ernst L. Wynder Chem Res Toxicol 14 7 2001 767 790
5. D.H. Phillips Polycyclic aromatic hydrocarbons in the diet Mutat Res 443 1-2 1999 139 147
6. D.H. Phillips Smoking-related DNA and protein adducts in human tissues Carcinogenesis 23 12 2002 1979 2004
7. International Agency for Research on Cancer IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans vol. 32 1983 IARC Lyon, France 211 224
8. S. Ellard, Y. Mohammed, S. Dogra, C. Wölfel, J. Doehmer, and J.M. Parry The use of genetically engineered V79 Chinese hamster cultures expressing rat liver CYP1A1, 1A2 and 2B1 cDNAs in micronucleus assays Mutagenesis 6 6 1991 461 470
9. D.W. Nebert The Ah locus: genetic differences in toxicity, cancer, mutation, and birth defects Crit Rev Toxicol 20 3 1989 153 174
10. A. Besaratinia, and G.P. Pfeifer Enhancement of the mutagenicity of benzo(a)pyrene diol epoxide by a nonmutagenic dose of ultraviolet A radiation Cancer Res 63 24 2003 8708 8716
11. Y.J. Surh Cancer chemoprevention with dietary phytochemicals Nat Rev Cancer 3 10 2003 768 780
12. V. Cohen, and F.R. Khuri Chemoprevention of lung cancer: current status and future prospects Cancer Metastasis Rev 21 3-4 2002 349 362
13. L.N. Bodduluru, E.R. Kasala, N. Thota, C.C. Barua, and R. Sistla Chemopreventive and therapeutic effects of nimbolide in cancer: the underlying mechanisms Toxicol In Vitro 28 5 2014 1026 1035
14. E.R. Kasala, L.N. Bodduluru, R.M. Madana, A.K. V, R. Gogoi, and C.C. Barua Chemopreventive and therapeutic potential of chrysin in cancer: mechanistic perspectives Toxicol Lett 233 2 2015 214 225
15. G.J. Kelloff, J.A. Crowell, V.E. Steele, R.A. Lubet, W.A. Malone, C.W. Boone, and et al. Progress in cancer chemoprevention: development of diet-derived chemopreventive agents J Nutr 130 2S 2000 467S 471S
16. B.B. Aggarwal, and S. Shishodia Molecular targets of dietary agents for prevention and therapy of cancer Biochem Pharmacol 71 10 2006 1397 1421
17. E.C. Miller Some current perspectives on chemical carcinogenesis in humans and experimental animals: presidential address Cancer Res 38 6 1978 1479 1496
18. R. Sinha, M. Kulldorff, M.J. Gunter, P. Strickland, and N. Rothman Dietary benzo[a]pyrene intake and risk of colorectal adenoma Cancer Epidemiol Biomarkers Prev 14 8 2005 2030 2034
19. J.E. Swauger, T.J. Steichen, P.A. Murphy, and S. Kinsler An analysis of the mainstream smoke chemistry of samples of the US cigarette market acquired between 1995 and 2000 Regul Toxicol Pharmacol 35 2 Pt 1 2002 142 156
20. J. Bartley, J.C. Bartholomew, and M.R. Stampfer Metabolism of benzo(a)pyrene by human epithelial and fibroblastic cells: metabolite patterns and DNA adduct formation J Cell Biochem 18 2 1982 135 148
21. F. Sureau, L. Chinsky, M. Duquesne, A. Laigle, P.Y. Turpin, C. Amirand, and et al. Microspectrofluorimetric study of the kinetics of cellular uptake and metabolization of benzo(a)pyrene in human T 47 D mammary tumor cells: evidence for cytochrome P1450 induction Eur Biophys J 18 5 1990 301 307
22. R. Barhoumi, Y. Mouneimne, K.S. Ramos, S.H. Safe, T.D. Phillips, V.E. Centonze, and et al. Analysis of benzo[a]pyrene partitioning and cellular homeostasis in a rat liver cell line Toxicol Sci 53 2 2000 264 270
