Indolylfuran, a potent aryl hydrocarbon receptor agonist from sauerkraut, interacts with the oestrogen pathway

Food Chemistry

Volumn 127, Issue 4, 2011, Pages 1764-1772

  Medjakovic, Svjetlana ^a   Zoechling, Alfred ^a   Vollmer, Günter ^b   Zierau, Oliver ^b   Kretzschmar, Georg ^b   Möller, Frank ^b   Kolba, Susanne ^b   Papke, Anja ^b   Opietnik, Martina ^a   Kosma, Paul ^a   Rosenau, Thomas ^a   Jungbauer, Alois ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

1 (2 furanyl)2 (3 indolyl)ethanone; Anti oestrogen; Brassicaceae; Nuclear receptors; Uterotrophic assay

Indexed keywords

1-(2-FURANYL)2-(3-INDOLYL)ETHANONE; BRASSICACEAE; NUCLEAR RECEPTORS; OESTROGENS; UTEROTROPHIC ASSAY;

HYDROCARBONS; LIGANDS;

TRANSCRIPTION FACTORS;

1 (2 FURANYL) 2 (3 INDOLYL)ETHANONE; ANTIESTROGEN; AROMATIC HYDROCARBON RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; SAUERKRAUT EXTRACT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; CABBAGE; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; DRUG POTENCY; DRUG RECEPTOR BINDING; DRUG SYNTHESIS; FEMALE; GENE EXPRESSION REGULATION; IN VIVO STUDY; NONHUMAN; RAT; SAUERKRAUT; STRUCTURE ANALYSIS; UTERUS WEIGHT;

BRASSICACEAE;

EID: 79953200113     PISSN: 03088146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodchem.2011.02.056     Document Type: Article

References (74)

