Trianthema portulacastrum linn. Displays anti-inflammatory responses during chemically induced rat mammary tumorigenesis through simultaneous and differential regulation of NF-κB and Nrf2 signaling pathways

International Journal of Molecular Sciences

Volumn 16, Issue 2, 2015, Pages 2426-2445

  Mandal, Animesh ^a   Bishayee, Anupam ^b  

^a NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

^b CALIFORNIA NORTHSTATE UNIVERSITY   (United States)

Author keywords

Anti inflammatory mechanisms; Breast tumor; COX 2; DMBA; HSP90; NF B; Nrf2; References; Trianthema portulacastrum

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; ALCOHOL; CYCLOOXYGENASE 2; HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PLANT EXTRACT; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR RELA; TRIANTHEMA PORTULACASTRUM EXTRACT; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT;

AIZOACEAE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BREAST CARCINOGENESIS; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG DOSE COMPARISON; FEMALE; IMMUNOHISTOCHEMISTRY; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BREAST TUMOR; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; ISOLATION AND PURIFICATION; METABOLISM; PATHOLOGY; PLANT STRUCTURES; SPRAGUE DAWLEY RAT;

RATTUS; TRIANTHEMA PORTULACASTRUM;

9,10-DIMETHYL-1,2-BENZANTHRACENE; AIZOACEAE; ANIMALS; ANTI-INFLAMMATORY AGENTS; BREAST NEOPLASMS; CYCLOOXYGENASE 2; FEMALE; HSP90 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; NF-E2-RELATED FACTOR 2; NF-KAPPA B; PLANT COMPONENTS, AERIAL; PLANT EXTRACTS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84921838788     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16022426     Document Type: Article

References (102)