23. D.J. Madureira, F.T. Weiss, P. Van Midwoud, D.E. Helbling, S.J. Sturla, and K. Schirmer Systems toxicology approach to understand the kinetics of benzo(a)pyrene uptake, biotransformation, and DNA adduct formation in a liver cell model Chem Res Toxicol 27 3 2014 443 453 10.1021/tx400446q
24. J.E. Klaunig, and L.M. Kamendulis Chemical carcinogenesis Casarett & Doull's toxicology: the basic science of poisons 7th ed. 2007 McGraw-Hill New York 329 380 [chapter 8]
25. A. Luch Nature and nurture - lessons from chemical carcinogenesis Nat Rev Cancer 5 2 2005 113 125
26. G.M. Williams Mechanisms of chemical carcinogenesis and application to human cancer risk assessment Toxicology 166 1-2 2001 3 10
27. L.G. Hernández, H. van Steeg, M. Luijten, and J. van Benthem Mechanisms of non-genotoxic carcinogens and importance of a weight of evidence approach Mutat Res 682 2-3 2009 94 109
28. S.S. Hecht Biochemistry, biology, and carcinogenicity of tobacco-specific N-nitrosamines Chem Res Toxicol 11 6 1998 559 603
29. D.A. Tuveson, and T. Jacks Modeling human lung cancer in mice: similarities and shortcomings Oncogene 18 38 1999 5318 5324
30. N. Wakamatsu, T.R. Devereux, H.H. Hong, and R.C. Sills Overview of the molecular carcinogenesis of mouse lung tumor models of human lung cancer Toxicol Pathol 35 1 2007 75 80
31. M. You, Y. Wang, G. Stoner, L. You, R. Maronpot, S.H. Reynolds, and et al. Parental bias of Ki-ras oncogenes detected in lung tumors from mouse hybrids Proc Natl Acad Sci U S A 89 13 1992 5804 5808
32. B. Chen, L. Johanson, J.S. Wiest, M.W. Anderson, and M. You The second intron of the K-ras gene contains regulatory elements associated with mouse lung tumor susceptibility Proc Natl Acad Sci U S A 91 1994 1589 1593
33. S.S. Hecht, F. Kassie, and D.K. Hatsukami Chemoprevention of lung carcinogenesis in addicted smokers and ex-smokers Nat Rev Cancer 9 7 2009 76 488
34. A.M. Malkinson Molecular comparison of human and mouse pulmonary adenocarcinomas Exp Lung Res 24 4 1998 541 555
35. A.E. Bonner, W.J. Lemon, T.R. Devereux, R.A. Lubet, and M. You Molecular profiling of mouse lung tumors: association with tumor progression, lung development, and human lung adenocarcinomas Oncogene 23 5 2003 1166 1176
36. M. You, and G. Bergman Preclinical and clinical models of lung cancer chemoprevention Hematol Oncol Clin North Am 12 5 1998 1037 1053
37. P. Rajendran, G. Ekambaram, and D. Sakthisekaran Protective role of mangiferin against benzo (a) pyrene induced lung carcinogenesis in experimental animals Biol Pharm Bull 31 6 2008 1053 1058
38. M. Panwar, R. Samarth, M. Kumar, W.J. Yoon, and A. Kumar Inhibition of benzo (a) pyrene induced lung adenoma by Panax ginseng extract, EFLA400, in Swiss albino mice Biol Pharm Bull 28 11 2005 2063 2067
39. J. Thyssen, J. Althoff, G. Kimmerle, and U. Mohr Inhalation studies with benzo [a] pyrene in Syrian golden hamsters J Natl Cancer Inst 66 3 1981 575 577
40. A.P. Wolterbeek, E.J. Schoevers, A.A. Rutten, and V.J. Feron A critical appraisal of intratracheal instillation of benzo[a]pyrene to Syrian golden hamsters as a model in respiratory tract carcinogenesis Cancer Lett 89 1 1995 107 116
