European Journal of Cancer
Volume 41, Issue 13 , Pages 1842-1853 , September 2005

Inhibition of survival signalling by dietary polyphenols and indole-3-carbinol

Received 1 March 2005 ,Accepted 3 May 2005.

References 

  1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70
  2. Surh Y-J. Cancer chemoprevention with dietary phytochemicals. Nature Revs Cancer. 2003;3:768–780
  3. Murphy LO, Smith S, Chen R-H, et al. Molecular interpretation of ERK signal duration by immediate early gene products. Nature Cell Biol. 2002;4:556–564
  4. Sebolt-Leopold JS, Herrera R. Targeting the mitogen-activated protein kinase cascade to treat cancer. Nature Revs Cancer. 2004;4:937–947
  5. Collett GP, Campbell FC. Curcumin induces c-jun N-terminal kinase-dependent apoptosis in HCT116 human colon cancer cells. Carcinogenesis. 2004;25:2183–2189
  6. Chen Y-R, Tan T-H. Inhibition of the c-jun N-terminal kinase (JNK) signalling pathway by curcumin. Oncogene. 1998;17:173–178
  7. Vivanco I, Sawyers CL. The phosphatidylinositol-3-kinase-AKT pathway in human cancer. Nature Revs Cancer. 2002;2:489–501
  8. Perkins ND. NF-κB: tumour promoter or suppressor?. Trends Cell Biol. 2004;14:64–69
  9. Darnell JE. Transcription factors as targets for cancer therapy. Nature Revs Cancer. 2002;2:740–749
  10. Pikarsky E, Porat RM, Stein I, et al. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature. 2004;431:461–466
  11. Ozes ON, Mayo LD, Gustin JA, et al. NF-κB activation by tumour necrosis factor requires the Akt serine–threonine kinase. Nature. 1999;401:82–85
  12. Romashkova JA, Makarov SS. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 1999;401:86–90
  13. Madrid LV, Mayo MW, Reuther JY, et al. Akt stimulates the transactivation potential of the RelA/p65 subunit of NF-κB through utilization of the IκB kinase and activation of the mitogen activated protein kinase p38. J Biol Chem. 2001;276:18934–18940
  14. Meng F, Liu L, Chin PC, et al. Akt is a downstream target of NF-κB. J Biol Chem. 2002;277:29674–29680
  15. Calo V, Migliavacca M, Bazan V, et al. STAT proteins: from normal control of cellular events to tumorigenesis. J Cell Physiol. 2003;197:157–168
  16. Yu H, Jove R. The STATs of cancer – new molecular targets come of age. Nature Revs Cancer. 2004;4:97–105
  17. Yoshikawa H, Matsubara K, Qian G-S, et al. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nature Genetics. 2001;28:29–35
  18. Ungureanu D, Vanhatupa S, Kotaja N, et al. PIAS proteins promote SUMO-1 conjugation to STAT-1. Blood. 2003;102:3311–3313
  19. Anto RJ, Mukhopadhyay A, Denning K, et al. Curcumin (diferuloylmethane) induces apoptosis through activation of caspase-8, BID cleavage and cytochrome c release: its suppression by ectopic expression of Bcl-2 and Bcl-xL. Carcinogenesis. 2002;23:143–150
  20. Bharti AC, Donato N, Aggarwal BB. Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J Immunol. 2003;171:3863–3871
  21. Brennan P, O’Neill LAJ. Inhibition of nuclear factor κB by direct modification in whole cells – mechanism of action of nordihydroguariaritic acid, curcumin and thiol modifiers. Biochem Pharmacol. 1998;55:965–973
  22. Bush JA, Cheung KJJ, Li G. Curcumin induces apoptosis in human melanoma cells through a Fas receptor/caspase 8 pathway independent of p53. Expt Cell Res. 2001;271:305–314
  23. Choudhuri T, Pal S, Agwarwal ML, et al. Curcumin induces apoptosis in human breast cancer cells through p53-dependent Bax induction. FEBS Lett. 2002;512:334–340
  24. Han S-S, Chung S-T, Robertson DA, et al. Curcumin causes the growth arrest and apoptosis of B-cell lymphoma by downregulation of egr-1, c-myc, Bcl-XL, NF-κB and p53. Clin Immunol. 1999;93:152–161
