The Journal of Nutritional Biochemistry
Volume 22, Issue 5 , Pages 502-510 , May 2011

Dietary soy and tea mitigate chronic inflammation and prostate cancer via NFκB pathway in the Noble rat model

  • Anna Hsu

      Affiliations

    • Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR 97331, USA
  • ,
  • Richard S. Bruno

      Affiliations

    • Department of Nutritional Sciences, University of Connecticut, Storrs, CT 06269, USA
  • ,
  • Christiane V. Löhr

      Affiliations

    • Department of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, USA
  • ,
  • Alan W. Taylor

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
  • ,
  • Rodrick H. Dashwood

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • Department of Environmental and Molecular Toxicology, Oregon State University, Corvallis, OR 97331, USA.
  • ,
  • Tammy M. Bray

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • Department of Environmental and Molecular Toxicology, Oregon State University, Corvallis, OR 97331, USA.
  • ,
  • Emily Ho

      Affiliations

    • Linus Pauling Institute, Oregon State University, Corvallis, OR 97331, USA
    • Department of Environmental and Molecular Toxicology, Oregon State University, Corvallis, OR 97331, USA.
    • Corresponding Author InformationCorresponding author. Oregon State University, Corvallis, OR 97331, USA. Tel.: +1 541 737 9559; fax: +1 541 737 6914.

Received 10 October 2009 ,Revised 15 March 2010 ,Accepted 13 April 2010.