41. Y. Yan, Y. Wang, Q. Tan, R.A. Lubet, and M. You Efficacy of deguelin and silibinin on benzo(a)pyrene-induced lung tumorigenesis in A/J mice Neoplasia 7 12 2005 1053 1057
42. S.S. Hecht, P.M.J. Kenney, M. Wang, N. Trushin, S. Agarwal, A.V. Rao, and et al. Evaluation of butylated hydroxyanisole, myo-inositol, curcumin, esculetin, resveratrol and lycopene as inhibitors of benzo [a] pyrene plus 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced lung tumorigenesis in A/J mice Cancer Lett 137 2 1999 123 130
43. K.P. Miller, and K.S. Ramos Impact of cellular metabolism on the biological effects of benzo [a] pyrene and related hydrocarbons Drug Metab Rev 33 1 2001 1 35
44. H.V. Gelboin Benzo [alpha] pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes Physiol Rev 60 4 1980 1107 1166
45. W.M. Baird, and S.L. Ralston Carcinogenic polycyclic aromatic hydrocarbons Compr Toxicol 12 1997 171 200
46. L.C.J. Gillet, and O.D. Schärer Molecular mechanisms of mammalian global genome nucleotide excision repair Chem Rev 106 2 2006 253 276
47. L. Cheng, M.R. Spitz, W.K. Hong, and Q. Wei Reduced expression levels of nucleotide excision repair genes in lung cancer: a case-control analysis Carcinogenesis 21 8 2000 1527 1530
48. Y. Zhang, X. Wu, D. Guo, O. Rechkoblit, N.E. Geacintov, and Z. Wang Two-step error-prone bypass of the (+)- and (-)-trans-anti-BPDE-N2-dG adducts by human DNA polymerases eta and kappa Mutat Res 510 1-2 2002 23 35
49. G.P. Pfeifer, M.F. Denissenko, M. Olivier, N. Tretyakova, S.S. Hecht, and P. Hainaut Tobacco smoke carcinogens, DNA damage and p 53 mutations in smoking-associated cancers Oncogene 21 48 2002 35 51
50. K.R.K. Sticha, M.E. Staretz, M. Wang, H. Liang, P.M.J. Kenney, and S.S. Hecht Effects of benzyl isothiocyanate and phenethyl isothiocyanate on benzo [a] pyrene metabolism and DNA adduct formation in the A/J mouse Carcinogenesis 21 9 2000 1711 1719
51. S.S. Hecht Tobacco smoke carcinogens and lung cancer J Natl Cancer Inst 91 14 1999 1194 1210
52. D.C. Spink, B.H. Katz, M.M. Hussain, B.C. Spink, S.J. Wu, N. Liu, and et al. Induction of CYP1A1 and CYP1B1 in T-47D human breast cancer cells by benzo [a] pyrene is diminished by arsenite Drug Metab Dispos 30 3 2002 262 269
53. W.M. Baird, L.A. Hooven, and B. Mahadevan Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action Environ Mol Mutagen 45 2-3 2005 106 114
54. N.Z. Jin, Y.P. Zhu, J.W. Zhou, L. Mao, R.C. Zhao, T.H. Fang, and et al. Preventive effects of quercetin against benzo [a] pyrene-induced DNA damages and pulmonary precancerous pathologic changes in mice Basic Clin Pharmacol Toxicol 98 6 2006 593 598
55. U. Hoffmann, and H.K. Kroemer The ABC transporters MDR1 and MRP2: multiple functions in disposition of xenobiotics and drug resistance Drug Metab Rev 36 3-4 2004 669 701
56. B. Ebert, A. Seidel, and A. Lampen Identification of BCRP as transporter of benzo [a] pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists Carcinogenesis 26 10 2005 1754 1763
57. S.K. Srivastava, S.C. Watkins, E. Schuetz, and S.V. Singh Role of glutathione conjugate efflux in cellular protection against benzo[a]pyrene-7,8-diol-9,10-epoxide-induced DNA damage Mol Carcinog 33 3 2002 156 162