1. Kirtikar, K.R.; Basu, B.D. Indian Medicinal Plants; Lalit Mohan Basu: Allahabad, India, 1975; Volume 2.
2. Jansen, P.C.M. Trianthema portulacastrum L.; Prota 2: Vegetables/Légumes. [CD-Rom]; Grubben, G.J.H., Denton, O.A., Eds.; PROTA: Wageningen, The Netherlands, 2004.
3. Khan, N.; Sultana, A.; Tahir, N.; Jamila, N. Nutritional composition, vitamins, minerals and toxic heavy metals analysis of Trianthema portulacastrum L., a wild edible plant from Peshawar, Khyber Pakhtunkhwa. Pak. Afr. J. Biotechnol. 2013, 12, 6079-6085.
4. Wahid, H.H.; Siddiqui, A. Survey of Drugs, 2nd ed.; Institute of History of Medicine and Medical Research: New Delhi, India, 1961.
5. Fazal, U.; Razzack, M. A Handbook of Common Remedies in Unani Medicine; Central Council for Research in Unani Medicine: New Delhi, India, 1978.
6. Khare, C.P. Indian Medicinal Plants, an Illustrated Dictionary; Springer-Verlag: Berlin/Heidelberg, Germany, 2006.
7. Vohora, S.B.; Shah, S.A.; Naqvi, S.A.H.; Ahmad, S.; Khan, M.S.Y. Studies on Trianthemaportulacastrum. Planta Medica 1983, 47, 106-108.
8. Nawaz, H.R.; Malik, A.; Ali, M.S. Trianthenol: An antifungal tetraterpenoid from Trianthema portulacastrum (Aizoaceae). Phytochemistry 2001, 56, 99-102.
9. Kumar, G.; Banu, G.S.; Pandian, M.R. Evaluation of the antioxidant activity of Trianthema portulacastrum L. Ind. J. Pharmacol. 2005, 37, 331-333.
10. Anreddy, R.N.R.; Porika, M.; Yellu, N.R.; Devarakonda, R.K. Hypogycemic and hypolipidemic activities of Trianthema portulacastrum Linn. plant in normal and alloxan induced diabetic rats. Int. J. Pharmacol. 2010, 6, 129-133.
11. Shivhare, M.K.; Singour, P.K.; Chaurasiya, P.K.; Pawar, R.S. Trianthema portulacastrum Linn. (Bishkhapra). Pharmacogn. Rev. 2012, 6, 132-140.
12. Bishayee, A.; Mandal, A.; Chatterjee, M. Prevention of alcohol-carbon tetrachloride-induced signs of early hepatotoxicity in mice by Trianthema portulacastrum L. Phytomedicine 1996, 3, 155-161.
13. Mandal, A.; Bishayee, A.; Chatterjee, M. Trianthema portulacastrum affords antihepatotoxic activity against carbon tetrachloride-induced chronic liver damage in mice: Reflections in subcellular levels. Phytother. Res. 1997, 11, 216-221.
14. Mandal, A.; Karmakar, R.; Bandyopadhyay, S.; Chatterjee, M. Antihepatotoxic potential of Trianthema portulacastrum in carbon tetrachloride-induced chronic hepatocellular injury in mice: Reflection in haematological, histological and biochemical characteristics. Arch. Pharm. Res. 1998, 21, 223-230.
15. Mandal, A.; Bandyopadhyay, S.; Chatterjee, M. Trianthema portulacastrum L. reverses hepatic lipid peroxidation, glutathione status and activities of related antioxidant enzymes in carbon tetrachloride-induced chronic liver damage in mice. Phytomedicine 1997, 4, 239-244.
16. Sarkar, A.; Pradhan, S.; Mukhopadhyay, I.; Bose, S.K.; Roy, S.; Chatterjee, M. Inhibition of early DNA-damage and chromosomal aberrations by Triantheme portulacastrum L. in carbon tetrachloride-induced mouse liver damage. Cell Biol. Int. 1999, 23, 703-708.
17. Kumar, G.; Sharmila Banu, G.; Vanitha Pappa, P.; Sundararajan, M.; Rajasekara Pandian, M. Hepatoprotective activity of Trianthema portulacastrum L. against paracetamol and thioacetamide intoxication in albino rats. J. Ethnopharmacol. 2004, 92, 37-40.