  25. Hong R-L, Spohn WH, Hung M-C. Curcumin inhibits tyrosine kinase activity of p185neuand also depletes p185neu. Clin Cancer Res. 1999;5:1884–1891
  26. Jaiswal AS, Marlow BP, Gupta N, et al. β-Catenin-mediated transactivation and cell-cell adhesion pathways are important in curcumin (diferuylmethane)-induced growth arrest and apoptosis in colon cancer cells. Oncogene. 2002;21:8414–8427
  27. Jana NR, Dikshit P, Goswami A, et al. Inhibition of proteosomal function by curcumin induces apoptosis through mitochondrial pathway. J Biol Chem. 2004;279:11680–11685
  28. Jee S-H, Shen S-C, Tseng C-R, et al. Curcumin induces a p53 dependent apoptosis in human basal cell carcinoma cells. J Invest Dermatol. 1998;111:656–661
  29. Jobin C, Bradham CA, Russo MP, et al. Curcumin blocks cytokine–mediated NF-κB activation and proinflammatory gene expression by inhibiting inhibitory factor I-κB kinase. J Immunol. 1999;163:3474–3483
  30. Kakar SS, Roy D. Curcumin inhibits TPA-induced expression of c-fos, c-jun and c-myc proto-oncogenes messenger RNAs in mouse skin. Cancer Lett. 1994;87:85–89
  31. Kim HY, Park EJ, Joe E-h, et al. Curcumin suppresses Janus kinase-STAT inflammatory signaling through activation of src homology 2 domain-containing tyrosine phosphatase 2 in brain microglia. J Immunol. 2003;171:6072–6079
  32. Korutla L, Cheung JY, Mendelsohn J, et al. Inhibition of ligand-induced activation of epidermal growth factor receptor tyrosine phosphorylation by curcumin. Carcinogenesis. 1995;16:1741–1745
  33. Li L, Aggarwal BB, Shishodia S, et al. Nuclear factor-κB and IκB are constitutively active in human pancreatic cells and their downregulation by curcumin (diferuloylmethane) is associated with the suppression of proliferation and induction of apoptosis. Cancer. 2004;101:2351–2362
  34. Liu J-Y, Lin S-J, Lin J-K. Inhibitory effects of curcumin on protein kinase C activity induced by 12-O-tetradecanoyl-phorbol-13-acetate in NIH3T3 cells. Carcinogenesis. 1993;14:857–861
  35. Moragoda L, Jaszewski R, Majumdar APN. Curcumin induced modulation of cell cycle and apoptosis in gastric and colon cancer cells. Anticancer Res. 2001;21:873–878
  36. Mukhopadhyay A, Banerjee S, Stafford LJ, et al. Curcumin-induced suppression of cell proliferation correlates with downregulation of cyclin D1 expression and CDK4-mediated retinoblastoma protein phosphorylation. Oncogene. 2002;21:8852–8861
  37. Mukhopadhyay A, Ramos CB, Chatterjee D, et al. Curcumin downregulates cell survival mechanisms in human prostate cancer cell lines. Oncogene. 2001;20:7597–7609
  38. Plummer SM, Holloway KA, Manson MM, et al. Inhibition of cyclo-oxygenase 2 expression in colon cells by the chemopreventive agent curcumin involves inhibition of NF-κB activation via the NIK/IKK signalling complex. Oncogene. 1999;18:6013–6020
  39. Prusty BK, Das BC. Constitutive activation of transcription factor AP-1 in cervical cancer and suppression of human papillomavirus (HPV) transcription and AP-1 activity in HeLa cells by curcumin. Int J Cancer. 2005;113:951–960
  40. Ramachandran C, You W. Differential sensitivity of human mammary epithelial and breast carcinoma cell lines to curcumin. Breast Cancer Res Treat. 1999;54:269–278
  41. Rashmi R, Kumar S, Karunagaran D. Ectopic expression of Bcl-XL or Ku70 protects human colon cancer cells (SW480) against curcumin-induced apoptosis while their downregulation potentiates it. Carcinogenesis. 2004;25:1867–1877
  42. Scott DW, Loo G. Curcumin-induced GADD153 gene upregulation in human colon cancer cells. Carcinogenesis. 2004;25:2155–2164