58. T.M. Penning, M.E. Burczynski, C.-F. Hung, K.D. McCoull, N.T. Palackal, and L.S. Tsuruda Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones Chem Res Toxicol 12 1 1999 1 18
59. R. Garg, S. Gupta, and G.B. Maru Dietary curcumin modulates transcriptional regulators of phase I and phase II enzymes in benzo [a] pyrene-treated mice: mechanism of its anti-initiating action Carcinogenesis 29 5 2008 1022 1032
60. J.W. Lee, and J.H. Kim Activation of the leukotriene B4 receptor 2-reactive oxygen species (BLT2-ROS) cascade following detachment confers anoikis resistance in prostate cancer cells J Biol Chem 288 42 2013 30054 30063
61. J.A. Ross, G.B. Nelson, K.H. Wilson, J.R. Rabinowitz, A. Galati, G.D. Stoner, and et al. Adenomas induced by polycyclic aromatic hydrocarbons in strain A/J mouse lung correlate with time-integrated DNA adduct levels Cancer Res 55 5 1995 1039 1044
62. H. Reyes, S. Reisz-Porszasz, and O. Hankinson Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor Science 256 5060 1992 1193 1195
63. D.W. Nebert, A.L. Roe, M.Z. Dieter, W.A. Solis, Y. Yang, and T.P. Dalton Role of the aromatic hydrocarbon receptor and Ah gene battery in the oxidative stress response, cell cycle control and apoptosis Biochem Pharmacol 59 1 2000 65 85
64. M. Sporn Chemoprevention of cancer Lancet 342 8881 1993 1211 1213
65. B.N. Gomperts, A. Spira, P.P. Massion, T.C. Walser, I.I. Wistuba, J.D. Minna, and et al. Evolving concepts in lung carcinogenesis Semin Respir Crit Care Med 32 1 2011 32 43
66. C.J. Smith, T.A. Perfetti, and J.A. King Perspectives on pulmonary inflammation and lung cancer risk in cigarette smokers Inhal Toxicol 18 9 2006 667 677
67. G. Block, B. Patterson, and A. Subar Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence Nutr Cancer 18 1 1992 1 29
68. R.L. Keith Chemoprevention of lung cancer Proc Am Thorac Soc 6 2 2009 187 193
69. X.L. Tan, and S.D. Spivack Dietary chemoprevention strategies for induction of phase II xenobiotic-metabolizing enzymes in lung carcinogenesis: a review Lung Cancer 65 2 2009 29 137
70. P. Anandakumar, S. Jagan, S. Kamaraj, G. Ramakrishnan, A.A. Titto, and T. Devaki Beneficial influence of capsaicin on lipid peroxidation, membrane-bound enzymes and glycoprotein profile during experimental lung carcinogenesis J Pharm Pharmacol 60 2008 803 808
71. C. Naveenkumar, S. Raghunandhakumar, S. Asokkumar, and T. Devaki Baicalein abrogates reactive oxygen species (ROS)-mediated mitochondrial dysfunction during experimental pulmonary carcinogenesis in vivo Basic Clin Pharmacol Toxicol 112 4 2013 270 281
72. P. Rajendran, T. Jayakumar, I. Nishigaki, G. Ekambaram, Y. Nishigaki, J. Vetriselvi, and et al. Immunomodulatory effect of mangiferin in experimental animals with benzo (a) pyrene-induced lung carcinogenesis Int J Biomed Sci 9 2 2013 68 74
73. P. Rajendran, G. Ekambaram, V. Magesh, and D. Sakthisekaran Chemopreventive efficacy of mangiferin against benzo (a) pyrene induced lung carcinogenesis in experimental animals Environ Toxicol Pharmacol 26 3 2008 278 282
74. P. Anandakumar, S. Kamaraj, G. Ramakrishnan, S. Jagan, and T. Devaki Chemopreventive task of capsaicin against benzo (a) pyrene-induced lung cancer in Swiss albino mice Basic Clin Pharmacol Toxicol 104 5 2009 360 365