18. Sharmila Banu, G.; Kumar, G.; Murugesan, A.G. Ethanolic leaves extract of Trianthema portulacastrum L. ameliorates aflatoxin B1 induced hepatic damage in rats. Ind. J. Clin. Biochem. 2009, 24, 250-256.
19. Sharmila Banu, G.; Kumar G.; Murugesan, A.G. Effect of ethanolic leaf extract of Trianthema portulacastrum L. on aflatoxin induced hepatic damage in rats. Ind. J. Clin. Biochem. 2009, 24, 414-418.
20. Shyam Sunder, A.; Rama Narsimha Reddy, A.; Rajeshwar, Y.; Kira, N.G.; Krishna Prasad, D.; Baburao, B.; Thirumurugu, S.; Karthik, A. Protective effect of methanolic extract of Trianthema portulacastrum in atherosclerotic diet induced renal and hepatic changes in rats. Der Pharm. Lett. 2010, 2, 540-545.
21. Bhattacharya, S.; Chatterjee, M. Protective role of Trianthema portulacastrum against diethylnitrosamine-induced experimental hepatocarcinogenesis. Cancer Lett. 1998, 129, 7-13.
22. Bhattacharya, S.; Chatterjee, M. Trianthema portulacastrum restores the antioxidant defense enzyme levels and hepatic biotransformation patterns in experimental rat hepatocarcinogenesis. Ital. J. Biochem. 1998, 48, 225-232.
23. Bhattacharya, S.; Chatterjee, M. Inhibitory effect of Trianthema portulacastrum L. diethylnitroso-amine-induced phenobarbital promoted hepatocarcinogenesis. Neoplasma 1999, 46, 105-111.
24. Reuben, S.C.; Gopalan, A.; Petit, D.M.; Bishayee, A. Modulation of angiogenesis by dietary phytoconstituents in the prevention and intervention of breast cancer. Mol. Nutr. Food Res. 2012, 56, 14-29.
25. Vadodkar, A.S.; Suman, S.; Lakshmanaswamy, R.; Damodaran, C. Chemoprevention of breast cancer by dietary compounds. Anticancer Agents Med. Chem. 2012, 12, 1185-1202.
26. Parikh, N.R.; Mandal, A.; Bhatia, D.; Siveen, K.S.; Sethi, G.; Bishayee, A. Oleanane triterpenoids in the prevention and therapy of breast cancer: Current evidence and future perspectives. Phytochem. Rev. 2014, 13, 793-810.
27. Bishayee, A.; Mandal, A. Trianthema portulacastrum Linn. exerts chemoprevention of 7,12-dimethylbenz(a)anthracene-induced mammary tumorigenesis in rats. Mutat. Res. 2014, 768, 107-118.
28. Macciò, A.; Madeddu, C. Obesity, inflammation, and postmenopausal breast cancer: Therapeutic implications. Sci. World J. 2011, 11, 2020-2036.
29. Shostak, K.; Chariot, A. NF-κB, stem cells and breast cancer: The links get stronger. Breast Cancer Res. 2011, 13, doi:10.1186/bcr2886.
30. Baumgarten, S.C.; Frasor, J. Minireview: Inflammation: An instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol. Endocrinol. 2012, 26, 360-371.
31. Harris, R.E.; Casto, B.C.; Harris, Z.M. Cyclooxygenase-2 and the inflammogenesis of breast cancer. World J. Clin. Oncol. 2014, 5, 677-692.
32. Brown, K.A. Impact of obesity on mammary gland inflammation and local estrogen production. J. Mammary Gland Biol. Neoplasia 2014, 19, 183-189.
33. Pick, E.; Kluger, Y.; Giltnane, J.M.; Moeder, C.; Camp, R.L.; Rimm, D.L.; Kluger, H.M. High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res. 2007, 67, 2932-2937.
34. Cheng, Q.; Chang, J.T.; Geradts, J.; Neckers, L.M.; Haystead, T.; Spector, N.L.; Lyerly, H.K. Amplification and high-level expression of heat shock protein 90 marks aggressive phenotypes of human epidermal growth factor receptor 2 negative breast cancer. Breast Cancer Res. 2012, 14, doi:10.1186/bcr3168.
