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The Diet, Prostate Inflammation, and the Development of Prostate Cancer

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Abstract

Evidence that somatic inactivation of GSTP1, encoding the human π-class glutathione S-transferase, may initiate prostatic carcinogenesis is reviewed along with epidemiological evidence implicating several environment and lifestyle factors, including the diet and sexually transmitted diseases, as prostate cancer risk factors. An integrated model is presented featuring GSTP1 function as a 'caretaker' gene during the pathogenesis of prostate cancer, in which the early loss of GSTP1 activity renders prostate cells vulnerable to genome damage associated with chronic prostatic inflammation and repeated exposure to carcinogens. The model predicts that the critical prostate carcinogens will be those that are substrates for GSTP1 detoxification and are associated with high prostate cancer risk diet and lifestyle habits.

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References

  1. Steinberg GD, Carter BS, Beaty TH, Childs B, Walsh PC: Family history and the risk of prostate cancer. Prostate 17: 337, 1990

    Google Scholar 

  2. Carter BS, Steinberg GD, Beaty TH, Childs B, Walsh PC: Familial risk factors for prostate cancer. Cancer Surv 11: 5, 1991

    Google Scholar 

  3. Carter BS, Beaty TH, Steinberg GD, Childs B, Walsh PC: Mendelian inheritance of familial prostate cancer. Proc Natl Acad Sci USA 89: 3367, 1992

    Google Scholar 

  4. Xu J, Zheng SL, Hawkins GA, Faith DA, Kelly B, Isaacs SD, Wiley KE, Chang B, Ewing CM, Bujnovszky P, Carpten JD, Bleecker ER, Walsh PC, Trent JM, Meyers DA, Isaacs WB: Linkage and association studies of prostate cancer susceptibility: evidence for linkage at 8p22-23. Am J Hum Genet 69: 341, 2001

    Google Scholar 

  5. Zheng SL, Xu J, Isaacs SD, Wiley K, Chang B, Bleecker ER, Walsh PC, Trent JM, Meyers DA, Isaacs WB: Evidence for a prostate cancer linkage to chromosome 20 in 159 hereditary prostate cancer families. Hum Genet 108: 430, 2001

    Google Scholar 

  6. Xu J, Zheng SL, Chang B, Smith JR, Carpten JD, Stine OC, Isaacs SD, Wiley KE, Henning L, Ewing C, Bujnovszky P, Bleeker ER, Walsh PC, Trent JM, Meyers DA, Isaacs WB: Linkage of prostate cancer susceptibility loci to chromosome 1. Hum Genet 108: 335, 2001

    Google Scholar 

  7. Xu J, Zheng SL, Carpten JD, Nupponen NN, Robbins CM, Mestre J, Moses TY, Faith DA, Kelly BD, Isaacs SD, Wiley KE, Ewing CM, Bujnovszky P, Chang B, Bailey-Wilson J, Bleecker ER, Walsh PC, Trent JM, Meyers DA, Isaacs WB: Evaluation of linkage and association of HPC2/ELAC2 in patients with familial or sporadic prostate cancer. Am J Hum Genet 68: 901, 2001

    Google Scholar 

  8. Gronberg H, Xu J, Smith JR, Carpten JD, Isaacs SD, Freije D, Bova GS, Danber JE, Bergh A, Walsh PC, Collins FS, Trent JM, Meyers DA, Isaacs WB: Early age at diagnosis in families providing evidence of linkage to the hereditary prostate cancer locus (HPC1) on chromosome 1. Cancer Res 57: 4707, 1997

    Google Scholar 

  9. Gronberg H, Isaacs SD, Smith JR, Carpten JD, Bova GS, Freije D, Xu J, Meyers DA, Collins FS, Trent JM, Walsh PC, Isaacs WB: Characteristics of prostate cancer in families potentially linked to the hereditary prostate cancer 1 (HPC1) locus. JAMA 278: 1251, 1997

    Google Scholar 

  10. Smith JR, Freije D, Carpten JD, Gronberg H, Xu J, Isaacs SD, Brownstein MJ, Bova GS, Guo H, Bujnovszky P, Nusskern DR, Damber JE, Bergh A, Emanuelsson M, Kallioniemi OP, Walker-Daniels J, Bailey-Wilson JE, Beaty TH, Meyers DA, Walsh PC, Collins FS, Trent JM, Isaacs WB: Major susceptibility locus for prostate cancer on chromosome 1 suggested by a genome-wide search. Science 274: 1371, 1996