75. P. Anandakumar, S. Kamaraj, S. Jagan, G. Ramakrishnan, and T. Devaki Capsaicin provokes apoptosis and restricts benzo (a) pyrene induced lung tumorigenesis in Swiss albino mice Int Immunopharmacol 17 2 2013 254 259
76. P. Anandakumar, S. Kamaraj, S. Jagan, G. Ramakrishnan, S. Asokkumar, C. Naveenkumar, and et al. Capsaicin inhibits benzo (a) pyrene-induced lung carcinogenesis in an in vivo mouse model Inflamm Res 61 11 2012 1169 1175
77. P. Anandakumar, S. Kamaraj, S. Jagan, G. Ramakrishnan, and T. Devaki Lysosomal abnormalities during benzo (a) pyrene-induced experimental lung carcinogenesis: defensive role of capsaicin Fundam Clin Pharmacol 23 1 2009 97 103
78. G. Nithya, R. Mani, and D. Sakthisekaran Oral administration of thymoquinone attenuates benzo (a) pyrene induced lung carcinogenesis in male Swiss albino mice Int J Pharm Pharma Sci 6 7 2014 260 263
79. D. Ramya, Siddikuzzaman, and V.M. Grace Effect of all-trans retinoic acid (ATRA) on syndecan-1 expression and its chemoprotective effect in benzo (α) pyrene-induced lung cancer mice model Immunopharmacol Immunotoxicol 34 6 2012 1020 1027
80. V. Magesh, K. DurgaBhavani, P. Senthilnathan, P. Rajendran, and D. Sakthisekaran In vivo protective effect of crocetin on benzo (a) pyrene-induced lung cancer in Swiss albino mice Phytother Res 23 4 2009 533 539
81. A. Malhotra, P. Nair, and D.K. Dhawan Curcumin and resveratrol in combination modulates benzo (a) pyrene-induced genotoxicity during lung carcinogenesis Hum Exp Toxicol 31 12 2012 1199 1206
82. A. Malhotra, P. Nair, and D.K. Dhawan Premature mitochondrial senescence and related ultrastructural changes during lung carcinogenesis modulation by curcumin and resveratrol Ultrastruct Pathol 36 3 2012 179 184
83. N. Ravichandran, G. Suresh, B. Ramesh, and G. Vijaiyan Siva Fisetin, a novel flavonol attenuates benzo (a) pyrene-induced lung carcinogenesis in Swiss albino mice Food Chem Toxicol 49 5 2011 1141 1147
84. N. Ravichandran, G. Suresh, B. Ramesh, R. Manikandan, Y.W. Choi, and G.V. Siva Fisetin modulates mitochondrial enzymes and apoptotic signals in benzo (a) pyrene-induced lung cancer Mol Cell Biochem 390 1-2 2014 225 234
85. D. Devadoss, M. Ramar, and A. Chinnasamy Galangin, a dietary flavonol inhibits tumor initiation during experimental pulmonary tumorigenesis by modulating xenobiotic enzymes and antioxidant status Arch Pharm Res 1 2014 11 10.1007/s12272-014-0330-8
86. S. Kamaraj, P. Anandakumar, S. Jagan, G. Ramakrishnan, and T. Devaki Modulatory effect of hesperidin on benzo (a) pyrene induced experimental lung carcinogenesis with reference to COX-2, MMP-2 and MMP-9 Eur J Pharmacol 649 1-3 2010 320 327
87. S. Kamaraj, G. Ramakrishnan, P. Anandakumar, S. Jagan, and T. Devaki Antioxidant and anticancer efficacy of hesperidin in benzo (a) pyrene induced lung carcinogenesis in mice Invest New Drugs 27 3 2009 214 222
88. S. Kamaraj, P. Anandakumar, S. Jagan, G. Ramakrishnan, and T. Devaki Hesperidin attenuates mitochondrial dysfunction during benzo (a) pyrene-induced lung carcinogenesis in mice Fundam Clin Pharmacol 25 1 2011 91 98