1. P. Andersson, J. McGuire, C. Rubio, K. Gradin, M.L. Whitelaw, and S. Pettersson A constitutively active dioxin/aryl hydrocarbon receptor induces stomach tumours Proceedings of the National Academy of Sciences of the United States of America 99 2002 9990 9995 (Pubitemid 34831160)
2. T. Baba, J. Mimura, N. Nakamura, N. Harada, M. Yamamoto, and K.I. Morohashi Intrinsic function of the aryl hydrocarbon (dioxin) receptor as a key factor in female reproduction Molecular and Cellular Biology 25 2005 10040 10051 (Pubitemid 41573694)
3. R. Barouki, X. Coumoul, and P.M. Fernandez-Salguero The aryl hydrocarbon receptor, more than a xenobiotic-interacting protein FEBS Letters 581 2007 3608 3615 (Pubitemid 47080995)
4. T.V. Beischlag, and G.H. Perdew ER alpha-AHR-ARNT protein-protein interactions mediate estradiol-dependent transrepression of dioxin-inducible gene transcription Journal of Biological Chemistry 280 2005 21607 21611 (Pubitemid 40805729)
5. V. Bemanian, R. Male, and A. Goksøyr The aryl hydrocarbon receptor-mediated disruption of vitellogenin synthesis in the fish liver: Cross-talk between AHR- and ERα -signalling pathways Comparative Hepatology 3 2004 2
6. E. Benito, A. Obrador, A. Stiggelbout, F.X. Bosch, M. Mulet, and N. Munoz A population-based case-control study of colorectal cancer in Majorca I. Dietary factors International Journal of Cancer 45 1990 69 76 (Pubitemid 20032100)
7. D.R. Boverhof, L.D. Burgoon, K.J. Williams, and T.R. Zacharewski Inhibition of oestrogen-mediated uterine gene expression responses by dioxin Molecular Pharmacology 73 2008 82 93 (Pubitemid 350294199)
8. E. Brantley, V. Patel, S.F. Stinson, V. Trapani, C.D. Hose, and H.P. Ciolino The antitumour drug candidate 2-(4-amino-3-methylphenyl)-5- fluorobenzothiazole induces NF-κB activity in drug-sensitive MCF-7 cells Anti-Cancer Drugs 16 2005 137 143 (Pubitemid 40250608)
9. O.R. Brunkow, W.H. Peterson, and E.B. Fred The influence of certain factors upon the chemical composition of sauerkraut Journal of the American Chemical Society 43 1921 2244 2255
10. J.M. Chan, F. Wang, and E.A. Holly Vegetable and fruit intake and pancreatic cancer in a population-based case-control study in the San Francisco bay area Cancer Epidemiology, Biomarkers and Prevention 14 2005 2093 2097 (Pubitemid 41603251)
11. J.T. Chang, H. Chang, P.H. Chen, S.L. Lin, and P. Lin Requirement of aryl hydrocarbon receptor overexpression for CYP1B1 up-regulation and cell growth in human lung adenocarcinomas Clinical Cancer Research 13 2007 38 45 (Pubitemid 46121850)
12. X. Chang, J.C. Tou, C. Hong, H.A. Kim, J.E. Riby, and G.L. Firestone 3, 3́-diindolylmethane inhibits angiogenesis and the growth of transplantable human breast carcinoma in athymic mice Carcinogenesis 26 2005 771 778 (Pubitemid 41214339)
13. N.M. Chau, P. Rogers, W. Aherne, V. Carroll, I. Collins, and E. McDonald Identification of novel small molecule inhibitors of hypoxia-inducible factor-1 that differentially block hypoxia-inducible factor-1 activity and hypoxia-inducible factor-1alpha induction in response to hypoxic stress and growth factors Cancer Research 65 2005 4918 4928 (Pubitemid 40740832)
14. I. Chen, T. Hsieh, T. Thomas, and S. Safe Identification of oestrogen-induced genes downregulated by AhR agonists in MCF-7 breast cancer cells using suppression subtractive hybridization Gene 262 2001 207 214 (Pubitemid 32155351)
15. I. Chen, A. McDougal, F. Wang, and S. Safe Aryl hydrocarbon receptor-mediated antioestrogenic and anti-tumourigenic activity of diindolylmethane Carcinogenesis 19 1998 1631 1639 (Pubitemid 28441867)
16. J.Y. Chung, J.Y. Kim, W.R. Kim, S.G. Lee, Y.J. Kim, and J.E. Park Abundance of aryl hydrocarbon receptor potentiates benzo[a]pyrene-induced apoptosis in Hepa1c1c7 cells via CYP1A1 activation Toxicology 235 2007 62 72 (Pubitemid 46669769)
17. J.H. Cohen, A.R. Kristal, and J.L. Stanford Fruit and vegetable intakes and prostate cancer risk Journal of the National Cancer Institute 92 2000 61 68 (Pubitemid 30082230)
18. W.A. Fritz, T.M. Lin, and R.E. Peterson The aryl hydrocarbon receptor (AhR) inhibits vanadate-induced vascular endothelial growth factor (VEGF) production in TRAMP prostates Carcinogenesis 29 2008 1077 1082 (Pubitemid 351982255)