35. Nakshatri, H.; Bhat-Nakshatri, P.; Martin, D.A.; Goulet, R.J., Jr.; Sledge, G.W., Constitutive activation of NF-κB during progression of breast cancer to hormone-independent growth. Mol. Cell. Biol. 1997, 17, 3629-3639.
36. Zubair, A.; Frieri, M. Role of nuclear factor-κB in breast and colorectal cancer. Curr. Allergy Asthma Rep. 2013, 13, 44-49.
37. Chaturvedi, M.M.; Sung, B.; Yadav, V.R.; Kannappan, R.; Aggarwal, B.B. NF-κB addiction and its role in cancer: “One size does not fit all”. Oncogene 2011, 30, 1615-1630.
38. Bellezza, I.; Mierla, A.L.; Minelli, A. Nrf2 and NF-κB and their concerted modulation in cancer pathogenesis and progression. Cancers 2010, 2, 483-497.
39. Nair, S.; Doh, S.T.; Chan, J.Y.; Kong, A.N.; Cai, L. Regulatory potential for concerted modulation of Nrf2- and Nfkb1-mediated gene expression in inflammation and carcinogenesis. Br. J. Cancer 2008, 99, 2070-2082.
40. Siegel, R.; Ma, J.; Zou, Z.; Jemal, A. Cancer statistics, 2014. CA Cancer J. Clin. 2014, 64, 9-29.
41. Fouad, T.M.; Kogawa, T.; Reuben, J.M.; Ueno, N.T. The role of inflammation in inflammatory breast cancer. Adv. Exp. Med. Biol. 2014, 816, 53-73.
42. Johnson, J.J. Carnosol: A promising anti-cancer and anti-inflammatory agent. Cancer Lett. 2011, 305, 1-7.
43. Sinha, D.; Biswas, J.; Sung, B.; Aggarwal, B.B.; Bishayee, A. Chemopreventive and chemotherapeutic potential of curcumin in breast cancer. Curr. Drug Targets 2012, 13, 1799-1819.
44. Howe, L.R.; Subbaramaiah, K.; Hudis, C.A.; Dannenberg, A.J. Molecular pathways: Adipose inflammation as a mediator of obesity-associated cancer. Clin. Cancer Res. 2013, 19, 6074-6083.
45. Crawford, S. Anti-inflammatory/antioxidant use in long-term maintenance cancer therapy: A new therapeutic approach to disease progression and recurrence. Ther. Adv. Med. Oncol. 2014, 6, 52-68.
46. Subbaramaiah, K.; Sue, E.; Bhardwaj, P.; Du, B.; Hudis, C.A.; Giri, D.; Kopelovich, L.; Zhou, X.K.; Dannenberg, A.J. Dietary polyphenols suppress elevated levels of proinflammatory mediators and aromatase in the mammary gland of obese mice. Cancer Prev. Res. 2013, 6, 886-897.
47. Howe, L.R. Inflammation and breast cancer. Cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res. 2007, 9, doi:10.1186/bcr1678.
48. Singh-Ranger, G.; Salhab, M.; Mokbel, K. The role of cyclooxygenase-2 in breast cancer: Review. Breast Cancer Res. Treat. 2008, 109, 189-198.
49. Williams, C.S.; Mann, M.; DuBois, R.N. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 1999, 18, 7908-7916.
50. Harris, R.E. Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 2009, 17, 55-67.
51. Glover, J.A.; Hughes, C.M.; Cantwell, M.M.; Murray, L.J. A systematic review to establish the frequency of cyclooxygenase-2 expression in normal breast epithelium, ductal carcinoma in situ, microinvasive carcinoma of the breast and invasive breast cancer. Br. J. Cancer 2011, 105, 13-17.
52. Abou-Issa, H.M.; Alshafie, G.A.; Seibert, K.; Koki, A.T.; Masferrer, J.L.; Harris, R.E. Dose-response effects of the COX-2 inhibitor, celecoxib, on the chemoprevention of mammary carcinogenesis. Anticancer Res. 2001, 21, 3425-3432.
53. Pandi, M.; Manikandan, R.; Muthumary, J. Anticancer activity of fungal taxol derived from Botryodiplodia theobromae Pat., an endophytic fungus, against 7,12 dimethyl benz(a)anthracene (DMBA)-induced mammary gland carcinogenesis in Sprague Dawley rats. Biomed. Pharmacother. 2010, 64, 48-53.