    Google Scholar 

  11. Goode EL, Stanford JL, Peters MA, Janer M, Gibbs M, Kolb S, Badzioch MD, Hood L, Ostrander EA, Jarvik GP: Clinical characteristics of prostate cancer in an analysis of linkage to four putative susceptibility loci. Clin Cancer Res 7: 2739, 2001

    Google Scholar 

  12. Peters MA, Jarvik GP, Janer M, Chakrabarti L, Kolb S, Goode EL, Gibbs M, DuBois CC, Schuster EF, Hood L, Ostrander EA, Stanford JL: Genetic linkage analysis of prostate cancer families to Xq27-28. Hum Hered 51: 107, 2001

    Google Scholar 

  13. Gibbs M, Stanford JL, Jarvik GP, Janer M, Badzioch M, Peters MA, Goode EL, Kolb S, Chakrabarti L, Shook M, Basom R, Ostrander EA, Hood L: A genomic scan of families with prostate cancer identifies multiple regions of interest. Am J Hum Genet 67: 100, 2000

    Google Scholar 

  14. Gibbs M, Stanford JL, McIndoe RA, Jarvik GP, Kolb S, Goode EL, Chakrabarti L, Schuster EF, Buckley VA, Miller EL, Brandzel S, Li S, Hood L, Ostrander EA: Evidence for a rare prostate cancer-susceptibility locus at chromosome 1p36. Am J Hum Genet 64: 776, 1999

    Google Scholar 

  15. Xu J, Meyers D, Freije D, Isaacs S, Wiley K, Nusskern D, Ewing C, Wilkens E, Bujnovszky P, Bova GS, Walsh P, Isaacs W, Schleutker J, Matikainen M, Tammela T, Visakorpi T, Kallioniemi OP, Berry R, Schaid D, French A, McDonnell S, Schroeder J, Blute M, Thibodeau S, Trent J: Evidence for a prostate cancer susceptibility locus on the X chromosome. Nat Genet 20: 175, 1998

    Google Scholar 

  16. Berry R, Schroeder JJ, French AJ, McDonnell SK, Peterson BJ, Cunningham JM, Thibodeau SN, Schaid DJ: Evidence for a prostate cancer-susceptibility locus on chromosome 20. Am J Hum Genet 67: 82, 2000

    Google Scholar 

  17. Berthon P, Valeri A, Cohen-Akenine A, Drelon E, Paiss T, Wohr G, Latil A, Millasseau P, Mellah I, Cohen N, Blanche H, Bellane-Chantelot C, Demenais F, Teillac P, Le Duc A, de Petriconi R, Hautmann R, Chumakov I, Bachner L, Maitland NJ, Lidereau R, Vogel W, Fournier G, Mangin P, Cussenot O: Predisposing gene for early-onset prostate cancer, localized on chromosome 1q42.2-43. Am J Hum Genet 62: 1416, 1998

    Google Scholar 

  18. Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K: Environmental and heritable factors in the causation of cancer - analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343: 78, 2000

    Google Scholar 

  19. Hsing AW, Devesa SS: Trends and patterns of prostate cancer: What do they suggest? Epidemiol Rev 23: 3, 2001

    Google Scholar 

  20. Hsing AW, Tsao L, Devesa SS: International trends and patterns of prostate cancer incidence and mortality. Int J Cancer 85: 60, 2000

    Google Scholar 

  21. Shimizu H, Ross RK, Bernstein L, Yatani R, Henderson BE, Mack TM: Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County. Br J Cancer 63: 963, 1991

    Google Scholar 

  22. Whittemore AS, Kolonel LN, Wu AH, John EM, Gallagher RP, Howe GR, Burch JD, Hankin J, Dreon DM, West DW: Prostate cancer in relation to diet, physical activity, and body size in blacks, whites, and Asians in the United States and Canada. J Natl Cancer Inst 87: 652, 1995

    Google Scholar 

  23. Lee WH, Isaacs WB, Bova GS, Nelson WG: CG island methylation changes near the GSTP1 gene in prostatic carcinoma cells detected using the polymerase chain reaction: a new prostate cancer biomarker. Cancer Epidemiol Biomarkers Prev 6: 443, 1997

    Google Scholar 

  24. Lee WH, Morton RA, Epstein JI, Brooks JD, Campbell PA, Bova GS, Hsieh WS, Isaacs WB, Nelson WG: Cytidine methylation of regulatory sequences near the pi-class glutathione S-transferase gene accompanies human prostatic carcinogenesis. Proc Natl Acad Sci USA 91: 11733, 1994

