1932

Abstract

Chemopreventive agents that the general population can consume for prolonged periods of time with minimal risk of any side effects are of great interest to all in search of a solution to the pervasive incidence of cancer. Dietary bioactive components have been found to modulate many deregulated molecular pathways associated with the initiation and progression of different types of cancer. Combination regimens with dietary bioactive components are a promising strategy for cancer chemoprevention because they may offer enhanced protective effects against cancer development but cause little or no adverse effects. This article provides an overview of studies examining the combination of dietary bioactive components for the chemoprevention of major types of cancer. A better understanding of existing research on the combination of dietary bioactive components will provide an important basis for the rational design of future combination studies and the successful development of cancer chemoprevention strategies.

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2015-04-10
2024-05-12
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Literature Cited

  1. Altenburg JD, Bieberich AA, Terry C, Harvey KA, VanHorn JF. et al. 2011. A synergistic antiproliferation effect of curcumin and docosahexaenoic acid in SK-BR-3 breast cancer cells: unique signaling not explained by the effects of either compound alone. BMC Cancer 11:149 [Google Scholar]
  2. Amin AR, Wang D, Zhang H, Peng S, Shin HJ. et al. 2010. Enhanced anti-tumor activity by the combination of the natural compounds (−)-epigallocatechin-3-gallate and luteolin: potential role of p53. J. Biol. Chem. 285:4534557–65 [Google Scholar]
  3. Awad AB, Burr AT, Fink CS. 2005. Effect of resveratrol and beta-sitosterol in combination on reactive oxygen species and prostaglandin release by PC-3 cells. Prostaglandins Leukot. Essent. Fatty Acids 72:3219–26 [Google Scholar]
  4. Barrera LN, Johnson IT, Bao Y, Cassidy A, Belshaw NH. 2013. Colorectal cancer cells Caco-2 and HCT116 resist epigenetic effects of isothiocyanates and selenium in vitro. Eur. J. Nutr. 52:41327–41 [Google Scholar]
  5. Basu A, Imrhan V. 2007. Tomatoes versus lycopene in oxidative stress and carcinogenesis: conclusions from clinical trials. Eur. J. Clin. Nutr. 61:3295–303 [Google Scholar]
  6. Bird RP. 1995. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Cancer Lett. 93:155–71 [Google Scholar]
  7. Bonnesen C, Eggleston IM, Hayes JD. 2001. Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines. Cancer Res. 61:166120–30 [Google Scholar]
  8. Bose M, Hao X, Husain A, Park S, Lambert JD, Yang. 2007. Inhibition of tumorigenesis in ApcMin/+ mice by a combination of (−)-epigallocatechin-3-gallate and fish oil.. J. Agric. Food Chem. 55:197695–700 [Google Scholar]
  9. Boursi B, Arber N. 2007. Current and future clinical strategies in colon cancer prevention and the emerging role of chemoprevention. Curr. Pharm. Des. 13:222274–82 [Google Scholar]
  10. Brahmbhatt M, Gundala SR, Asif G, Shamsi SA, Aneja R. 2013. Ginger phytochemicals exhibit synergy to inhibit prostate cancer cell proliferation. Nutr. Cancer 65:2263–72 [Google Scholar]
  11. Butler LM, Wu AH, Wang R, Koh WP, Yuan JM, Yu MC. 2010. A vegetable-fruit-soy dietary pattern protects against breast cancer among postmenopausal Singapore Chinese women. Am. J. Clin. Nutr. 91:41013–19 [Google Scholar]
  12. Canene-Adams K, Lindshield BL, Wang S, Jeffery EH, Clinton SK, Erdman JW Jr. 2007. Combinations of tomato and broccoli enhance antitumor activity in dunning r3327-h prostate adenocarcinomas. Cancer Res. 67:2836–43 [Google Scholar]