References 

  1. Jemal A, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58(2):71–96
  2. Muir CS, Nectoux J, Staszewski J. The epidemiology of prostatic cancer. Geographical distribution and time-trends. Acta Oncol. 1991;30(2):133–140
  3. Cook LS, et al. Incidence of adenocarcinoma of the prostate in Asian immigrants to the United States and their descendants. J Urol. 1999;161(1):152–155
  4. Lamartiniere CA. Protection against breast cancer with genistein: a component of soy. Am J Clin Nutr. 2000;71(6 Suppl):1705S–1707S[discussion 1708S-9S]
  5. Gilani GS, Anderson JB. In:  Gilani GS,  Anderson JJB editor. Phytoestrogens and Health. Champaign, IL: AOCS Press; 2002;p. 660
  6. Dixon RA. Phytoestrogens. Annu Rev Plant Biol. 2004;55:225–261
  7. Fujiki H, et al. Cancer inhibition by green tea. Mutat Res. 1998;402(1-2):307–310
  8. Inoue M, et al. Tea and coffee consumption and the risk of digestive tract cancers: data from a comparative case-referent study in Japan. Cancer Causes Control. 1998;9(2):209–216
  9. Ji BT, et al. Green tea consumption and the risk of pancreatic and colorectal cancers. Int J Cancer. 1997;70(3):255–258
  10. Nakachi K, et al. Influence of drinking green tea on breast cancer malignancy among Japanese patients. Jpn J Cancer Res. 1998;89(3):254–261
  11. Beltz LA, et al. Mechanisms of cancer prevention by green and black tea polyphenols. Anticancer Agents Med Chem. 2006;6(5):389–406
  12. Handayani R, et al. Soy isoflavones alter expression of genes associated with cancer progression, including interleukin-8, in androgen-independent PC-3 human prostate cancer cells. J Nutr. 2006;136(1):75–82
  13. Fotsis T, et al. Genistein, a dietary ingested isoflavonoid, inhibits cell proliferation and in vitro angiogenesis. J Nutr. 1995;125(3 Suppl):790S–797S
  14. Zhu BH, et al. (−)-Epigallocatechin-3-gallate inhibits growth of gastric cancer by reducing VEGF production and angiogenesis. World J Gastroenterol. 2007;13(8):1162–1169
  15. Adhami VM, Ahmad N, Mukhtar H. Molecular targets for green tea in prostate cancer prevention. J Nutr. 2003;133(7 Suppl):2417S–2424S
  16. Cooke PS, Selvaraj V, Yellayi S. Genistein, estrogen receptors, and the acquired immune response. J Nutr. 2006;136(3):704–708
  17. Greten FR, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004;118(3):285–296
  18. Pikarsky E, et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature. 2004;431(7007):461–466
  19. Luo JL, et al. Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature. 2007;446(7136):690–694
  20. Li Y, Sarkar FH. Inhibition of nuclear factor kappaB activation in PC3 cells by genistein is mediated via Akt signaling pathway. Clin Cancer Res. 2002;8(7):2369–2377
  21. Okabe S, et al. Modulation of gene expression by (−)-epigallocatechin gallate in PC-9 cells using a cDNA expression array. Biol Pharm Bull. 2001;24(8):883–886
  22. Raffoul JJ, et al. Genistein inhibits radiation-induced activation of NF-kappaB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer. 2006;6:107
  23. Orner GA, Dashwood WM, Dashwood RH. Tumor-suppressing effects of antioxidants from tea. J Nutr. 2004;134(11):3177S–3178S
  24. Mentor-Marcel R, et al. Genistein in the diet reduces the incidence of poorly differentiated prostatic adenocarcinoma in transgenic mice (TRAMP). Cancer Res. 2001;61(18):6777–6782
  25. Han X, Liehr JG, Bosland MC. Induction of a DNA adduct detectable by 32P-postlabeling in the dorsolateral prostate of NBL/Cr rats treated with estradiol-17 beta and testosterone. Carcinogenesis. 1995;16(4):951–954
  26. Drago JR. The induction of NB rat prostatic carcinomas. Anticancer Res. 1984;4(4-5):255–256
  27. Bosland MC, Ford H, Horton L. Induction at high incidence of ductal prostate adenocarcinomas in NBL/Cr and Sprague-Dawley Hsd:SD rats treated with a combination of testosterone and estradiol-17 beta or diethylstilbestrol. Carcinogenesis. 1995;16(6):1311–1317
  28. Kenny AM, et al. Soy proteins and isoflavones affect bone mineral density in older women: a randomized controlled trial. Am J Clin Nutr. 2009;
  29. Ofner P, Bosland MC, Vena RL. Differential effects of diethylstilbestrol and estradiol-17 beta in combination with testosterone on rat prostate lobes. Toxicol Appl Pharmacol. 1992;112(2):300–309
  30. Hernaez J, Xu M, Dashwood R. Effects of tea and chlorophyllin on the mutagenicity of N-hydroxy-IQ: studies of enzyme inhibition, molecular complex formation, and degradation/scavenging of the active metabolites. Environ Mol Mutagen. 1997;30(4):468–474
  31. Noble RL. The development of prostatic adenocarcinoma in Nb rats following prolonged sex hormone administration. Cancer Res. 1977;37(6):1929–1933
  32. Bernoulli J, et al. Prostatic inflammation and obstructive voiding in the adult Noble rat: impact of the testosterone to estradiol ratio in serum. Prostate. 2008;68(12):1296–1306
  33. Palapattu GS, et al. Prostate carcinogenesis and inflammation: emerging insights. Carcinogenesis. 2005;26(7):1170–1181
  34. Tam NN, Leav I, Ho SM. Sex hormones induce direct epithelial and inflammation-mediated oxidative/nitrosative stress that favors prostatic carcinogenesis in the noble rat. Am J Pathol. 2007;171(4):1334–1341