    Google Scholar 

  25. Lin X, Tascilar M, Lee WH, Vles WJ, Lee BH, Veeraswamy R, Asgari K, Freije D, van Rees B, Gage WR, Bova GS, Isaacs WB, Brooks JD, DeWeese TL, De Marzo AM, Nelson WG: GSTP1 CpG island hypermethylation is responsible for the absence of GSTP1 expression in human prostate cancer cells. Am J Pathol 159: 1815, 2001

    Google Scholar 

  26. Nelson WG, De Marzo AM, DeWeese TL: The molecular pathogenesis of prostate cancer: Implications for prostate cancer prevention. Urology 57: 39, 2001

    Google Scholar 

  27. Fearon ER, Vogelstein B: A genetic model for colorectal tumorigenesis. Cell 61: 759, 1990

    Google Scholar 

  28. Baylin SB, Herman JG: DNA hypermethylation in tumorigenesis: Epigenetics joins genetics. Trends Genet 16: 168, 2000

    Google Scholar 

  29. Kinzler KW, Vogelstein B: Cancer-susceptibility genes. Gatekeepers and caretakers (news; comment) (see comments). Nature 386: 761, 1997

    Google Scholar 

  30. Kolonel LN: Fat, meat, and prostate cancer. Epidemiol Rev 23: 72, 2001

    Google Scholar 

  31. Chan JM, Giovannucci EL: Vegetables, fruits, associated micronutrients, and risk of prostate cancer. Epidemiol Rev 23: 82, 2001

    Google Scholar 

  32. Strickler HD, Goedert JJ: Sexual behavior and evidence for an infectious cause of prostate cancer. Epidemiol Rev 23: 144, 2001

    Google Scholar 

  33. Hayes JD, Pulford DJ: The glutathione S-transferase super-gene family: Regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30: 445, 1995

    Google Scholar 

  34. Sakr WA, Grignon DJ, Crissman JD, Heilbrun LK, Cassin BJ, Pontes JJ, Haas GP: High grade prostatic intraepithelial neoplasia (HGPIN) and prostatic adenocarcinoma between the ages of 20-69: an autopsy study of 249 cases. In vivo 8: 439, 1994

    Google Scholar 

  35. Isaacs WB, Bova GS, Morton RA, Bussemakers MJ, Brooks JD, Ewing CM: Genetic alterations in prostate cancer. Cold Spring Harb Symp Quant Biol 59: 653, 1994

    Google Scholar 

  36. Ruijter ET, Miller GJ, van de Kaa CA, van Bokhoven A, Bussemakers MJ, Debruyne FM, Ruiter DJ, Schalken JA: Molecular analysis of multifocal prostate cancer lesions. J Pathol 188: 271, 1999

    Google Scholar 

  37. Suzuki H, Freije D, Nusskern DR, Okami K, Cairns P, Sidransky D, Isaacs WB, Bova GS: Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res 58: 204, 1998

    Google Scholar 

  38. Cairns P, Okami K, Halachmi S, Halachmi N, Esteller M, Herman JG, Jen J, Isaacs WB, Bova GS, Sidransky D: Frequent inactivation of PTEN/MMAC1 in primary prostate cancer. Cancer Res 57: 4997, 1997

    Google Scholar 

  39. Jarrard DF, Bova GS, Ewing CM, Pin SS, Nguyen SH, Baylin SB, Cairns P, Sidransky D, Herman JG, Isaacs WB: Deletional, mutational, and methylation analyses of CDKN2 (p16/MTS1) in primary and metastatic prostate cancer. Genes Chromosomes Cancer 19: 90, 1997

    Google Scholar 

  40. Dong JT, Suzuki H, Pin SS, Bova GS, Schalken JA, Isaacs WB, Barrett JC, Isaacs JT: Down-regulation of the KAI1 metastasis suppressor gene during the progression of human prostatic cancer infrequently involves gene mutation or allelic loss. Cancer Res 56: 4387, 1996

    Google Scholar 

  41. Cher ML, Bova GS, Moore DH, Small EJ, Carroll PR, Pin SS, Epstein JI, Isaacs WB, Jensen RH: Genetic alterations in untreated metastases and androgen-independent prostate cancer detected by comparative genomic hybridization and allelotyping. Cancer Res 56: 3091, 1996

    Google Scholar 

  42. Visakorpi T, Kallioniemi AH, Syvanen AC, Hyytinen ER, Karhu R, Tammela T, Isola JJ, Kallioniemi OP: Genetic changes in primary and recurrent prostate cancer by comparative genomic hybridization. Cancer Res 55: 342, 1995

    Google Scholar 

  43. De Marzo AM, Marchi VL, Epstein JI, Nelson WG: Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol 155: 1985, 1999