  43. Shao Z-M, Shen Z-Z, Liu C-H, et al. Curcumin exerts multiple suppressive effects on human breast carcinoma cells. Int J Cancer. 2002;98:234–240
  44. Squires MS, Hudson EA, Howells L, et al. Relevance of mitogen activated protein kinase (MAPK) and phosphotidylinositol-3-kinase/protein kinase B (PI3K/PKB) pathways to induction of apoptosis by curcumin in breast cells. Biochem Pharmacol. 2003;65:361–376
  45. Surh Y-J, Chun K-S, Cha H-H, et al. Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: downregulation of COX-2 and iNOS through suppression of NF-κB activation. Mut Res. 2001;480–481:243–268(and references therein)
  46. Woo J-H, Kim Y-H, Choi Y-J, et al. Molecular mechanisms of curcumin-induced cytotoxicity: induction of apoptosis through generation of reactive oxygen species, downregulation of Bcl-Xl and IAP, the release of cytochrome c and inhibition of Akt. Carcinogenesis. 2003;24:1199–1280
  47. Zheng S, Chen A. Activation of PPARγ is required for curcumin to induce apoptosis and to inhibit the expression of extracellular matrix genes in hepatic stellate cells in vitro. Biochem J. 2004;384:149–157
  48. Ahmad N, Gupta S, Mukhtar H. Green tea polyphenol epigallocatechin gallate differentially modulates nuclear factor κB in cancer cells versus normal cells. Arch Biochem Biophys. 2000;376:338–346
  49. Ahn H-Y, Hadizadeh KR, Seul C, et al. Epigallocatechin-3 gallate selectively inhibits the PDGF-BB-induced intracellular signalling transduction pathway in vascular smooth muscle cells and inhibits transformation of sis-transfected NIH 3T3 fibroblasts and human glioblastoma cells (A172). Mol Biol Cell. 1999;10:1093–1104
  50. Ahn SC, Kim GY, Kim JH, et al. Epigallocatechin-3-gallate, constituent of green tea, suppresses the LPS-induced phenotypic and functional maturation of murine dendritic cells through inhibition of mitogen-activated protein kinases and NF-κB. Biochem Biophys Res Comm. 2004;313:148–155
  51. Chen C, Shen G, Hebbar V, et al. Epigallocatechin-3-gallate-induced stress signals in HT-29 human colon adenocarcinoma cells. Carcinogenesis. 2003;24:1369–1378
  52. Chen JJ, Ye Z-Q, Koo MWL. Growth inhibition and cell cycle arrest effects of epigallocatechin gallate in the NBT-II bladder tumour cell line. BJU Int. 2004;93:1082–1086
  53. Cheng XW, Kuzuya M, Kanda S. Epigallocatechin-3-gallate binding to MMP-2 inhibits gelatinolytic activity without influencing the attachment to extracellular matrix proteins but enhances MMP-2 binding to TIMP-2. Arch Biochem Biophys. 2003;415:126–132
  54. Chung JY, Huang C, Meng X, et al. Inhibition of activator protein 1 activity and cell growth by purified green tea and black tea polyphenols in H-ras- transformed cells: structure–activity relationship and mechanisms involved. Cancer Res. 1999;59:4610–4617
  55. Dashwood W-M, Orner GA, Dashwood RH. Inhibition of β-catenin/Tcf activity by white tea, green tea, and epigallocatechin-3-gallate (EGCG): minor contribution of H2O2 at physiologically relevant EGCG concentrations. Biochem Biophys Res Commun. 2002;296:584–588
  56. Fang MZ, Wang Y, Ai N. Tea polyphenol (−)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res. 2003;63:7563–7570
  57. Gupta S, Hastak K, Afaq F, et al. Essential role of caspases in epigallocatechin-3-gallate-mediated inhibition of nuclear factor κB and induction of apoptosis. Oncogene. 2004;23:2507–2522
  58. Hastak K, Gupta S, Ahmad N, et al. Role of p53 and NF-kB in epigallocatechin-3-gallate-induced apoptosis of LNCaP cells. Oncogene. 2003;22:4851–4859