54. Roy, P.; George, J.; Srivastava, S.; Tyagi, S.; Shukla, Y. Inhibitory effects of tea polyphenols by targeting cyclooxygenase-2 through regulation of nuclear factor kappa B, Akt and p53 in rat mammary tumors. Investig. New Drugs 2011, 29, 225-231.
55. Nakatsugi, S.; Ohta, T.; Kawamori, T.; Mutoh, M.; Tanigawa, T.; Watanabe, K.; Sugie, S.; Sugimura, T.; Wakabayashi, K. Chemoprevention by nimesulide, a selective cyclooxygenase-2 inhibitor, of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP)-induced mammary gland carcinogenesis in rats. Jpn. J. Cancer Res. 2000, 91, 886-892.
56. Banerjee, S.; Bueso-Ramos, C.; Aggarwal, B.B. Suppression of 7,12-dimethylbenz(a)anthracene induced mammary carcinogenesis in rats by resveratrol: Role of nuclear factor-κB, cyclooxygenase 2, and matrix metalloprotease 9. Cancer Res. 2006, 62, 4945-4954.
57. Shimp, S.K., 3rd; Parson, C.D.; Regna, N.L.; Thomas, A.N.; Chafin, C.B.; Reilly, C.M.; Nichole Rylander, M. HSP90 inhibition by 17-DMAG reduces inflammation in J774 macrophages through suppression of Akt and nuclear factor-κB pathways. Inflamm. Res. 2012, 61, 521-533.
58. Tamura, Y.; Torigoe, T.; Kutomi, G.; Hirata, K.; Sato, N. New paradigm for intrinsic function of heat shock proteins as endogenous ligands in inflammation and innate immunity. Curr. Mol. Med. 2012, 12, 1198-1206.
59. Kumar, P.; Kolls, J.K. Act1-hsp90 heats up TH17 inflammation. Nat. Immunol. 2013, 14, 16-17.
60. Kamal, A.; Thao, L.; Sensintaffar, J.; Zhang, L.; Boehm, M.F.; Fritz, L.C.; Burrows, FJ. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003, 425, 407-410.
61. Trepel, J.; Mollapour, M.; Giaccone, G.; Neckers, L. Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 2010, 10, 537-549.
62. Sankhala, K.K.; Mita, M.M.; Mita, A.C.; Takimoto, C.H. Heat shock proteins: A potential anticancer target. Curr. Drug Targets 2011, 12, 2001-2008.
63. Barrott, J.J.; Haystead, T.A. Hsp90, an unlikely ally in the war on cancer. FEBS J. 2013, 280, 1381-1396.
64. Park, K.; Choi, K.; Kim, H.; Kim, K.; Lee, M.H.; Lee, J.H.; Kim Rim, J.C. Isoflavone-deprived soy peptide suppresses mammary tumorigenesis by inducing apoptosis. Exp. Mol. Med. 2009, 41, 371-381.
65. Tran, P.L.; Kim, S.A.; Choi, H.S.; Yoon, J.H.; Ahn, S.G. Epigallocatechin-3-gallate suppresses the expression of HSP70 and HSP90 and exhibits anti-tumor activity in vitro and in vivo. BMC Cancer 2010, 10, doi:10.1186/1471-2407-10-276.
66. Bishayee, A.; Thoppil, R.J.; Mandal, A.; Darvesh, A.S.; Ohanyan, V.; Meszaros, J.G.; Háznagy-Radnai, E.; Hohmann, J.; Bhatia, D. Black currant phytoconstituents exert chemoprevention of diethylnitrosamine-initiated hepatocarcinogenesis by suppression of the inflammatory response. Mol. Carcinogenes. 2013, 52, 304-317.
67. Grivennikov, S.I.; Greten, F.R.; Karin, M. Immunity, inflammation, and cancer. Cell 2010, 140, 883-899.
68. Hayden, M.S.; Ghosh, S. Shared principles in NF-κB signaling. Cell 2008, 132, 344-362.
69. Rayet, B.; Gélinas, C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene 1999, 18, 6938-6947.
70. Viatour, P.; Merville, M.P.; Bours, V.; Chariot, A. Phosphorylation of NF-κB and IκB proteins: Implications in cancer and inflammation. Trends Biochem. Sci. 2005, 30, 43-52.