    Google Scholar 

  44. Putzi MJ, De Marzo AM: Morphologic transitions between proliferative inflammatory atrophy and high-grade prostatic intraepithelial neoplasia (In process citation). Urology 56: 828, 2000

    Google Scholar 

  45. Parsons JK, Nelson CP, Gage WR, Nelson WG, Kensler TW, De Marzo AM: GSTA1 expression in normal, preneoplastic, and neoplastic human prostate tissue. Prostate 49: 30, 2001

    Google Scholar 

  46. Brooks JD, Weinstein M, Lin X, Sun Y, Pin SS, Bova GS, Epstein JI, Isaacs WB, Nelson WG: CG island methylation changes near the GSTP1 gene in prostatic intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev 7: 531, 1998

    Google Scholar 

  47. Cairns P, Esteller M, Herman JG, Schoenberg M, Jeronimo C, Sanchez-Cespedes M, Chow NH, Grasso M, Wu L, Westra WB, Sidransky D: Molecular detection of prostate cancer in urine by GSTP1 hypermethylation. Clin Cancer Res 7: 2727, 2001

    Google Scholar 

  48. Goessl C, Krause H, Muller M, Heicappell R, Schrader M, Sachsinger J, Miller K: Fluorescent methylation-specific polymerase chain reaction for DNA-based detection of prostate cancer in bodily fluids. Cancer Res 60: 5941, 2000

    Google Scholar 

  49. Goessl C, Muller M, Heicappell R, Krause H, Straub B, Schrader M, Miller K: DNA-based detection of prostate cancer in urine after prostatic massage. Urology 58: 335, 2001

    Google Scholar 

  50. Goessl C, Muller M, Heicappell R, Krause H, Miller K: DNA-based detection of prostate cancer in blood, urine, and ejaculates. Ann N Y Acad Sci 945: 51, 2001

    Google Scholar 

  51. Jeronimo C, Usadel H, Henrique R, Oliveira J, Lopes C, Nelson WG, Sidransky D: Quantitation of GSTP1 methylation in non-neoplastic prostatic tissue and organ-confined prostate adenocarcinoma. J Natl Cancer Inst 93: 1747, 2001

    Google Scholar 

  52. Suh CI, Shanafelt T, May DJ, Shroyer KR, Bobak JB, Crawford ED, Miller GJ, Markham N, Glode LM: Comparison of telomerase activity and GSTP1 promoter methylation in ejaculate as potential screening tests for prostate cancer. Mol Cell Probes 14: 211, 2000

    Google Scholar 

  53. Santourlidis S, Florl A, Ackermann R, Wirtz HC, Schulz WA: High frequency of alterations in DNA methylation in adenocarcinoma of the prostate. Prostate 39: 166, 1999

    Google Scholar 

  54. Millar DS, Ow KK, Paul CL, Russell PJ, Molloy PL, Clark SJ: Detailed methylation analysis of the glutathione S-transferase pi (GSTP1) gene in prostate cancer. Oncogene 18: 1313, 1999

    Google Scholar 

  55. Lin X, Asgari K, Putzi MJ, Gage WR, Yu X, Cornblatt BS, Kumar A, Piantadosi S, DeWeese TL, De Marzo AM, Nelson WG: Reversal of GSTP1 CpG island hypermethylation and reactivation of pi-class glutathione S-transferase (GSTP1) expression in human prostate cancer cells by treatment with procainamide. Cancer Res 61: 8611, 2001

    Google Scholar 

  56. Singal R, van Wert J, Bashambu M: Cytosine methylation represses glutathione S-transferase P1 (GSTP1) gene expression in human prostate cancer cells. Cancer Res 61: 4820, 2001

    Google Scholar 

  57. Ng HH, Jeppesen P, Bird A: Active repression of methylated genes by the chromosomal protein MBD1. Mol Cell Biol 20: 1394, 2000

    Google Scholar 

  58. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, Reinberg D: Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 13: 1924, 1999

    Google Scholar 

  59. Mielnicki LM, Ying AM, Head KL, Asch HL, Asch BB: Epigenetic regulation of gelsolin expression in human breast cancer cells. Exp Cell Res 249: 161, 1999

    Google Scholar 

  60. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP: Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19: 187, 1998

    Google Scholar 

  61. Cameron EE, Bachman KE, Myohanen S, Herman JG, Baylin SB: Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21: 103, 1999

    Google Scholar 

  62. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A: Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386, 1998

    Google Scholar 

  63. Pikaart MJ, Recillas-Targa F, Felsenfeld G: Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators. Genes Dev 12: 2852, 1998