  13. Challa A, Rao DR, Reddy BS. 1997. Interactive suppression of aberrant crypt foci induced by azoxymethane in rat colon by phytic acid and green tea. Carcinogenesis 18:102023–26 [Google Scholar]
  14. Chen C, Kong AN. 2005. Dietary cancer-chemopreventive compounds: from signaling and gene expression to pharmacological effects. Trends Pharmacol. Sci. 26:6318–26 [Google Scholar]
  15. Cheng AL, Hsu CH, Lin JK, Hsu MM, Ho YF. et al. 2001. Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res. 21:4B2895–900 [Google Scholar]
  16. Chou TC. 2006. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 58:3621–81 [Google Scholar]
  17. Chou TC, Talalay P. 1984. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 22:27–55 [Google Scholar]
  18. Constantinou AI, White BE, Tonetti D, Yang Y, Liang W. et al. 2005. The soy isoflavone daidzein improves the capacity of tamoxifen to prevent mammary tumours. Eur. J. Cancer 41:4647–54 [Google Scholar]
  19. Crim KC, Sanders LM, Hong MW, Taddeo SS, Turner ND. et al. 2008. Upregulation of p21Waf1/Cip1 expression in vivo by butyrate administration can be chemoprotective or chemopromotive depending on the lipid component of the diet. Carcinogenesis 29:71415–20 [Google Scholar]
  20. Cruz-Correa M, Shoskes DA, Sanchez P, Zhao R, Hylind LM. et al. 2006. Combination treatment with curcumin and quercetin of adenomas in familial adenomatous polyposis. Clin. Gastroenterol. Hepatol. 4:81035–38 [Google Scholar]
  21. Dagne A, Melkamu T, Schutten MM, Qian X, Upadhyaya P. et al. 2011. Enhanced inhibition of lung adenocarcinoma by combinatorial treatment with indole-3-carbinol and silibinin in A/J mice. Carcinogenesis 32:4561–67 [Google Scholar]
  22. Davis CD, Emenaker NJ, Milner JA. 2010. Cellular proliferation, apoptosis and angiogenesis: molecular targets for nutritional preemption of cancer. Semin. Oncol. 37:3243–57 [Google Scholar]
  23. Dong X, Xu W, Sikes RA, Wu C. 2013. Combination of low dose of genistein and daidzein has synergistic preventive effects on isogenic human prostate cancer cells when compared with individual soy isoflavone. Food Chem. 141:31923–33 [Google Scholar]
  24. Fan S, Meng Q, Auborn K, Carter T, Rosen EM. 2006. BRCA1 and BRCA2 as molecular targets for phytochemicals indole-3-carbinol and genistein in breast and prostate cancer cells. Br. J. Cancer 94:3407–26 [Google Scholar]
  25. Fresco P, Borges F, Diniz C, Marques MP. 2006. New insights on the anticancer properties of dietary polyphenols. Med. Res. Rev. 26:6747–66 [Google Scholar]
  26. Garcea G, Berry DP, Jones DJ, Singh R, Dennison AR. et al. 2005. Consumption of the putative chemopreventive agent curcumin by cancer patients: assessment of curcumin levels in the colorectum and their pharmacodynamic consequences. Cancer Epidemiol. Biomark. Prev. 14:1120–25 [Google Scholar]
  27. George J, Singh M, Srivastava AK, Bhui K, Roy P. et al. 2011a. Resveratrol and black tea polyphenol combination synergistically suppress mouse skin tumors growth by inhibition of activated MAPKs and p53. PLOS ONE 6:8e23395 [Google Scholar]
  28. George J, Singh M, Srivastava AK, Bhui K, Shukla Y. 2011b. Synergistic growth inhibition of mouse skin tumors by pomegranate fruit extract and diallyl sulfide: evidence for inhibition of activated MAPKs/NF-κB and reduced cell proliferation. Food Chem. Toxicol. 49:71511–20 [Google Scholar]
  29. Greco WR, Bravo G, Parsons JC. 1995. The search for synergy: a critical review from a response surface perspective. Pharmacol. Rev. 47:2331–85 [Google Scholar]
  30. Greenwald P. 2002. Cancer chemoprevention. BMJ 324:7339714–18 [Google Scholar]
  31. Gunasekera RS, Sewgobind K, Desai S, Dunn L, Black HS, McKeehan WL, Patil B. 2007. Lycopene and lutein inhibit proliferation in rat prostate carcinoma cells. Nutr. Cancer 58:2171–77 [Google Scholar]