71. Sethi, G.; Sung, B.; Aggarwal, B.B. Nuclear factor-κB activation: From bench to bedside. Exp. Biol. Med. 2008, 233, 21-31.
72. Sovak, M.A.; Bellas, R.E.; Kim, D.W.; Zanieski, G.J.; Rogers, A.E.; Traish, A.M.; Sonenshein, G.E. Aberrant nuclear factor-κB/Rel expression and the pathogenesis of breast cancer. J. Clin. Investig. 1997, 100, 2952-2960.
73. Van Laere, S.; van der Auwera, I.; van den Eynden, G.G.; Fox, S.B.; Bianchi, F.; Harris, A.L.; van Dam, P.; van Marck, E.A.; Vermeulen, P.B.; Dirix, L.Y. Distinct molecular signature of inflammatory breast cancer by cDNA microarray analysis. Breast Cancer Res. Treat. 2005, 93, 237-246.
74. Jana, D.; Das, S.; Sarkar, D.K.; Mandal, S.; Maji, A.; Mukhopadhyay, M. Role of nuclear factor-κB in female breast cancer: A study in Indian patients. Asian Pac. J. Cancer Prev. 2012, 13, 5511-5515.
75. Ralhan, R.; Pandey, M.K.; Aggarwal, B.B. Nuclear factor-κB links carcinogenic and chemopreventive agents. Front. Biosci. 2009, 1, 45-60.
76. Gupta, S.C.; Sundaram, C.; Reuter, S.; Aggarwal, B.B. Inhibiting NF-κB activation by small molecules as a therapeutic strategy. Biochim. Biophys. Acta 2010, 1799, 775-787.
77. Zhu, Z.; Zhong, S.; Shen, Z. Targeting the inflammatory pathways to enhance chemotherapy of cancer. Cancer Biol. Ther. 2011, 12, 95-105.
78. Kim, D.W.; Sovak, M.A.; Zanieski, G.; Nonet, G.; Romieu-Mourez, R.; Lau, A.W.; Hafer L.J.; Yaswen, P.; Stampfer, M.; Rogers, A.E.; et al. Activation of NF-κB/Rel occurs early during neoplastic transformation of mammary cells. Carcinogenesis 2000, 21, 871-879.
79. Currier, N.; Solomon, S.E.; Demicco, E.G.; Chang, D.L.; Farago, M.; Ying, H.; Dominguez, I.; Sonenshein, G.E.; Cardiff, R.D.; Xiao, Z.X.; et al. Oncogenic signaling pathways activated in DMBA-induced mouse mammary tumors. Toxicol. Pathol. 2005, 33, 726-737.
80. Vinothini, G.; Manikandan, P.; Anandan, R.; Nagini, S. Chemoprevention of rat mammary carcinogenesis by Azadirachta indica leaf fractions: Modulation of hormone status, xenobiotic-metabolizing enzymes, oxidative stress, cell proliferation and apoptosis. Food Chem. Toxicol. 2009, 47, 1852-1863.
81. Baird, L.; Dinkova-Kostova, A.T. The cytoprotective role of the Keap1-Nrf2 pathway. Arch. Toxicol. 2011, 85, 241-272.
82. Khor, T.O.; Yu, S.; Kong, A.N. Dietary cancer chemopreventive agents—Targeting inflammation and Nrf2 signaling pathway. Planta Med. 2008, 74, 1540-1547.
83. Hu, R.; Saw, C.L.; Yu, R.; Kong, A.N. Regulation of NF-E2-related factor 2 signaling for cancer chemoprevention: Antioxidant coupled with antiinflammatory. Antioxid. Redox Signal. 2010, 13, 1679-1698.
84. Kundu, J.K.; Surh, Y.J. Nrf2-Keap1 signaling as a potential target for chemoprevention of inflammation-associated carcinogenesis. Pharm. Res. 2010, 27, 999-1013.
85. Slocum, S.L.; Kensler, T.W. Nrf2: Control of sensitivity to carcinogens. Arch. Toxicol. 2011, 85, 273-284.
86. Cardozo, L.F.; Pedruzzi, L.M.; Stenvinkel, P.; Stockler-Pinto, M.B.; Daleprane, J.B.; Leite, M.,; Mafra, D. Nutritional strategies to modulate inflammation and oxidative stress pathways via activation of the master antioxidant switch Nrf2. Biochimie 2013, 95, 1525-1533.