19. W.A. Fritz, T.M. Lin, S. Safe, R.W. Moore, and R.E. Peterson The selective aryl hydrocarbon receptor modulator 6-methyl-1, 3, 8-trichlorodibenzofuran inhibits prostate tumour metastasis in TRAMP mice Biochemical Pharmacology 77 2009 1151 1160
20. V.P. Garikapaty, B.T. Ashok, K. Tadi, A. Mittelman, and R.K. Tiwari Synthetic dimer of indole-3-carbinol: Second generation diet derived anti-cancer agent in hormone sensitive prostate cancer Prostate 66 2006 453 462
21. J.F. Gierthy, D.W. Ii Lincoln, S.J. Kampcik, H.W. Dickerman, H.L. Bradlow, and T. Niwa Enhancement of 2- and 16α-estradiol hydroxylation in MCF-7 human breast cancer cells by 2, 3, 7, 8-tetrachlorodibenzo-P-dioxin Biochemical and Biophysical Research Communications 157 1988 515 520 (Pubitemid 19021210)
22. Y.D. Hang Sauerkraut Y.H. Hui, L. Meunier-Goddik, A.S. Hansen, J. Josephsen, W. Nip, P.S. Stanfield, F. Toldra, Handbook of food and beverage fermentation technology 2005 Taylor & Francis New York 768 775
23. C.L. Hayes, D.C. Spink, B.C. Spink, J.Q. Cao, N.J. Walker, and T.R. Sutter 17β-Estradiol hydroxylation catalysed by human cytochrome P450 1B1 Proceedings of the National Academy of Sciences of the United States of America 93 1996 9776 9781 (Pubitemid 26296685)
24. K. Hirose, M. Morita, M. Ema, J. Mimura, K. Sogawa, and Y. Fujii-Kuriyama CDNA cloning and tissue-specific expression of a novel basic helix-loop-helix/PAS factor (Arnt2) with close sequence similarity to the aryl hydrocarbon receptor nuclear translocator (Arnt) Molecular and Cellular Biology 16 1996 1706 1713
25. H.D. Hosgood 3rd, D. Baris, S.H. Zahm, T. Zheng, and A.J. Cross Diet and risk of multiple myeloma in connecticut women Cancer Causes and Control 18 2007 1065 1076 (Pubitemid 47498157)
26. C.C. Hsu, W.H. Chow, P. Boffetta, L. Moore, D. Zaridze, and A. Moukeria Dietary risk factors for kidney cancer in Eastern and Central Europe American Journal of Epidemiology 166 2007 62 70 (Pubitemid 47234290)
27. T. Ikuta, T. Namiki, Y. Fujii-Kuriyama, and K. Kawajiri AhR protein trafficking and function in the skin Biochemical Pharmacology 77 2009 588 596
28. P.H. Jellinck, P.G. Forkert, D.S. Riddick, A.B. Okey, J.J. Michnovicz, and H.L. Bradlow Ah receptor binding properties of indole carbinols and induction of hepatic estradiol hydroxylation Biochemical Pharmacology 45 1993 1129 1136 (Pubitemid 23079991)
29. K. Kawajiri, Y. Kobayashi, F. Ohtake, T. Ikuta, Y. Matsushima, and J. Mimura Aryl hydrocarbon receptor suppresses intestinal carcinogenesis in ApcMin/+ mice with natural ligands Proceedings of the National Academy of Sciences of the United States of America 106 2009 13481 13486
30. T.J. Key, N. Allen, P. Appleby, K. Overvad, A. Tjonneland, and A. Miller Fruits and vegetables and prostate cancer: no association among 1104 cases in a prospective study of 130544 men in the European prospective investigation into cancer and nutrition (EPIC) International Journal of Cancer 109 2004 119 124 (Pubitemid 38160671)
31. I. Kharat, and F. Saatcioglu Antioestrogenic effects of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded oestrogen receptor: Cross-talk between aryl hydrocarbon- and oestrogen-mediated signalling Journal of Biological Chemistry 271 1996 10533 10537
32. C.M. Klinge, J.L. Bowers, P.C. Kulakosky, K.K. Kamboj, and H.I. Swanson The aryl hydrocarbon receptor (AHR)/AHR nuclear translocator (ARNT) heterodimer interacts with naturally occurring oestrogen response elements Molecular and Cellular Endocrinology 157 1999 105 119 (Pubitemid 29505132)
33. C.M. Klinge, K. Kaur, and H.I. Swanson The aryl hydrocarbon receptor interacts with oestrogen receptor alpha and orphan receptors COUP-TFI and ERRα1 Archives of Biochemistry and Biophysics 373 2000 163 174 (Pubitemid 30046501)
34. G. Kretzschmar, A. Papke, O. Zierau, F.J. Moeller, S. Medjakovic, and A. Jungbauer Estradiol regulates aryl hydrocarbon receptor expression in the rat uterus Molecular and Cellular Endocrinology 321 2010 253 257
35. A. Kuchenhoff, G. Seliger, T. Klonisch, G. Tscheudschilsuren, P. Kaltwasser, and E. Seliger Arylhydrocarbon receptor expression in the human endometrium Fertility and Sterility 71 1999 354 360 (Pubitemid 29069917)
36. T. Kung, K.A. Murphy, and L.A. White The aryl hydrocarbon receptor (AhR) pathway as a regulatory pathway for cell adhesion and matrix metabolism Biochemical Pharmacology 77 2009 536 546