  32. Harper CE, Cook LM, Patel BB, Wang J, Eltoum IA. et al. 2009. Genistein and resveratrol, alone and in combination, suppress prostate cancer in SV-40 tag rats. Prostate 69:151668–82 [Google Scholar]
  33. Horie N, Hirabayashi N, Takahashi Y, Miyauchi Y, Taguchi H, Takeishi K. 2005. Synergistic effect of green tea catechins on cell growth and apoptosis induction in gastric carcinoma cells. Biol. Pharm. Bull. 28:4574–79 [Google Scholar]
  34. Hsieh TC, Wu JM. 2008. Suppression of cell proliferation and gene expression by combinatorial synergy of EGCG, resveratrol and gamma-tocotrienol in estrogen receptor-positive MCF-7 breast cancer cells. Int. J. Oncol. 33:4851–59 [Google Scholar]
  35. Hsieh TC, Wu JM. 2009. Targeting CWR22Rv1 prostate cancer cell proliferation and gene expression by combinations of the phytochemicals EGCG, genistein and quercetin. Anticancer Res. 29:104025–32 [Google Scholar]
  36. Hsu A, Bray TM, Helferich WG, Doerge DR, Ho E. 2010. Differential effects of whole soy extract and soy isoflavones on apoptosis in prostate cancer cells. Exp. Biol. Med. (Maywood) 235:190–97 [Google Scholar]
  37. Hsu A, Bruno RS, Löhr CV, Taylor AW, Dashwood RH. et al. 2011. Dietary soy and tea mitigate chronic inflammation and prostate cancer via NFκB pathway in the Noble rat model. J. Nutr. Biochem. 22:5502–10 [Google Scholar]
  38. Hsu EL, Chen N, Westbrook A, Wang F, Zhang R. et al. 2009. Modulation of CXCR4, CXCL12, and tumor cell invasion potential in vitro by phytochemicals. J. Oncol. 2009:491985 [Google Scholar]
  39. Hu Y, McIntosh GH, Le Leu RK, Nyskohus LS, Woodman RJ. et al. 2013. Combination of selenium and green tea improves the efficacy of chemoprevention in a rat colorectal cancer model by modulating genetic and epigenetic biomarkers. PLOS ONE 8:5e64362 [Google Scholar]
  40. Hutzen B, Willis W, Jones S, Chen L, Deangelis S. et al. 2009. Dietary agent, benzyl isothiocyanate inhibits signal transducer and activator of transcription 3 phosphorylation and collaborates with sulforaphane in the growth suppression of PANC-1 cancer cells. Cancer Cell Int. 9:24–27 [Google Scholar]
  41. Ip C, Ganther HE. 1991. Combination of blocking agents and suppressing agents in cancer prevention. Carcinogenesis 12:2365–67 [Google Scholar]
  42. Iwuchukwu OF, Tallarida RJ, Nagar S. 2011. Resveratrol in combination with other dietary polyphenols concomitantly enhances antiproliferation and UGT1A1 induction in Caco-2 cells. Life Sci. 88:23–241047–54 [Google Scholar]
  43. Jemal A, Siegal R, Xu J, Ward E. 2010. Cancer statistics, 2010. CA Cancer J. Clin. 60:277–300 [Google Scholar]
  44. Jeune MA, Kumi-Diaka J, Brown J. 2005. Anticancer activities of pomegranate extracts and genistein in human breast cancer cells. J. Med. Food 8:4469–75 [Google Scholar]
  45. Jiang H, Shang X, Wu H, Huang G, Wang Y. et al. 2010. Combination treatment with resveratrol and sulforaphane induces apoptosis in human U251 glioma cells. Neurochem. Res. 35:1152–61 [Google Scholar]
  46. Khafif A, Schantz SP, Chou TC, Edelstein D, Sacks PG. 1998. Quantitation of chemopreventive synergism between (−)-epigallocatechin-3-gallate and curcumin in normal, premalignant and malignant human oral epithelial cells. Carcinogenesis 19:3419–24 [Google Scholar]
  47. Klein EA, Thompson IM, Tangen CM, Crowley JJ, Lucia MS. et al. 2011. Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 306:141549–56 [Google Scholar]
  48. Kolar SS, Barhoumi R, Callaway ES, Fan Y-Y, Wang N. et al. 2007. Synergy between docosahexaenoic acid and butyrate elicits p53-independent apoptosis via mitochondrial Ca2+ accumulation in colonocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 293:5G935–943 [Google Scholar]