    Google Scholar 

  64. Brawley OW, Knopf K, Thompson I: The epidemiology of prostate cancer part II: the risk factors. Semin Urol Oncol 16: 193, 1998

    Google Scholar 

  65. Carter BS, Carter HB, Isaacs JT: Epidemiologic evidence regarding predisposing factors to prostate cancer. Prostate 16: 187, 1990

    Google Scholar 

  66. Haenszel W, Kurihara M: Studies of Japanese migrants. I. Mortality from cancer and other diseases among Japanese in the United States. J Natl Cancer Inst 40: 43, 1968

    Google Scholar 

  67. Danley KL, Richardson JL, Bernstein L, Langholz B, Ross RK: Prostate cancer: Trends in mortality and stage-specific incidence rates by racial/ethnic group in Los Angeles County, California (United States). Cancer Causes Control 6: 492, 1995

    Google Scholar 

  68. Giovannucci E, Rimm EB, Colditz GA, Stampfer MJ, Ascherio A, Chute CC, Willett WC: A prospective study of dietary fat and risk of prostate cancer. J Natl Cancer Inst 85: 1571, 1993

    Google Scholar 

  69. Gann PH, Hennekens CH, Sacks FM, Grodstein F, Giovannucci EL, Stampfer MJ: Prospective study of plasma fatty acids and risk of prostate cancer. J Natl Cancer Inst 86: 281, 1994

    Google Scholar 

  70. Le Marchand L, Kolonel LN, Wilkens LR, Myers BC, Hirohata T: Animal fat consumption and prostate cancer: A prospective study in Hawaii. Epidemiology 5: 276, 1994

    Google Scholar 

  71. Gross GA, Turesky RJ, Fay LB, Stillwell WG, Skipper PL, Tannenbaum SR: Heterocyclic aromatic amine formation in grilled bacon, beef and fish and in grill scrapings. Carcinogenesis 14: 2313, 1993

    Google Scholar 

  72. Lijinsky W, Shubik P: Benzo(a)pyrene and other polynuclear hydrocarbons in charcoal-broiled meat. Science 145: 53, 1964

    Google Scholar 

  73. Gann PH, Ma J, Giovannucci E, Willett W, Sacks FM, Hennekens CH, Stampfer MJ: Lower prostate cancer risk in men with elevated plasma lycopene levels: Results of a prospective analysis. Cancer Res 59: 1225, 1999

    Google Scholar 

  74. Giovannucci E, Ascherio A, Rimm EB, Stampfer MJ, Colditz GA, Willett WC: Intake of carotenoids and retinal in relation to risk of prostate cancer. J Natl Cancer Inst 87: 1767, 1995

    Google Scholar 

  75. Giovannucci E: Tomatoes, tomato-based products, lycopene, and cancer: Review of the epidemiologic literature. J Natl Cancer Inst 91: 317, 1999

    Google Scholar 

  76. Jain MG, Hislop GT, Howe GR, Ghadirian P: Plant foods, antioxidants, and prostate cancer risk: Findings from case-control studies in Canada. Nutr Cancer 34: 173, 1999

    Google Scholar 

  77. Cohen JH, Kristal AR, Stanford JL: Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst 92: 61, 2000

    Google Scholar 

  78. Kolonel LN, Hankin JH, Whittemore AS, Wu AH, Gallagher RP, Wilkens LR, John EM, Howe GR, Dreon DM, West DW, Paffenbarger RS Jr: Vegetables, fruits, legumes and prostate cancer: A multiethnic case-control study. Cancer Epidemiol Biomarkers Prev 9: 795, 2000

    Google Scholar 

  79. Zhang Y, Talalay P, Cho CG, Posner GH: A major inducer of anticarcinogenic protective enzymes from broccoli: Isolation and elucidation of structure. Proc Natl Acad Sci USA 89: 2399, 1992

    Google Scholar 

  80. Clinton SK: The dietary antioxidant network and prostate carcinoma. Cancer 86: 1629, 1999

    Google Scholar 

  81. Christen S, Woodall AA, Shigenaga MK, Southwell-Keely PT, Duncan MW, Ames BN: Gamma-tocopherol traps mutagenic electrophiles such as NO(X) and complements alpha-tocopherol: Physiological implications. Proc Natl Acad Sci USA 94: 3217, 1997

    Google Scholar 

  82. Freeman VL, Meydani M, Yong S, Pyle J, Wan Y, Arvizu-Durazo R, Liao Y: Prostatic levels of tocopherols, carotenoids, and retinol in relation to plasma levels and self-reported usual dietary intake. Am J Epidemiol 151: 109, 2000