37. P. Lin, H. Chang, W.T. Tsai, M.H. Wu, Y.S. Liao, and J.T. Chen Overexpression of aryl hydrocarbon receptor in human lung carcinomas Toxicologic Pathology 31 2003 22 30 (Pubitemid 36169418)
38. L.N. Lysenkova, M.I. Reznikova, A.M. Korolev, and M.N. Preobrazhenskaya Study of the transformations of 2-C-(indol-3-yl)methyl-α-L-xylo-hex-3- ulofuranosonic acid (the open form of ascorbigen) in an acidic medium Russian Chemical Bulletin 50 2001 1309 1313 (Pubitemid 33401763)
39. A. McDougal, C. Wilson, and S. Safe Inhibition of 7, 12-dimethylbenz[a] anthracene-induced rat mammary tumour growth by aryl hydrocarbon receptor agonists Cancer Letters 120 1997 53 63 (Pubitemid 27483311)
40. A. McDougal, M. Wormke, J. Calvin, and S. Safe Tamoxifen-induced antitumourigenic/antioestrogenic action synergized by a selective aryl hydrocarbon receptor modulator Cancer Research 61 2001 3902 3907 (Pubitemid 32720948)
41. S. Medjakovic, and A. Jungbauer Red clover isoflavones biochanin A and formononetin are potent ligands of the human aryl hydrocarbon receptor Journal of Steroid Biochemistry and Molecular Biology 108 2008 171 177 (Pubitemid 351173832)
42. J.J. Michnovicz, H. Adlercreutz, and H.L. Bradlow Changes in levels of urinary oestrogen metabolites after oral indole-3- carbinol treatment in humans Journal of the National Cancer Institute 89 1997 718 723 (Pubitemid 27229860)
43. P. Mishra, R.K. Kale, and A. Kar Chemoprevention of mammary tumourigenesis and chemomodulation of the antioxidative enzymes and peroxidative damage in prepubertal Sprague Dawley rats by biochanin A Molecular and Cellular Biochemistry 312 2008 1 9
44. O. Moennikes, S. Loeppen, A. Buchmann, P. Andersson, C. Ittrich, and L. Poellinger A constitutively active dioxin/aryl hydrocarbon receptor promotes hepatocarcinogenesis in mice Cancer Research 64 2004 4707 4710 (Pubitemid 38924510)
45. 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 Biochemical Pharmacology 59 2000 65 85
46. C.W. Nho, and E. Jeffery The synergistic upregulation of phase II detoxification enzymes by glucosinolate breakdown products in cruciferous vegetables Toxicology and Applied Pharmacology 174 2001 146 152 (Pubitemid 32675517)
47. C.W. Nho, and E. Jeffery 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 Toxicology and Applied Pharmacology 198 2004 40 48 (Pubitemid 38789127)
48. T. Niwa, G. Swaneck, and H.L. Bradlow Alterations in estradiol metabolism in MCF-7 cells induced by treatment with indole-3-carbinol and related compounds Steroids 59 1994 523 527 (Pubitemid 24286766)
49. U. Nothlings, L.R. Wilkens, S.P. Murphy, J.H. Hankin, B.E. Henderson, and L.N. Kolonel Vegetable intake and pancreatic cancer risk: The multiethnic cohort study American Journal of Epidemiology 165 2007 138 147 (Pubitemid 46096375)
50. S.H. Oh, J.K. Woo, Q. Jin, H.J. Kang, J.W. Jeong, and K.W. Kim Identification of novel antiangiogenic anticancer activities of deguelin targeting hypoxia-inducible factor-1 alpha International Journal of Cancer 122 2008 5 14 (Pubitemid 350209972)
51. F. Ohtake, K.I. Takeyama, T. Matsumoto, H. Kitagawa, J. Yanagisawa, and S. Kato Modulation of ooestrogen receptor signalling by association with the activated dioxin receptor Nature 423 2003 545 550 (Pubitemid 36648579)
52. S.Y. Pan, A.M. Ugnat, Y. Mao, S.W. Wen, and K.C. Johnson A case-control study of diet and the risk of ovarian cancer Cancer Epidemiology, Biomarkers and Prevention 13 2004 1521 1527 (Pubitemid 39202321)
53. P.H. Pang, Y.H. Lin, Y.H. Lee, H.H. Hou, S.P. Hsu, and S.H. Juan Molecular mechanisms of p21 and p27 induction by 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, involved in antiproliferation of human umbilical vascular endothelial cells Journal of Cellular Physiology 215 2008 161 171
54. G. Powis, and L. Kirkpatrick Hypoxia inducible factor-1alpha as a cancer drug target Molecular Cancer Therapeutics 3 2004 647 654 (Pubitemid 39193744)
55. J.K. Pru, T. Kaneko-Tarui, A. Jurisicova, A. Kashiwagi, K. Selesniemi, and J.L. Tilly Induction of proapoptotic gene expression and recruitment of p53 herald ovarian follicle loss caused by polycyclic aromatic hydrocarbons Reproductive Science 16 2009 347 356