  59. Hong J, Smith TJ, Ho C-T, et al. Effects of purified green and black tea polyphenols on cyclooxygenase and lipoxygenase-dependent metabolism of arachidonic acid in human colon mucosa and colon tumour tissues. Biochem Pharmacol. 2001;62:1175–1183
  60. Hsu S, Lewis J, Singh B, et al. Green tea polyphenol targets the mitochondria in tumour cells inducing caspase 3-dependent apoptosis. Anticancer Res. 2003;23:1533–1539
  61. Hussain T, Gupta S, Adhami VM, et al. Green tea constituent epigallcatechin-3-gallate selectively inhibits COX-2 without affecting COX-1 expression in human prostate cancer cells. Int J Cancer. 2005;113:660–669
  62. Jeong W-S, Kim I-W, Hu R, et al. Modulation of AP-1 by natural chemopreventive compounds in human colon HT-29 cancer cell line. Pharm Res. 2004;21:649–660
  63. Kim HS, Kim MH, Jeong M, et al. EGCG blocks tumor promoter-induced MMP-9 expression via suppression of MAPK and AP-1 activation in human gastric AGC cells. Anticancer Res. 2004;24:747–753
  64. Kuo PL, Lin CC. Green tea constituent (−)-epigallocatechin-3-gallate inhibits HepG2 cell proliferation and induces apoptosis through p53-dependent and Fas-mediated pathways. J Biomed Sci. 2003;10:219–227
  65. Lambert JD, Yang CS. Mechanisms of cancer prevention by green tea. J Nutr. 2003;133:3262S–3267S(and references therein)
  66. Lamy S, Gingras D, Beliveau R. Green tea catechins inhibit vascular endothelial growth factor receptor phosphorylation. Cancer Res. 2002;62:381–385
  67. Lee YK, Bone ND, Strege AK, et al. VEGF receptor phosphorylation status and apoptosis is modulated by a green tea component epigallocatechin-3-gallate (EGCG) in B-cell chronic lymphocytic leukemia. Blood. 2004;104:788–794
  68. Leone M, Zhai D, Sarth S, et al. Cancer prevention by tea polyphenols is linked to their direct inhibition of antiapoptotic Bcl-2-family proteins. Cancer Res. 2003;63:8118–8121
  69. Liang Y-C, Lin-Shiau S-Y, Chen C-F, et al. Suppression of extracellular signals and cell proliferation through EGF receptor binding by (−)-epigallocatechin gallate in human A431 epidermoid carcinoma cells. J Cell Biochem. 1997;67:55–65
  70. Lin J-K, Liang Y-C, Lin-Shiau S-Y. Cancer chemoprevention by tea polyphenols through mitotic signal transduction blockade. Biochem Pharmacol. 1999;58:911–915
  71. Maeda-Yamamoto M, Susuki N, Sawai Y, et al. Association of suppression of extracellular signal-related kinase phosphorylation by epigallocatechin gallate with the reduction of matrix metalloproteinase activities in human fibrosarcoma HT1080 cells. J Agric Food Chem. 2003;51:1858–1863
  72. Masuda M, Suzui M, Lim JTE, et al. Epigallocatechin-3-gallate inhibits activation of Her-2/Neu and downstream signaling pathways in human head and neck and breast carcinoma cells. Clin Cancer Res. 2003;9:3486–3491
  73. Masuda M, Suzui M, Weinstein IB. Effects of epigallocatechin-3-gallate on growth, epidermal growth factor receptor signaling pathways, gene expression and chemosensitivity in human head and neck squamous cell carcinoma cell lines. Clin Cancer Res. 2001;7:4220–4229
  74. Mittal A, Pate MS, Wylie RC, et al. EGCG downregulates telomerase in human breast carcinoma MCF-7 cells, leading to suppression of cell viability and induction of apoptosis. Int J Oncol. 2004;24:703–710
  75. Nomura M, Kaji A, He Z, et al. Inhibitory mechanisms of tea polyphenols on the ultraviolet B-activated phosphatidylinositol 3 kinase-dependent pathway. J Biol Chem. 2001;276:46624–46631
  76. Pianetti S, Guo S, Kavanagh KT, et al. Green tea polyphenol epigallocatechin-3 gallate inhibits Her-2/Neu signalling, proliferation and transformed phenotype of breast cancer cells. Cancer Res. 2002;62:652–655