89. N. Madhusudhanan, V. Ignatus, and T. Lakshmi Antioxidant activity of berberine on benzo (A) pyrene induced experimental lung carcinogenesis in mice J Chem Pharm Res 5 10 2013 194 200
90. G.Q. Zheng, P.M. Kenney, J. Zhang, and L.K. Lam Inhibition of benzo [a] pyrene-induced tumorigenesis by myristicin, a volatile aroma constituent of parsley leaf oil Carcinogenesis 13 10 1992 1921 1923
91. K. Selvendiran, C. Thirunavukkarasu, J.P.V. Singh, R. Padmavathi, and D. Sakthisekaran Chemopreventive effect of piperine on mitochondrial TCA cycle and phase-I and glutathione-metabolizing enzymes in benzo (a) pyrene induced lung carcinogenesis in Swiss albino mice Mol Cell Biochem 271 1-2 2005 101 106
92. K. Selvendiran, S.M. Banu, and D. Sakthisekaran Protective effect of piperine on benzo (a) pyrene-induced lung carcinogenesis in Swiss albino mice Clin Chim Acta 350 1-2 2004 73 78
93. K. Selvendiran, J. Prince Vijeya Singh, and D. Sakthisekaran In vivo effect of piperine on serum and tissue glycoprotein levels in benzo (a) pyrene induced lung carcinogenesis in Swiss albino mice Pulm Pharmacol Ther 19 2 2006 107 111
94. P. Nair, A. Malhotra, and D.K. Dhawan COX-2 as a potential target in chemoprevention of benzo (a) pyrene induced lung carcinogenesis in mice-combined role of curcumin and quercetin Am J Biomed Sci 4 3 2012 194 203
95. S. Kamaraj, R. Vinodhkumar, P. Anandakumar, S. Jagan, G. Ramakrishnan, and T. Devaki The effects of quercetin on antioxidant status and tumor markers in the lung and serum of mice treated with benzo (a) pyrene Biol Pharm Bull 30 12 2007 2268 2273
96. S. Manna, S. Mukherjee, A. Roy, S. Das, and C.K. Panda Tea polyphenols can restrict benzo [a] pyrene-induced lung carcinogenesis by altered expression of p53-associated genes and H-ras, c-myc and cyclin D1 J Nutr Biochem 20 5 2009 337 349
97. S.K. Katiyar, R. Agarwal, M.T. Zaim, and H. Mukhtar Protection against N-nitrosodiethylamine and benzo [a] pyrene-induced forestomach and lung tumorigenesis in A/J mice by green tea Carcinogenesis 14 5 1993 849 855
98. Q. Gu, C. Hu, Q. Chen, and Y. Xia Tea polyphenols prevent lung from preneoplastic lesions and effect p53 and bcl-2 gene expression in rat lung tissues Int J Clin Exp Pathol 6 8 2013 1523 1531
99. A. Revel, H. Raanani, E. Younglai, J. Xu, I. Rogers, R. Han, and et al. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects lung from DNA damage and apoptosis caused by benzo [a] pyrene J Appl Toxicol 23 4 2003 255 261
100. D.K. Priya, R. Gayathri, G. Gunassekaran, S. Murugan, and D. Sakthisekaran Chemopreventive role of sulforaphane by upholding the GSH redox cycle in pre- and post-initiation phases of experimental lung carcinogenesis Asian Pac J Cancer Prev 12 1 2011 103 110
101. D. Kalpana Deepa Priya, R. Gayathri, and D. Sakthisekaran Role of sulforaphane in the anti-initiating mechanism of lung carcinogenesis in vivo by modulating the metabolic activation and detoxification of benzo (a) pyrene Biomed Pharmacother 65 1 2011 9 16
102. D. Kalpana Deepa Priya, R. Gayathri, G.R. Gunassekaran, S. Murugan, and D. Sakthisekaran Apoptotic role of natural isothiocyanate from broccoli (Brassica oleracea Italica) in experimental chemical lung carcinogenesis Pharm Biol 51 5 2013 621 628