  49. Kramer F, Johnson IT, Doleman JF, Lund EK. 2009. A comparison of the effects of soya isoflavonoids and fish oil on cell proliferation, apoptosis and the expression of oestrogen receptors alpha and beta in the mammary gland and colon of the rat. Br. J. Nutr. 102:129–36 [Google Scholar]
  50. Kronbak R, Duus F, Vang O. 2010. Effect of 4-methoxyindole-3-carbinol on the proliferation of colon cancer cells in vitro, when treated alone or in combination with indole-3-carbinol. J. Agric. Food Chem. 58:148453–59 [Google Scholar]
  51. Kumar R, Verma V, Jain A, Jain RK, Maikhuri JP, Gupta G. 2011. Synergistic chemoprotective mechanisms of dietary phytoestrogens in a select combination against prostate cancer. J. Nutr. Biochem. 22:8723–31 [Google Scholar]
  52. Kumi-Diaka J, Merchant K, Haces A, Hormann V, Johnson M. 2010. Genistein-selenium combination induces growth arrest in prostate cancer cells. J. Med. Food 13:4842–50 [Google Scholar]
  53. Lansky EP, Jiang W, Mo H, Bravo L, Froom P. et al. 2005. Possible synergistic prostate cancer suppression by anatomically discrete pomegranate fractions. Investig. New Drugs 23:111–20 [Google Scholar]
  54. Lee JJ, Kong M, Ayers GD, Lotan R. 2007. Interaction index and different methods for determining drug interaction in combination therapy. J. Biopharm. Stat. 17:3461–80 [Google Scholar]
  55. Legg RL, Tolman JR, Lovinger CT, Lephart ED, Setchell K, Christensen MJ. 2008. Diets high in selenium and isoflavones decrease androgen-regulated gene expression in healthy rat dorsolateral prostate. Reprod. Biol. Endocrinol. 6:57 [Google Scholar]
  56. Li W, Wu JX, Tu YY. 2010. Synergistic effects of tea polyphenols and ascorbic acid on human lung adenocarcinoma SPC-A-1 cells. J. Zhejiang Univ. Sci. B 11:6458–64 [Google Scholar]
  57. Lindshield BL, Ford NA, Canene-Adams K, Diamond AM, Wallig MA, Erdman JW. 2010. Selenium, but not lycopene or vitamin E, decreases growth of transplantable dunning R3327-H rat prostate tumors. PLOS ONE 5:4e10423 [Google Scholar]
  58. Lund E. 2003. Non-nutritive bioactive constituents of plants: dietary sources and health benefits of glucosinolates. Int. J. Vitam. Nutr. Res. 73:2135–43 [Google Scholar]
  59. Majumdar AP, Banerjee S, Nautiyal J, Patel V, Du J. et al. 2009. Curcumin synergizes with resveratrol to inhibit colon cancer. Nutr. Cancer 61:4544–53 [Google Scholar]
  60. Martin KR. 2006. Targeting apoptosis with dietary bioactive agents. Exp. Biol. Med. (Maywood) 231:2117–29 [Google Scholar]
  61. Martinez-Montemayor MM, Otero-Franqui E, Martinez J, De La Mota-Peynado A, Cubano LA, Dharmawardhane S. 2010. Individual and combined soy isoflavones exert differential effects on metastatic cancer progression. Clin. Exp. Metastasis 27:7465–80 [Google Scholar]
  62. McGrath DR, Spigelman AD. 2008. Putative mechanisms of action for indole-3-carbinol in the prevention of colorectal cancer. Expert Opin. Ther. Targets 12:6729–38 [Google Scholar]
  63. Mertens-Talcott SU, Percival SS. 2005. Ellagic acid and quercetin interact synergistically with resveratrol in the induction of apoptosis and cause transient cell cycle arrest in human leukemia cells. Cancer Lett. 218:2141–51 [Google Scholar]
  64. Nakagawa H, Yamamoto D, Kiyozuka Y, Tsuta K, Uemura Y. et al. 2000. Effects of genistein and synergistic action in combination with eicosapentaenoic acid on the growth of breast cancer cell lines. J. Cancer Res. Clin. Oncol. 126:8448–54 [Google Scholar]
  65. Nakamura Y, Yogosawa S, Izutani Y, Watanabe H, Otsuji E, Sakai T. 2009. A combination of indol-3-carbinol and genistein synergistically induces apoptosis in human colon cancer HT-29 cells by inhibiting Akt phosphorylation and progression of autophagy. Mol. Cancer 8:100 [Google Scholar]