87. Carayol, N.; Chen, J.; Yang, F.; Jin, T.; Jin, L.; States, D.; Wang, C.Y. A dominant function of IKK/NF-κB signaling in global lipopolysaccharide-induced gene expression. J. Biol. Chem. 2006, 281, 31142-31151.
88. Khor, T.O.; Huang, M.T.; Kwon, K.H.; Chan, J.Y.; Reddy, B.S.; Kong, A.N. Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res. 2006, 66, 11580-11584.
89. Li, W.; Khor, T.O.; Xu, C.; Shen, G.; Jeong, W.S.; Yu, S.; Kong, A.N. Activation of Nrf2-antioxidant signaling attenuates NFκB-inflammatory response and elicits apoptosis. Biochem. Pharmacol. 2008, 76, 1485-1489.
90. Becks, L.; Prince, M.; Burson, H.; Christophe, C.; Broadway, M.; Itoh, K.; Yamamoto, M.; Mathis, M.; Orchard, E.; Shi, R.; et al. Aggressive mammary carcinoma progression in Nrf2 knockout mice treated with 7,12-dimethylbenz[a]anthracene. BMC Cancer 2010, 10, doi:10.1186/1471-2407-10-540.
91. Singh, B.; Bhat, N.K.; Bhat, H.K. Induction of NAD(P)H-quinone oxidoreductase 1 by antioxidants in female ACI rats is associated with decrease in oxidative DNA damage and inhibition of estrogen-induced breast cancer. Carcinogenesis 2012, 33, 156-163.
92. Singh, B.; Bhat, H.K. Superoxide dismutase 3 is induced by antioxidants, inhibits oxidative DNA damage and is associated with inhibition of estrogen-induced breast cancer. Carcinogenesis 2012, 33, 2601-2610.
93. Singh, B.; Chatterjee, A.; Ronghe, A.M.; Bhat, N.K.; Bhat, H.K. Antioxidant-mediated up-regulation of OGG1 via NRF2 induction is associated with inhibition of oxidative DNA damage in estrogen-induced breast cancer. BMC Cancer 2013, 13, doi:10.1186/1471-2407-13-253.
94. Yao, Y.; Brodie, A.M.; Davidson, N.E.; Kensler, T.W.; Zhou, Q. Inhibition of estrogen signaling activates the NRF2 pathway in breast cancer. Breast Cancer Res. Treat. 2010, 124, 585-591.
95. Manzanares, M.A.; Solanas, M.; Moral, R.; Escrich, R.; Vela, E.; Costa, I.; Escrich, E. Dietary extra-virgin olive oil and corn oil differentially modulate the mRNA expression of xenobiotic-metabolizing enzymes in the liver and in the mammary gland in a rat chemically induced breast cancer model. Eur. J. Cancer Prev. 2014, in press.
96. Chen, B.; Zhang, Y.; Wang, Y.; Rao, J.; Jiang, X.; Xu, Z. Curcumin inhibits proliferation of breast cancer cells through Nrf2-mediated down-regulation of Fen1 expression. J. Steroid Biochem. Mol. Biol. 2014, 143, 11-18.
97. Na, H.K.; Surh, Y.J. Oncogenic potential of Nrf2 and its principal target protein heme oxygenase-1. Free Radic. Biol. Med. 2014, 67, 353-365.
98. Liu, R.H. Potential synergy of phytochemicals in cancer prevention: Mechanism of action. J. Nutr. 2004, 134, 3479S-3485S.
99. De Kok, T.M.; van Breda, S.G.; Manson, M.M. Mechanisms of combined action of different chemopreventive dietary compounds: A review. Eur. J. Nutr. 2008, 47, 51-59.
100. Bode, A.M.; Dong, Z. Epigallocatechin 3-gallate and green tea catechins: United they work, divided they fail. Cancer Prev. Res. 2009, 2, 514-517.
101. Bishayee, A.; Mandal, A.; Thoppil, R.J.; Darvesh, A.S.; Bhatia, D. Chemopreventive effect of a novel oleanane triterpenoid in a chemically induced rodent model of breast cancer. Int. J. Cancer 2013, 133, 1054-1064.
102. Mandal, A.; Bhatia, D.; Bishayee, A. Suppression of inflammatory cascade is implicated in methyl amooranin-mediated inhibition of experimental mammary carcinogenesis. Mol. Carcinogenes. 2014, 53, 999-1010.