103. D. Kalpana Deepa Priya, R. Gayathri, G.R. Gunassekaran, and D. Sakthisekaran Protective role of sulforaphane against oxidative stress mediated mitochondrial dysfunction induced by benzo (a) pyrene in female Swiss albino mice Pulm Pharmacol Ther 24 1 2011 110 117
104. C.C. Conaway, C.X. Wang, B. Pittman, Y.M. Yang, J.E. Schwartz, D. Tian, and et al. Phenethyl isothiocyanate and sulforaphane and their N-acetylcysteine conjugates inhibit malignant progression of lung adenomas induced by tobacco carcinogens in A/J mice Cancer Res 65 18 2005 8548 8557
105. S. Asokkumar, C. Naveenkumar, S. Raghunandhakumar, S. Kamaraj, P. Anandakumar, S. Jagan, and et al. Antiproliferative and antioxidant potential of beta-ionone against benzo (a) pyrene-induced lung carcinogenesis in Swiss albino mice Mol Cell Biochem 363 1-2 2012 335 345
106. J.R. Anand, H. Rijhwani, K. Malapati, P. Kumar, K. Saikia, and M. Lakhar Anticancer activity of esculetin via-modulation of Bcl-2 and NF-κB expression in benzo [a] pyrene induced lung carcinogenesis in mice Biomed Prev Nutr 3 2 2013 107 112
107. F. Kassie, L.B. Anderson, R. Scherber, N. Yu, D. Lahti, P. Upadhyaya, and et al. Indole-3-carbinol inhibits 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone plus benzo (a) pyrene-induced lung tumorigenesis in A/J mice and modulates carcinogen-induced alterations in protein levels Cancer Res 67 13 2007 6502 6511
108. Y.S. Lee, T.H. Kim, K.J. Cho, and J.J. Jang Inhibitory effects of biochanin A on benzo (a) pyrene induced carcinogenesis in mice In Vivo 6 2 1991 283 286
109. R.D. Estensen, and L.W. Wattenberg Studies of chemopreventive effects of myo-inositol on benzo (a) pyrene-induced neoplasia of the lung and forestomach of female A/J mice Carcinogenesis 14 9 1993 1975 1977
110. Q. Zhang, J. Pan, Y. Wang, R. Lubet, and M. You Beetroot red (betanin) inhibits vinyl carbamate and benzo (a) pyrene-induced lung tumorigenesis through apoptosis Mol Carcinog 52 9 2012 686 691
111. R. Zoltaszek, M. Hanausek, T. Slaga, and Z. Walaszek Proapoptotic effects of d-glucarate on chemically induced lung tumorigenesis in A/J mice Cancer Res 67 9S 2007 3344
112. S. Al-Jasabi, A. Saad, and E.T.M.E. Haque The role of antioxidant anthocyanin in the attenuation of lung cancer caused by benzo [a] pyrene in Balb/C mice Middle-East J Sci Res 14 2 2013 168 172
113. R.M. Samarth, M. Panwar, M. Kumar, and A. Kumar Protective effects of Mentha piperita Linn on benzo [a] pyrene-induced lung carcinogenicity and mutagenicity in Swiss albino mice Mutagenesis 21 1 2006 61 66
114. V. Rajesh, and P. Perumal Cytoprotective effect of Smilax zeylanica Linn. leaves against benzo [a] pyrene induced lung cancer with reference to lipid peroxidation and antioxidant system in Swiss albino mice Oriental Pharm Exp Med 13 4 2013 267 277
115. P.N. Venkatesan, P. Rajendran, G. Ekambaram, and D. Sakthisekaran Combination therapeutic effect of cisplatin along with Solanum trilobatum on benzo (a) pyrene induced experimental lung carcinogenesis Nat Prod Res 22 12 2008 1094 1106
116. S. Paul, S. Bhattacharyya, A. Samaddar, N. Boujedaini, and A.R. Khuda-Bukhsh Anticancer potentials of root extract of Polygala senega against benzo [a] pyrene-induced lung cancer in mice Zhong Xi Yi Jie He Xue Bao 9 3 2011 320 327