  77. Roy AM, Baliga MS, Katiyar SK. Epigallocatechin gallate induces apoptosis in estrogen receptor-negative breast carcinoma cells via modulation in protein expression of p53 and Bax and caspase activation. Mol Cancer Ther. 2005;4:81–90
  78. Sah JF, Balasubramanian S, Eckert RL, et al. Epigallocatechin-3-gallate inhibits epidermal growth factor receptor signaling pathway. J Biol Chem. 2004;279:12755–12762
  79. Sartippour MR, Shao ZM, Heber D, et al. Green tea inhibits vascular endothelial growth factor (VEGF) induction in human breast cancer cells. J Nutr. 2002;132:2307–2311
  80. Siddiqui IA, Adhami VM, Afaq F, et al. Modulation of phosphatidylinositol-3-kinase/protein kinase B- and mitogen-activated protein kinase pathways by tea polyphenols in human prostate cancer cells. J Cell Biochem. 2004;91:232–242
  81. Tachibana H, Koga K, Fujimura Y, et al. A receptor for green tea polyphenol EGCG. Nature Struct Mol Biol. 2004;11:380–381
  82. Tang F-Y, Nguyen N, Meydani M. Green tea catechins inhibit VEGF-induced angiogenesis in vitro through suppression of VE-cadherin phosphorylation and inactivation of Akt molecule. Int J Cancer. 2003;106:871–878
  83. Vayalil PK, Katiyar SK. Treatment of epigallocatechin-3-gallate inhibits matrix metalloproteinases-2 and -9 via inhibition of activation of mitogen-activated protein kinases, c-jun, and NF-κB in human prostate carcinoma DU-145 cells. Prostate. 2004;59:33–42
  84. Yang FJ, Oz HS, Barve S, et al. The green tea polyphenol (−)-epigallocatechin-3-gallate blocks nuclear factor-κB activation by inhibiting IκB kinase activity in the intestinal epithelial cell line IEC-6. Mol Pharmacol. 2001;60:528–533
  85. Yokoyama M, Noguchi M, Nakao Y, et al. The tea polyphenol (−)-epigallocatechin gallate effects on growth, apoptosis and telomerase activity in cervical cell lines. Gynecol Oncol. 2004;92:197–204
  86. Aggarwal BB, Bhardwaj A, Aggarwal RS, et al. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res. 2004;24:2783–2840
  87. Ahmad N, Adhami VM, Afaq F, et al. Resveratrol causes WAF-1/p21-mediated G1-phase arrest of cell cycle and induction of apoptosis in human epidermoid carcinoma cells. Clin Cancer Res. 2001;7:1466–1473
  88. Aristotle L, Yeger H. Curcumin and resveratrol induce apoptosis and nuclear translocation and activation of p53 in human neuroblastoma. Anticancer Res. 2004;24:987–998
  89. Bannerjee S, Bueso-Ramos C, Aggarwal BB. Suppression of 7,12-dimethylbenz (a)anthracene-induced mammary carcinogenesis in rats by resveratrol: role of nuclear factor-κB, cyclooxygenase 2 and matrix metalloproteinase 9. Cancer Res. 2002;62:4945–4954
  90. Bhat KPL, Lantvit D, Christov K, et al. Estrogenic and antiestrogenic properties of resveratrol in mammary tumor models. Cancer Res. 2001;61:7456–7463
  91. Chen Y, Tseng SH, Lai HS, et al. Resveratrol-induced cellular apoptosis and cell cycle arrest in neuroblastoma cells and antitumor effects on neuroblastoma in mice. Surgery. 2004;136:57–66
  92. Delmas D, Rebe C, Micheau O, et al. Redistribution of CD95, DR4 and DR5 in rafts accounts for the synergistic toxicity of resveratrol and death receptor ligands in colon carcinoma cells. Oncogene. 2004;23:8979–8986
  93. Fulda S, Debatin K-M. Sensitization for anticancer drug-induced apoptosis by the chemopreventive agent resveratrol. Oncogene. 2004;23:6702–6711
  94. Gusman J, Malonne H, Atassi G. A reappraisal of the potential chemopreventive and chemotherapeutic properties of resveratrol. Carcinogenesis. 2001;22:1111–1117(and references therein)
  95. Kim YA, Lee WH, Choi TH, et al. Involvement of p21WAF1/CIP1, pRB, Bax and NF-κB in induction of growth arrest and apoptosis by resveratrol in human lung carcinoma A549 cells. Int J Oncol. 2003;23:1143–1149