    Google Scholar 

  83. Clinton SK, Emenhiser C, Schwartz SJ, Bostwick DG, Williams AW, Moore BJ, Erdman JW Jr: Cis-trans lycopene isomers, carotenoids, and retinol in the human prostate. Cancer Epidemiol Biomarkers Prev 5: 823, 1996

    Google Scholar 

  84. Clark LC, Combs GF Jr, Turnbull BW, Slate EH, Chalker DK, Chow J, Davis LS, Glover RA, Graham GF, Gross EG, Krongrad A, Lesher JL Jr, Park HK, Sanders BB Jr, Smith CL, Taylor JR: Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial. Nutritional Prevention of Cancer Study Group (see comments) (published erratum appears in JAMA 1997 May 21; 277(19): 1520). JAMA 276: 1957, 1996

    Google Scholar 

  85. Clark LC, Dalkin B, Krongrad A, Combs GF Jr, Turnbull BW, Slate EH, Witherington R, Herlong JH, Janosko E, Carpenter D, Borosso C, Falk S, Rounder J: Decreased incidence of prostate cancer with selenium supplementation: Results of a double-blind cancer prevention trial. Br J Urol 81: 730, 1998

    Google Scholar 

  86. Heinonen OP, Albanes D, Virtamo J, Taylor PR, Huttunen JK, Hartman AM, Haapakoski J, Malila N, Rautalahti M, Ripatti S, Maenpaa H, Teerenhovi L, Koss L, Virolainen M, Edwards BK: Prostate cancer and supplementation with alpha-tocopherol and beta-carotene: Incidence and mortality in a controlled trial (see comments). J Natl Cancer Inst 90: 440, 1998

    Google Scholar 

  87. Zhang Y, Kensler TW, Cho CG, Posner GH, Talalay P: Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proc Natl Acad Sci USA 91: 3147, 1994

    Google Scholar 

  88. Fahey JW, Zhang Y, Talalay P: Broccoli sprouts: An exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci USA 94: 10,367, 1997

    Google Scholar 

  89. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P: Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: Metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev 10: 501, 2001

    Google Scholar 

  90. Hayes RB, Pottern LM, Strickler H, Rabkin C, Pope V, Swanson GM, Greenberg RS, Schoenberg JB, Liff J, Schwartz AG, Hoover RN, Fraumeni JF Jr: Sexual behaviour, STDs and risks for prostate cancer. Br J Cancer 82: 718, 2000

    Google Scholar 

  91. Ames BN, Gold LS, Willett WC: The causes and prevention of cancer. Proc Natl Acad Sci USA 92: 5258, 1995

    Google Scholar 

  92. Roberts RO, Lieber MM, Rhodes T, Girman CJ, Bostwick DG, Jacobsen SJ: Prevalence of a physician-assigned diagnosis of prostatitis: The olmsted county study of urinary symptoms and health status among men. Urology 51: 578, 1998

    Google Scholar 

  93. Rushmore TH, King RG, Paulson KE, Pickett CB: Regulation of glutathione S-transferase Ya subunit gene expression: Identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc Natl Acad Sci USA 87: 3826, 1990

    Google Scholar 

  94. Rushmore TH, Pickett CB: Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants. J Biol Chem 265: 14648, 1990

    Google Scholar 

  95. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW: From the Cover: Sensitivity to carcinogenesis is increased and chemo-protective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 98: 3410, 2001

    Google Scholar 

  96. Henderson CJ, Smith AG, Ure J, Brown K, Bacon EJ, Wolf CR: Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc Natl Acad Sci USA 95: 5275, 1998

    Google Scholar 

  97. Nelson CP, Kidd LC, Sauvageot J, Isaacs WB, De Marzo AM, Groopman JD, Nelson WG, Kensler TW: Protection against 2-hydroxyamino-1-methyl-6-phenylimidazo[4,5-b]pyridine cytotoxicity and DNA adduct formation in human prostate by glutathione Stransferase P1. Cancer Res 61: 103, 2001

    Google Scholar 

  98. Morgenthaler PM, Holzhauser D: Analysis of mutations induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in human lymphoblastoid cells. Carcinogenesis 16: 713, 1995

    Google Scholar 

  99. Nagaoka H, Wakabayashi K, Kim SB, Kim IS, Tanaka Y, Ochiai M, Tada A, Nukaya H, Sugimura T, Nagao M: Adduct formation at C-8 of guanine on in vitro reaction of the ultimate form of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine with 2_-deoxyguanosine and its phosphate esters. Jpn J Cancer Res 83: 1025, 1992