  66. Neergheen VS, Bahorun T, Taylor EW, Jen LS, Aruoma OI. 2010. Targeting specific cell signaling transduction pathways by dietary and medicinal phytochemicals in cancer chemoprevention. Toxicology 278:2229–41 [Google Scholar]
  67. Nho CW, Jeffery E. 2004. Crambene, a bioactive nitrile derived from glucosinolate hydrolysis, acts via the antioxidant response element to upregulate quinone reductase alone or synergistically with indole-3-carbinol. Toxicol. Appl. Pharmacol. 198:140–48 [Google Scholar]
  68. Osaki M, Oshimura M, Ito H. 2004. PI3K-Akt pathway: its functions and alterations in human cancer. Apoptosis 9:6667–76 [Google Scholar]
  69. Pappa G, Strathmann J, Lowinger M, Bartsch H, Gerhauser C. 2007. Quantitative combination effects between sulforaphane and 3,3-diindolylmethane on proliferation of human colon cancer cells in vitro. Carcinogenesis 28:71471–77 [Google Scholar]
  70. Pesakhov S, Khanin M, Studzinski GP, Danilenko M. 2010. Distinct combinatorial effects of the plant polyphenols curcumin, carnosic acid, and silibinin on proliferation and apoptosis in acute myeloid leukemia cells. Nutr. Cancer 62:6811–24 [Google Scholar]
  71. Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR. et al. 1992. APC mutations occur early during colorectal tumorigenesis. Nature 359:6392235–37 [Google Scholar]
  72. Power KA, Chen JM, Saarinen NM, Thompson LU. 2008. Changes in biomarkers of estrogen receptor and growth factor signaling pathways in MCF-7 tumors after short- and long-term treatment with soy and flaxseed. J. Steroid Biochem. Mol. Biol. 112:1–313–19 [Google Scholar]
  73. Power KA, Thompson LU. 2007. Can the combination of flaxseed and its lignans with soy and its isoflavones reduce the growth stimulatory effect of soy and its isoflavones on established breast cancer?. Mol. Nutr. Food Res. 51:7845–56 [Google Scholar]
  74. Pradhan SJ, Mishra R, Sharma P, Kundu GC. 2010. Quercetin and sulforaphane in combination suppress the progression of melanoma through the down-regulation of matrix metalloproteinase-9. Exp. Ther. Med. 1:6915–20 [Google Scholar]
  75. Radhakrishnan S, Reddivari L, Sciafani R, Das UN, Vanamala J. 2011. Resveratrol potentiates grape seed extract induced human colon cancer cell apoptosis. Front. Biosci. (Elite Ed.) 3:1509–23 [Google Scholar]
  76. Raj MH, Abd Elmageed ZY, Zhou J, Gaur RL, Nguyen L. et al. 2008. Synergistic action of dietary phyto-antioxidants on survival and proliferation of ovarian cancer cells. Gynecol. Oncol. 110:3432–38 [Google Scholar]
  77. Ramos S. 2008. Cancer chemoprevention and chemotherapy: dietary polyphenols and signalling pathways. Mol. Nutr. Food Res. 52:5507–26 [Google Scholar]
  78. Rao CV, Reddy BS. 2004. NSAIDs and chemoprevention. Curr. Cancer Drug Targets 4:129–42 [Google Scholar]
  79. Reagan-Shaw S, Nihal M, Ahsan H, Mukhtar H, Ahmad N. 2008. Combination of vitamin E and selenium causes an induction of apoptosis of human prostate cancer cells by enhancing Bax/Bcl-2 ratio. Prostate 68:151624–34 [Google Scholar]
  80. Roy MJ, Dionne S, Marx G, Qureshi I, Sarma D. et al. 2009. In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition 25:11–121193–201 [Google Scholar]
  81. Saarinen NM, Power K, Chen J, Thompson LU. 2006. Flaxseed attenuates the tumor growth stimulating effect of soy protein in ovariectomized athymic mice with MCF-7 human breast cancer xenografts. Int. J. Cancer 119:4925–31 [Google Scholar]
  82. Saha A, Kuzuhara T, Echigo N, Suganuma M, Fujiki H. 2010. New role of (−)-epicatechin in enhancing the induction of growth inhibition and apoptosis in human lung cancer cells by curcumin. Cancer Prev. Res. (Phila.) 3:8953–62 [Google Scholar]