  35. Karin M. NF-kappaB and cancer: mechanisms and targets. Mol Carcinog. 2006;45(6):355–361
  36. LaCasse EC, et al. IAP-targeted therapies for cancer. Oncogene. 2008;27(48):6252–6275
  37. Jemal A, et al. Cancer statistics, 2007. CA Cancer J Clin. 2007;57(1):43–66
  38. Hedlund TE, et al. Long-term dietary habits affect soy isoflavone metabolism and accumulation in prostatic fluid in Caucasian men. J Nutr. 2005;135(6):1400–1406
  39. Slavin JL, et al. Influence of soybean processing, habitual diet, and soy dose on urinary isoflavonoid excretion. Am J Clin Nutr. 1998;68(6 Suppl):1492S–1495S
  40. Dashwood RH. Frontiers in polyphenols and cancer prevention. J Nutr. 2007;137(1 Suppl):267S–269S
  41. Lambert JD, et al. Effect of genistein on the bioavailability and intestinal cancer chemopreventive activity of (−)-epigallocatechin-3-gallate. Carcinogenesis. 2008;29(10):2019–2024
  42. Bu-Abbas A, et al. Stimulation of rat hepatic UDP-glucuronosyl transferase activity following treatment with green tea. Food Chem Toxicol. 1995;33(1):27–30
  43. Xu M, Dashwood RH. Chemoprevention studies of heterocyclic amine-induced colon carcinogenesis. Cancer Lett. 1999;143(2):179–183
  44. Hara Y. Influence of tea catechins on the digestive tract. J Cell Biochem Suppl. 1997;27:52–58
  45. Narayanan BA, et al. Regression of mouse prostatic intraepithelial neoplasia by nonsteroidal anti-inflammatory drugs in the transgenic adenocarcinoma mouse prostate model. Clin Cancer Res. 2004;10(22):7727–7737
  46. Narayanan BA, et al. Adenocarcina of the mouse prostate growth inhibition by celecoxib: downregulation of transcription factors involved in COX-2 inhibition. Prostate. 2006;66(3):257–265
  47. Kearney PM, et al. Do selective cyclo-oxygenase-2 inhibitors and traditional non-steroidal anti-inflammatory drugs increase the risk of atherothrombosis? Meta-analysis of randomised trials. BMJ. 2006;332(7553):1302–1308
  48. Traversa G, et al. Gastroduodenal toxicity of different nonsteroidal antiinflammatory drugs. Epidemiology. 1995;6(1):49–54
  49. Cavalieri EL, et al. Catechol estrogen metabolites and conjugates in different regions of the prostate of Noble rats treated with 4-hydroxyestradiol: implications for estrogen-induced initiation of prostate cancer. Carcinogenesis. 2002;23(2):329–333
  50. Soronen P, et al. Sex steroid hormone metabolism and prostate cancer. J Steroid Biochem Mol Biol. 2004;92(4):281–286
  51. Cavalieri EL, Rogan EG. A unifying mechanism in the initiation of cancer and other diseases by catechol quinones. Ann N Y Acad Sci. 2004;1028:247–257
  52. Zhu BT, Conney AH. Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis. 1998;19(1):1–27
  53. Suh J, et al. Mechanisms of constitutive NF-kappaB activation in human prostate cancer cells. Prostate. 2002;52(3):183–200
  54. Suh J, Rabson AB. NF-kappaB activation in human prostate cancer: important mediator or epiphenomenon?. J Cell Biochem. 2004;91(1):100–117
  55. Kazi A, et al. Inhibition of the proteasome activity, a novel mechanism associated with the tumor cell apoptosis-inducing ability of genistein. Biochem Pharmacol. 2003;66(6):965–976
  56. Messina MJ. Emerging evidence on the role of soy in reducing prostate cancer risk. Nutr Rev. 2003;61(4):117–131
  57. Adhami VM, et al. Oral consumption of green tea polyphenols inhibits insulin-like growth factor-I-induced signaling in an autochthonous mouse model of prostate cancer. Cancer Res. 2004;64(23):8715–8722
  58. Adhami VM, et al. Effective prostate cancer chemopreventive intervention with green tea polyphenols in the TRAMP model depends on the stage of the disease. Clin Cancer Res. 2009;15(6):1947–1953
  59. O'Sullivan J, et al. The effect of green tea on oxidative damage and tumour formation in Lobund-Wistar rats. Eur J Cancer Prev. 2008;17(6):489–501
  60. Cohen LA, et al. Effect of soy protein isolate and conjugated linoleic acid on the growth of Dunning R-3327-AT-1 rat prostate tumors. Prostate. 2003;54(3):169–180
  61. Siddiqui IA, et al. Suppression of NFkappaB and its regulated gene products by oral administration of green tea polyphenols in an autochthonous mouse prostate cancer model. Pharm Res. 2008;25(9):2135–2142
  62. Allred CD, et al. Soy processing influences growth of estrogen-dependent breast cancer tumors. Carcinogenesis. 2004;25(9):1649–1657
  63. Murrill WB, et al. Prepubertal genistein exposure suppresses mammary cancer and enhances gland differentiation in rats. Carcinogenesis. 1996;17(7):1451–1457
  64. Zhou JR, et al. Soy phytochemicals and tea bioactive components synergistically inhibit androgen-sensitive human prostate tumors in mice. J Nutr. 2003;133(2):516–521
  65. Bode AM, Dong Z. Epigallocatechin 3-gallate and green tea catechins: United they work, divided they fail. Cancer Prev Res (Phila Pa). 2009;2(6):514–517

 Grant Support: This work was supported by NIH grant CA107693 and CA909890, Oregon AES (OR00735), the Environmental Health Science Center at Oregon State University (NIEHS P30 ES00210), and the Donaghue Foundation (University of Connecticut Health Center GCRC no. 648).

PII: S0955-2863(10)00111-7

doi: 10.1016/j.jnutbio.2010.04.006

The Journal of Nutritional Biochemistry
Volume 22, Issue 5 , Pages 502-510 , May 2011