    Google Scholar 

  100. Knize MG, Sinha R, Rothman N, Brown ED, Salmon CP, Levander OA, Cunningham PL, Felton JS: Heterocyclic amine content in fast-food meat products. Food Chem Toxicol 33: 545, 1995

    Google Scholar 

  101. Davis CD, Schut HA, Snyderwine EG: Adduction of the heterocyclic amine food mutagens IQ and PhIP to mitochondrial and nuclear DNA in the liver of Fischer-344 rats. Carcinogenesis 15: 641, 1994

    Google Scholar 

  102. Shirai T, Sano M, Tamano S, Takahashi S, Hirose M, Futakuchi M, Hasegawa R, Imaida K, Matsumoto K, Wakabayashi K, Sugimura T, Ito N: The prostate: A target for carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) derived from cooked foods. Cancer Res 57: 195, 1997

    Google Scholar 

  103. Shirai T, Cui L, Takahashi S, Futakuchi M, Asamoto M, Kato K, Ito N: Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine (PhIP) in the rat prostate and induction of invasive carcinomas by subsequent treatment with testosterone propionate. Cancer Lett 143: 217, 1999

    Google Scholar 

  104. Stuart GR, Holcroft J, de Boer JG, Glickman BW: Prostate mutations in rats induced by the suspected human carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Cancer Res 60: 266, 2000

    Google Scholar 

  105. Fields WR, Morrow CS, Doss AJ, Sundberg K, Jernstrom B, Townsend AJ: Overexpression of stably transfected human glutathione S-transferase P1-1 protects against DNA damage by benzo[a]pyrene diol-epoxide in human T47D cells. Mol Pharmacol 54: 298, 1998

    Google Scholar 

  106. Sundberg K, Johansson AS, Stenberg G, Widersten M, Seidel A, Mannervik B, Jernstrom B: Differences in the catalytic efficiencies of allelic variants of glutathione transferase P1-1 towards carcinogenic diol epoxides of polycyclic aromatic hydrocarbons. Carcinogenesis 19: 433, 1998

    Google Scholar 

  107. Helzlsouer KJ, Selmin O, Huang HY, Strickland PT, Hoffman S, Alberg AJ, Watson M, Comstock GW, Bell D: Association between glutathione S-transferase M1, P1, and T1 genetic polymorphisms and development of breast cancer. J Natl Cancer Inst 90: 512, 1998

    Google Scholar 

  108. Henderson CJ, Wolf CR, Kitteringham N, Powell H, Otto D, Park BK: Increased resistance to acetaminophen hepatotoxicity in mice lacking glutathione S-transferase Pi. Proc Natl Acad Sci USA 97: 12,741, 2000

    Google Scholar 

  109. Diah SK, Smitherman PK, Townsend AJ, Morrow CS: Detoxification of 1-chloro-2,4-dinitrobenzene in MCF7 breast cancer cells expressing glutathione S-transferase P1-1 and/or multidrug resistance protein 1. Toxicol Appl Pharmacol 157: 85, 1999

    Google Scholar 

  110. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CJ, Wolf CR, Davis RJ, Ronai Z: Regulation of JNK signaling by GSTp. Embo J 18: 1321, 1999

    Google Scholar 

  111. Wang T, Arifoglu P, Ronai Z, Tew KD: Glutathione Stransferase P1-1 (GSTP1-1) Inhibits c-Jun N-terminal Kinase (JNK1) signaling through interaction with the C terminus. J Biol Chem 276: 20999, 2001

    Google Scholar 

  112. Yin Z, Ivanov VN, Habelhah H, Tew K, Ronai Z: Glutathione S-transferase p elicits protection against H2O2-induced cell death via coordinated regulation of stress kinases. Cancer Res 60: 4053, 2000

    Google Scholar 

  113. Ruscoe JE, Rosario LA, Wang T, Gate L, Arifoglu P, Wolf CR, Henderson CJ, Ronai Z, Tew KD: Pharmacologic or genetic manipulation of glutathione S-transferase P1-1 (GSTpi) influences cell proliferation pathways. J Pharmacol Exp Ther 298: 339, 2001

    Google Scholar 

  114. Reznik G, Hamlin MH II, Ward JM, Stinson SF: Prostatic hyperplasia and neoplasia in aging F344 rats. Prostate 2: 261, 1981

    Google Scholar 

  115. Gilardoni MB, Rabinovich GA, Oviedo M, Depiante-Depaoli M: Prostate cancer induction in autoimmune rats and modulation of T cell apoptosis. J Exp Clin Cancer Res 18: 493, 1999