  96. Kuwajerwala N, Cifuentes E, Gautam S, et al. Resveratrol induces prostate cancer cell entry into S phase and inhibits DNA synthesis. Cancer Res. 2002;62:2488–2492
  97. Lee HS, Sur EY, Kim WK. Resveratrol induces apoptosis in SW480 human colon cancer cell lines. Food Sci BioTech. 2004;13:80–84
  98. Liang YC, Tsai SH, Chen L, et al. Resveratrol-induced G(2) arrest through the inhibition of CDK7 and p34 (CDC2) kinases in colon carcinoma HT29 cells. Biochem Pharmacol. 2003;65:1053–1060
  99. Lin MT, Yen ML, Lin CY, et al. Inhibition of vascular endothelial growth factor-induced angiogenesis by resveratrol through interruption of Src-dependent vascular endothelial cadherin tyrosine phosphorylation. Mol Pharmacol. 2003;64:1029–1036
  100. Mahyar-Roemer M, Kohler H, Roemer K. Role of Bax in resveratrol-induced apoptosis of colorectal carcinoma cells. BMC Cancer. 2002;2:27
  101. Mutoh M, Takahashi M, Fukuda K, et al. Suppression of cyclooxygenase-2 promoter-dependent transcriptional activity in colon cancer cells by chemopreventive agents with a resorcin-type structure. Carcinogenesis. 2000;21:959–963
  102. Narayanan BA, Narayanan NK, Re GG, et al. Differential expression of genes induced by resveratrol in LNCAP cells: p53-mediated molecular targets. Int J Cancer. 2003;104:204–212
  103. Pozo-Guisado E, Lorenzo-Benayas MJ, Fernandez-Salguero PM. Resveratrol modulates the phosphoinositide 3-kinase pathway through an estrogen receptor α-dependent mechanism: relevance in cell proliferation. Int J Cancer. 2004;109:167–173
  104. Reagan-Shaw S, Afaq F, Aziz MH, et al. Modulations of critical cell cycle regulatory events during chemoprevention of ultraviolet B-mediated responses by resveratrol in SKH-1 hairless mouse skin. Oncogene. 2004;23:5151–5160
  105. Slater SJ, Seiz JL, Cook AC, et al. Inhibition of protein kinase C by resveratrol. Biochim Biophys Acta. 2003;1637:59–69
  106. Su J-L, Lin M-T, Hong C-C, et al. Resveratrol induces FasL-related apoptosis through Cdc42 activation of ASK1/JNK-dependent signaling pathway in human leukemia HL-60 cells. Carcinogenesis. 2005;26:1–10
  107. Szewczuk LM, Forti L, Stivala LA, et al. Resveratrol is a peroxidase-mediated inactivator of COX-1 but not COX-2. A mechanistic approach to the design of COX-1 selective agents. J Biol Chem. 2004;279:22727–22737
  108. Woo JH, Lim JH, Kim YH, et al. Resveratrol inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting JNK and PKC δ signal transduction. Oncogene. 2004;23:1845–1853
  109. Yang S, Meyskens FL. Alterations in activating protein 1 composition correlate with phenotypic differentiation changes induced by resveratrol in human melanoma. Mol Pharmacol. 2005;67:298–308
  110. Chinni SR, Sarkar FH. Akt inactivation is a key event in indole-3-carbinol-induced apoptosis in PC-3 cells. Clin Cancer Res. 2002;8:1228–1236
  111. Cover CM, Hsieh SJ, Tran SH, et al. Indole-3-carbinol inhibits the expression of cycli-dependent kinase-6 and induces a G1 cell cycle arrest of human breast cancer cells independent of estrogen receptor signalling. J Biol Chem. 1998;273:3838–3847
  112. Howells L, Gallacher-Horley B, Houghton CE, et al. Indole-3-carbinol inhibits Akt/PKB and induces apoptosis in the human breast tumor cell line MDA MB468, but not in the non-tumorigenic HBL100 line. Mol Cancer Ther. 2002;1:1161–1172
  113. IARC Handbooks of Cancer Prevention. Cruciferous vegetables, isothiocyanates and indoles. In: Cancer preventive effects, vol. 9. IARC: Lyon; 2004. p. 43–176. Chapter 4 [and references therein].