  83. Sakamoto K. 2000. Synergistic effects of thearubigin and genistein on human prostate tumor cell (PC-3) growth via cell cycle arrest. Cancer Lett. 151:1103–9 [Google Scholar]
  84. Saw CL, Cintron M, Wu TY, Guo Y, Huang Y. et al. 2011. Pharmacodynamics of dietary phytochemical indoles I3C and DIM: induction of Nrf2-mediated phase II drug metabolizing and antioxidant genes and synergism with isothiocyanates. Biopharm. Drug Dispos. 32:5289–300 [Google Scholar]
  85. Schwartz B, Birk Y, Raz A, Madar Z. 2004. Nutritional-pharmacological combinations—a novel approach to reducing colon cancer incidence. Eur. J. Nutr. 43:4221–29 [Google Scholar]
  86. Seeram NP, Adams LS, Hardy ML, Heber D. 2004. Total cranberry extract versus its phytochemical constituents: antiproliferative and synergistic effects against human tumor cell lines. J. Agric. Food Chem. 52:92512–17 [Google Scholar]
  87. Seeram NP, Adams LS, Henning SM, Niu Y, Zhang Y. et al. 2005. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J. Nutr. Biochem. 16:6360–67 [Google Scholar]
  88. Sengupta A, Ghosh S, Das S. 2003. Tomato and garlic can modulate azoxymethane-induced colon carcinogenesis in rats. Eur. J. Cancer Prev. 12:3195–200 [Google Scholar]
  89. Sengupta A, Ghosh S, Das S. 2004. Modulatory influence of garlic and tomato on cyclooxygenase-2 activity, cell proliferation and apoptosis during azoxymethane induced colon carcinogenesis in rat. Cancer Lett. 208:2127–36 [Google Scholar]
  90. Shen G, Khor TO, Hu R, Yu S, Nair S. et al. 2007. Chemoprevention of familial adenomatous polyposis by natural dietary compounds sulforaphane and dibenzoylmethane alone and in combination in ApcMin/+mouse. Cancer Res. 67:209937–44 [Google Scholar]
  91. Siler U, Barella L, Spitzer V, Schnow Lein M. et al. 2004. Lycopene and vitamin E interfere with autocrine/paracrine loops in the Dunning prostate cancer model. FASEB J. 18:91019–21 [Google Scholar]
  92. Svehliková V, Wang S, Jakubikova J, Williamson G, Mithen R, Bao Y. 2004. Interactions between sulforaphane and apigenin in the induction of UGT1A1 and GSTA1 in CaCo-2 cells. Carcinogenesis 25:91629–37 [Google Scholar]
  93. Tanaka T, Makita H, Kawabata K, Mori H, Kakumoto M. et al. 1997. Chemoprevention of azoxymethane-induced rat colon carcinogenesis by the naturally occurring flavonoids, diosmin and hesperidin. Carcinogenesis 18:5957–65 [Google Scholar]
  94. Tang FY, Cho HJ, Pai MH, Chen YH. 2009. Concomitant supplementation of lycopene and eicosapentaenoic acid inhibits the proliferation of human colon cancer cells. J. Nutr. Biochem. 20:6426–34 [Google Scholar]
  95. Tang SN, Singh C, Nall D, Meeker D, Shankar S, Srivastava RK. 2010. The dietary bioflavonoid quercetin synergizes with epigallocathechin gallate (EGCG) to inhibit prostate cancer stem cell characteristics, invasion, migration and epithelial-mesenchymal transition. J. Mol. Signal. 5:14 [Google Scholar]
  96. Tolman JR, Lephart ED, Setchell KD, Eggett DL, Christensen MJ. 2008. Timing of supplementation of selenium and isoflavones determines prostate cancer risk factor reduction in rats. Nutr. Metab. (Lond.) 5:31 [Google Scholar]
  97. Tsuda H, Ohshima Y, Nomoto H, Fujita KI, Matsuda E. et al. 2004. Cancer prevention by natural compounds. Drug Metab. Pharmacokinet. 19:4245–63 [Google Scholar]
  98. Vaishampayan U, Hussain M, Banerjee M, Seren S, Sarkar FH. et al. 2007. Lycopene and soy isoflavones in the treatment of prostate cancer. Nutr. Cancer 59:11–7 [Google Scholar]