56. A. Puga, Y. Xia, and C. Elferink Role of the aryl hydrocarbon receptor in cell cycle regulation Chemico-Biological Interactions 141 2002 117 130 (Pubitemid 35223208)
57. K.M. Rahman, O. Aranha, and F.H. Sarkar Indole-3-carbinol (I3C) induces apoptosis in tumourigenic but not in nontumourigenic breast epithelial cells Nutrition and Cancer 45 2003 101 112 (Pubitemid 36736897)
58. R.K. Reen, A. Cadwallader, and G.H. Perdew The subdomains of the transactivation domain of the aryl hydrocarbon receptor (AhR) inhibit AhR and oestrogen receptor transcriptional activity Archives of Biochemistry and Biophysics 408 2002 93 102 (Pubitemid 36062540)
59. F.H. Sarkar, Y. Li, Z. Wang, and D. Kong Cellular signalling perturbation by natural products Cellular Signalling 21 2009 1541 1547
60. I. Schreck, D. Chudziak, S. Schneider, A. Seidel, K.L. Platt, and F. Oesch Influence of aryl hydrocarbon- (Ah) receptor and genotoxins on DNA repair gene expression and cell survival of mouse hepatoma cells Toxicology 259 2009 91 96
61. H. Sekine, J. Mimura, M. Yamamoto, and Y. Fujii-Kuriyama Unique and overlapping transcriptional roles of arylhydrocarbon receptor nuclear translocator (Arnt) and Arnt2 in xenobiotic and hypoxic responses Journal of Biological Chemistry 281 2006 37507 37516 (Pubitemid 46042054)
62. K.P. Singh, F.L. Casado, L.A. Opanashuk, and T.A. Gasiewicz The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations Biochemical Pharmacology 77 2009 577 587
63. D.O. Stram, J.H. Hankin, L.R. Wilkens, S. Park, B.E. Henderson, and A.M. Nomura Prostate cancer incidence and intake of fruits, vegetables and related micronutrients: the multiethnic cohort study Cancer Causes and Control 17 2006 1193 1207 (United States) (Pubitemid 44470409)
64. P.M. Swamy Sauerkraut fermentation R.K. Rastogi, Laboratory manual on biotechnology 2008 Rastogi Publications Meerut India (pp. 248)
65. Y. Takada, M. Andreeff, and B.B. Aggarwal Indole-3-carbinol suppresses NF-κB and IκBa kinase activation, causing inhibition of expression of NF-κB-regulated antiapoptotic and metastatic gene products and enhancement of apoptosis in myeloid and leukemia cells Blood 106 2005 641 649 (Pubitemid 40981262)
66. C. Tan, R.G. de Noronha, A.J. Roecker, B. Pyrzynska, F. Khwaja, and Z. Zhang Identification of a novel small-molecule inhibitor of the hypoxia-inducible factor 1 pathway Cancer Research 65 2005 605 612
67. L.E. Voorrips, R.A. Goldbohm, D.T.H. Verhoeven, G.A.F.C. Van Poppel, F. Sturmans, and R.J.J. Hermus Vegetable and fruit consumption and lung cancer risk in the Netherlands cohort study on diet and cancer Cancer Causes and Control 11 2000 101 115 (Pubitemid 30088388)
68. C.L. Waller, and J.D. McKinney Three-dimensional quantitative structure-activity relationships of dioxins and dioxin-like compounds: Model validation and Ah receptor characterisation Chemical Research in Toxicology 8 1995 847 858
69. M. Wormke, M. Stoner, B. Saville, and S. Safe Crosstalk between oestrogen receptor α and the aryl hydrocarbon receptor in breast cancer cells involves unidirectional activation of proteasomes FEBS Letters 478 2000 109 112 (Pubitemid 30462268)
70. R. Wu, L. Zhang, M.S. Hoagland, and H.I. Swanson Lack of the aryl hydrocarbon receptor leads to impaired activation of AKT/protein kinase B and enhanced sensitivity to apoptosis induced via the intrinsic pathway Journal of Pharmacology and Experimental Therapeutics 320 2007 448 457 (Pubitemid 46028485)
71. H. Yasuda Solid tumour physiology and hypoxia-induced chemo/radio-resistance. Novel strategy for cancer therapy: Nitric oxide donor as a therapeutic enhancer Nitric Oxide 19 2008 205 216
72. J.M. Yuan, M. Gago-Dominguez, J.E. Castelao, J.H. Hankin, R.K. Ross, and M.C. Yu Cruciferous vegetables in relation to renal cell carcinoma International Journal of Cancer 77 1998 211 216 (Pubitemid 28287971)
73. C.X. Zhang, S.C. Ho, Y.M. Chen, J.H. Fu, S.Z. Cheng, and F.Y. Lin Greater vegetable and fruit intake is associated with a lower risk of breast cancer among Chinese women International Journal of Cancer 125 2009 181 188
74. J.E. Ziello, I.S. Jovin, and Y. Huang Hypoxia-Inducible Factor (HIF)-1 regulatory pathway and its potential for therapeutic intervention in malignancy and ischaemia Yale Journal of Biology and Medicine 80 2007 51 60