    Google Scholar 

  116. Yoshizawa K, Willett WC, Morris SJ, Stampfer MJ, Spiegelman D, Rimm EB, Giovannucci E: Study of prediagnostic selenium level in toenails and the risk of advanced prostate cancer (see comments). J Natl Cancer Inst 90: 1219, 1998

    Google Scholar 

  117. Helzlsouer KJ, Huang HY, Alberg AJ, Hoffman S, Burke A, Norkus EP, Morris JS, Comstock GW: Association between alpha-tocopherol, gamma-tocopherol, selenium, and subsequent prostate cancer. J Natl Cancer Inst 92: 2018, 2000

    Google Scholar 

  118. Kucuk O, Sarkar FH, Sakr W, Djuric Z, Pollak MN, Khachik F, Li YW, Banerjee M, Grignon D, Bertram JS, Crissman JD, Pontes EJ, Wood DP Jr: Phase II randomized clinical trial of lycopene supplementation before radical prostatectomy. Cancer Epidemiol Biomarkers Prev 10: 861, 2001

    Google Scholar 

  119. Chen L, Stacewicz-Sapuntzakis M, Duncan C, Sharifi R, Ghosh L, Breemen Rv R, Ashton D, Bowen PE: Oxidative DNA damage in prostate cancer patients consuming tomato sauce-based entrees as a whole-food intervention. J Natl Cancer Inst 93: 1872, 2001

    Google Scholar 

  120. Wechter WJ, Leipold DD, Murray ED Jr, Quiggle D, McCracken JD, Barrios RS, Greenberg NM: E-7869 (R-flurbiprofen) inhibits progression of prostate cancer in the TRAMP mouse. Cancer Res 60: 2203, 2000

    Google Scholar 

  121. Nelson JE, Harris RE: Inverse association of prostate cancer and non-steroidal anti-inflammatory drugs (NSAIDs): Results of a case-control study. Oncol Rep 7: 169, 2000

    Google Scholar 

  122. Nelson WG, Wilding G: Prostate cancer prevention agent development: Criteria and pipeline for candidate chemoprevention agents. Urology 57: 56, 2001

    Google Scholar 

  123. Rountree MR, Bachman KE, Baylin SB: DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet 25: 269, 2000

    Google Scholar 

  124. Kensler TW: Chemoprevention by inducers of carcinogen detoxication enzymes. Environ Health Perspect 105 Suppl(4): 965, 1997

    Google Scholar 

  125. Wang JS, Shen X, He X, Zhu YR, Zhang BC, Wang JB, Qian GS, Kuang SY, Zarba A, Egner PA, Jacobson LP, Munoz A, Helzlsouer KJ, Groopman JD, Kensler TW: Protective alterations in phase 1 and 2 metabolism of aflatoxin B1 by oltipraz in residents of Qidong, People's Republic of China. J Natl Cancer Inst 91: 347, 1999

    Google Scholar 

  126. Jacobson LP, Zhang BC, Zhu YR, Wang JB, Wu Y, Zhang QN, Yu LY, Qian GS, Kuang SY, Li YF, Fang X, Zarba A, Chen B, Enger C, Davidson NE, Gorman MB, Gordon GB, Prochaska HJ, Egner PA, Groopman JD, Munoz A, Helzlsouer KJ, Kensler TW: Oltipraz chemoprevention trial in Qidong, People's Republic of China: Study design and clinical outcomes. Cancer Epidemiol Biomarkers Prev 6: 257, 1997

    Google Scholar 

  127. Kensler TW, He X, Otieno M, Egner PA, Jacobson LP, Chen B, Wang JS, Zhu YR, Zhang BC, Wang JB, Wu Y, Zhang QN, Qian GS, Kuang SY, Fang X, Li YF, Yu LY, Prochaska HJ, Davidson NE, Gordon GB, Gorman MB, Zarba A, Enger C, Munoz A, Helzlsouer KJ: Oltipraz chemoprevention trial in Qidong, People's Republic of China: Modulation of serum aflatoxin albumin adduct biomarkers. Cancer Epidemiol Biomarkers Prev 7: 127, 1998

    Google Scholar 

  128. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P: Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol Biomarkers Prev 7: 1091, 1998

    Google Scholar 

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Nelson, W.G., DeWeese, T.L. & DeMarzo, A.M. The Diet, Prostate Inflammation, and the Development of Prostate Cancer. Cancer Metastasis Rev 21, 3–16 (2002). https://doi.org/10.1023/A:1020110718701

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