  99. Velmurugan B, Mani A, Nagini S. 2005. Combination of S-allylcysteine and lycopene induces apoptosis by modulating Bcl-2, Bax, Bim and caspases during experimental gastric carcinogenesis. Eur. J. Cancer Prev. 14:4387–93 [Google Scholar]
  100. Venkateswaran V, Fleshner NE, Klotz LH. 2004. Synergistic effect of vitamin E and selenium in human prostate cancer cell lines. Prostate Cancer Prostatic Dis. 7:154–56 [Google Scholar]
  101. Venkateswaran V, Klotz LH, Ramani M, Sugar LM, Jacob LE. et al. 2009. A combination of micronutrients is beneficial in reducing the incidence of prostate cancer and increasing survival in the Lady transgenic model. Cancer Prev. Res. (Phila.) 2:5473–83 [Google Scholar]
  102. Verma SP, Salamone E, Goldin B. 1997. Curcumin and genistein, plant natural products, show synergistic inhibitory effects on the growth of human breast cancer MCF-7 cells induced by estrogenic pesticides. Biochem. Biophys. Res. Commun. 233:3692–96 [Google Scholar]
  103. Vicinanza R, Zhang Y, Henning SM, Heber D. 2013. Pomegranate juice metabolites, ellagic acid and urolithin A, synergistically inhibit androgen-independent prostate cancer cell growth via distinct effects on cell cycle control and apoptosis. Evid. Based Complement. Altern. Med. 2013:247504 [Google Scholar]
  104. Vieira A, Heidor R, Cardozo MT, Scolastici C, Purgatto E. et al. 2011. Efficacy of geraniol but not of beta-ionone or their combination for the chemoprevention of rat colon carcinogenesis. Braz. J. Med. Biol Res. 44:6538–45 [Google Scholar]
  105. Wang P, Heber D, Henning SM. 2012. Quercetin increased bioavailability and decreased methylation of green tea polyphenols in vitro and in vivo. Food Funct. 3:6635–42 [Google Scholar]
  106. Wang Z, Desmoulin S, Banerjee S, Kong D, Li Y. et al. 2008. Synergistic effects of multiple natural products in pancreatic cancer cells. Life Sci. 83:7–8293–300 [Google Scholar]
  107. Willard ST, Frawley LS. 1998. Phytoestrogens have agonistic and combinatorial effects on estrogen-responsive gene expression in MCF-7 human breast cancer cells. Endocrine 8:2117–21 [Google Scholar]
  108. Xiao H, Yang CS. 2008. Combination regimen with statins and NSAIDs: a promising strategy for cancer chemoprevention. Int. J. Cancer 123:5983–90 [Google Scholar]
  109. Xu G, Ren G, Yuan H, Wang Z, Kang L. et al. 2010. Combination of curcumin and green tea catechins prevents dimethylhydrazine-induced colon carcinogenesis. Food Chem. Toxicol. 48:1390–95 [Google Scholar]
  110. Yang J, Liu RH. 2009. Synergistic effect of apple extracts and quercetin 3-β-D-glucoside combination on antiproliferative activity in MCF-7 human breast cancer cells in vitro. J. Agric. Food Chem. 57:188581–86 [Google Scholar]
  111. Yi W, Wetzstein HY. 2011. Anti-tumorigenic activity of five culinary and medicinal herbs grown under greenhouse conditions and their combination effects. J. Sci. Food Agric. 91:101849–54 [Google Scholar]
  112. Zhou JR, Li L, Pan W. 2007. Dietary soy and tea combinations for prevention of breast and prostate cancers by targeting metabolic syndrome elements in mice. Am. J. Clin. Nutr. 86:3s882–88 [Google Scholar]
  113. Zhou JR, Yu L, Mai Z, Blackburn GL. 2004. Combined inhibition of estrogen-dependent human breast carcinoma by soy and tea bioactive components in mice. Int. J. Cancer 108:18–14 [Google Scholar]
  114. Zhou JR, Yu L, Zhong Y, Blackburn GL. 2003. Soy phytochemicals and tea bioactive components synergistically inhibit androgen-sensitive human prostate tumors in mice. J. Nutr. 133:2516–21 [Google Scholar]
  115. Zuniga KE, Clinton SK, Erdman JW. 2013. The interactions of dietary tomato powder and soy germ on prostate carcinogenesis in the TRAMP model. Cancer Prev. Res. (Phila.) 6:6548–57 [Google Scholar]
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