  114. Lee IJ, Han F, Baek J, et al. Inhibition of MUC1 expression by indole-3-carbinol. Int J Cancer. 2004;109:810–816
  115. Lian JP, Word B, Taylor S, et al. Modulation of the constitutive activated STAT3 transcription factor in pancreatic cancer prevention: effects of indole-3-carbinol (I3C) and genistein. Anticancer Res. 2004;24:133–137
  116. Matsuzaki Y, Koyama M, Hitomi T, et al. Indole-3-carbinol activates the cyclin-dependent kinase inhibitor p15 INK4b gene. FEBS Lett. 2004;576:137–140
  117. Rahman KMW, Li Y, Sarkar FH. Inactivation of Akt and NF-κB play important roles during indole-3-carbinol-induced apoptosis in breast cancer cells. Nutr Cancer. 2004;48:84–94
  118. Meng Q, Qi M, Chen D-Z, et al. Suppression of breast cancer invasion and migration by indole-3-carbinol: associated with up-regulation of BRCA1 and E-cadherin/catenin complexes. J Mol Med. 2000;78:155–165
  119. Li Y, Chinni SR, Sarkar FH. Selective growth regulatory and pro-apoptotic effects of DIM are mediated by Akt and NF-κB pathways in prostate cancer cells. Frontiers Biosci. 2005;10:236–243
  120. Rahman KMW, Sarkar FH. Inhibition of nuclear translocation of nuclear factor-κB contributes to 3,3′-diindolylmethane-induced apoptosis in breast cancer cells. Cancer Res. 2005;65:364–371
  121. Natarajan C, Bright JJ. Curcumin inhibits experimental allergic encephalomyelitis by blocking IL12 signaling through Janus kinase-STAT pathway in T lymphocytes. J Immunol. 2002;169:6506–6513
  122. Li WQ, Dehnade F, Zafarullah M. Oncostatin M-induced matrix metalloproteinase and tissue inhibitor of metalloproteinase-3 genes expression in chondrocytes requires Janus kinase/STAT signaling pathway. J Immunol. 2001;166:3491–3498
  123. Torrance CJ, Jackson PE, Montgomery E, et al. Combinatorial chemoprevention of intestinal neoplasia. Nature Med. 2000;6:1024–1028
  124. Donald S, Verschoyle RD, Greaves P, et al. Dietary agent indole-3-carbinol protects female rats against the hepatotoxicity of the antitumor drug ET743 (Trabectidin) without compromising efficacy in a rat mammary carcinoma. Int J Cancer. 2004;111:961–967
  125. Suganuma M, Okabe S, Kai Y, et al. Synergistic effects of (−)-epigallocatechin gallate with (−)-epicatechin, sulindac, or tamoxifen on cancer preventive activity in the human lung cancer cell line PC-9. Cancer Res. 1999;59:44–47
  126. Orner GA, Dashwood W-M, Blum CA, et al. Suppression of tumorigenesis in the Apcmin mouse: downregulation of β-catenin signaling by a combination of tea plus sulindac. Carcinogenesis. 2003;24:263–267
  127. Ohishi T, Kishimoto Y, Miura N, et al. Synergistic effects of (−)-epigallocatechin gallate with sulindac against colon carcinogenesis of rats treated with azoxymethane. Cancer Lett. 2002;177:49–56
  128. Khafif A, Schantz SP, Chou T-C, et al. Quantitation of chemopreventive synergism between (−)-epigallocatechin-3-gallate and curcumin in normal, premalignant and malignant human oral epithelial cells. Carcinogenesis. 1998;19:419–424
  129. Li N, Chen XX, Liao J, et al. Inhibition of 7, 12-dimethylbenz[a]anthracene (DMBA)-induced oral carcinogenesis in hamsters by tea and curcumin. Carcinogenesis. 2002;23:1307–1313
  130. Deeb D, Xu YX, Jiang H, et al. Curcumin (diferuloyl-methane) enhances tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in LNCaP prostate cancer cells. Mol Cancer Ther. 2003;2:95–103
  131. Somasundaram S, Edmund NA, Moore DT, et al. Dietary curcumin inhibits chemotherapy-induced apoptosis in models on human breast cancer. Cancer Res. 2002;62:3868–3875

PII: S0959-8049(05)00473-9

doi: 10.1016/j.ejca.2005.05.008

European Journal of Cancer
Volume 41, Issue 13 , Pages 1842-1853 , September 2005