117. L. Feng, X. Jia, M. Zhu, Y. Chen, and F. Shi Chemoprevention by Prunella vulgaris L. extract of non-small cell lung cancer via promoting apoptosis and regulating the cell cycle Asian Pac J Cancer Prev 11 5 2010 1355 1358
118. P. Senthilnathan, R. Padmavathi, V. Magesh, and D. Sakthisekaran Chemotherapeutic efficacy of paclitaxel in combination with Withania somnifera on benzo (a) pyrene-induced experimental lung cancer Cancer Sci 97 7 2006 658 664
119. A.M. Ibrahim, I.H. Borai, M.M. Ali, H.M. Ghanem, A.E.-S.A. Hegazi, and A.M. Mousa Inhibitory effect of a mixture containing vitamin C, lysine, proline, epigallocatechin gallate, zinc and alpha-1-antitrypsin on lung carcinogenesis induced by benzo (a) pyrene in mice J Res Med Sci 18 5 2013 427 434
120. K. Sak Cytotoxicity of dietary flavonoids on different human cancer types Pharmacogn Rev 8 16 2014 122 146
121. M. González-Vallinas, M. González-Castejón, A. Rodríguez-Casado, and A. Ramírez de Molina Dietary phytochemicals in cancer prevention and therapy: a complementary approach with promising perspectives Nutr Rev 71 9 2013 585 599
122. R.B. Shekelle, M. Lepper, S. Liu, C. Maliza, W.J. Raynor Jr., A.H. Rossof, and et al. Dietary vitamin A and risk of cancer in the Western Electric study Lancet 28 8257 1981 1185 1190
123. N. van Zandwijk, O. Dalesio, U. Pastorino, N. de Vries, and H. van Tinteren EUROSCAN, a randomized trial of vitamin A and N-acetylcysteine in patients with head and neck cancer or lung cancer. For the EUropean Organization for Research and Treatment of Cancer Head and Neck and Lung Cancer Cooperative Groups J Natl Cancer Inst 92 12 2000 977 986
124. T. Tanvetyanon, and G. Bepler Beta-carotene in multivitamins and the possible risk of lung cancer among smokers versus former smokers: a meta-analysis and evaluation of national brands Cancer 113 1 2008 150 157
125. P. Hodek, J. Krízková, K. Burdová, M. Sulc, R. Kizek, J. Hudecek, and et al. Chemopreventive compounds - view from the other side Chem Biol Interact 180 1 2009 1 9
126. X.J. Wang, Z. Sun, N.F. Villeneuve, S. Zhang, F. Zhao, Y. Li, and et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2 Carcinogenesis 29 6 2008 1235 1243
127. A. Scalbert, and G. Williamson Dietary intake and bioavailability of polyphenols J Nutr 130 8S 2000 2073S 2085S
128. J.K. Woo, D.S. Choi, H.T. Tran, B.E. Gilbert, W.K. Hong, and H.Y. Lee Liposomal encapsulation of deguelin: evidence for enhanced antitumor activity in tobacco carcinogen-induced and oncogenic k-ras-induced lung tumorigenesis Cancer Prev Res (Phila) 2 4 2009 361 369
129. S. Bisht, G. Feldmann, S. Soni, R. Ravi, C. Karikar, A. Maitra, and et al. Polymeric nanoparticle-encapsulated curcumin (nanocurcumin): a novel strategy for human cancer therapy J Nanobiotechnol 5 3 2007 1 18
130. R.C. Gupta, S. Bansal, F. Aqil, J. Jeyabalan, P. Cao, H. Kausar, and et al. Controlled-release systemic delivery-a new concept in cancer chemoprevention Carcinogenesis 33 8 2012 1608 1615
131. S. Cauchi, W. Han, S.V. Kumar, and S.D. Spivack Haplotype-environment interactions that regulate the human glutathione S-transferase P1 promoter Cancer Res 66 12 2006 6439 6448