Constitutive expression of bioactivating enzymes in normal human prostate suggests a capability to activate pro-carcinogens to DNA-damaging metabolites

Prostate

Volumn 70, Issue 14, 2010, Pages 1586-1599

  Martin, Francis L ^a   Patel, Imran I ^a   Sozeri, Osman ^b   Singh, Paras B ^a   Ragavan, Narasimhan ^a   Nicholson, Caroline M ^c   Frei, Eva ^d   Meinl, Walter ^e   Glatt, Hansruedi ^e   Phillips, David H ^b   Arlt, Volker M ^b  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c LANCASHIRE TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

Bioactivation; Carcinogenesis; Constitutive expression; Etiology; Phase I II metabolism; Prostate

Indexed keywords

ACYLTRANSFERASE; CARCINOGEN; CYCLOOXYGENASE 1; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; DNA; ENZYME; PROSTAGLANDIN SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; AMINO ACID ACETYLTRANSFERASE; CYTOCHROME P 450 CYP1B1; CYTOCHROME P-450 CYP1B1; ESTRADIOL; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; UNSPECIFIC MONOOXYGENASE;

ADULT; AGED; ARTICLE; CANCER RISK; CARCINOGENESIS; CAUCASIAN; CLINICAL ARTICLE; DNA DAMAGE; ENZYME ACTIVITY; ENZYME METABOLISM; EPITHELIUM CELL; HISTOCHEMISTRY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; RADICAL RETROPUBIC PROSTATECTOMY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROMA; UNITED KINGDOM; WESTERN BLOTTING; BLOOD; DNA ADDUCT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PROSTATE; PROSTATECTOMY;

AGED; AGED, 80 AND OVER; AMINO-ACID N-ACETYLTRANSFERASE; ARYL HYDROCARBON HYDROXYLASES; BLOTTING, WESTERN; CARCINOGENS; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DNA ADDUCTS; DNA DAMAGE; ESTRADIOL; GENE EXPRESSION REGULATION; HUMANS; MALE; MIDDLE AGED; PROSTATE; PROSTATECTOMY; SEX HORMONE-BINDING GLOBULIN; TESTOSTERONE;

EID: 77957004254     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.21194     Document Type: Article

References (49)

1. Williams JA, Martin FL, Muir GH, Hewer A, Grover PL, Phillips DH,. Metabolic activation of carcinogens and expression of various cytochromes P450 in human prostate tissue. Carcinogenesis 2000; 21: 1683 -1689.
2. Ragavan N, Hewitt R, Cooper LJ, Ashton KM, Hindley AC, Nicholson CM, Fullwood NJ, Matanhelia SS, Martin FL,. CYP1B1 expression in prostate is higher in the peripheral than in the transition zone. Cancer Lett 2004; 215: 69 -78.
3. John K, Ragavan N, Pratt MM, Singh PB, Al-Buheissi S, Matanhelia SS, Phillips DH, Poirier MC, Martin FL,. Quantification of phase I/II metabolizing enzyme gene expression and polycyclic aromatic hydrocarbon-DNA adduct levels in human prostate. Prostate 2009; 69: 505 -519.
4. Wang CY, Debiec-Rychter M, Schut HA, Morse P, Jones RF, Archer C, King CM, Haas GP,. N-acetyltransferase expression and DNA binding of N-hydroxyheterocyclic amines in human prostate epithelium. Carcinogenesis 1999; 20: 1591 -1595.
5. 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 S-transferase P1. Cancer Res 2001; 61: 103 -109.
6. McNeal JE,. Normal histology of the prostate. Am J Surg Pathol 1988; 12: 619 -633.
7. Kobayashi M, Ishida H, Shindo T, Niwa S, Kino M, Kawamura K, Kamiya N, Imamoto T, Suzuki H, Hirokawa Y, Shiraishi T, Tanizawa T, Nakatani Y, Ichikawa T,. Molecular analysis of multifocal prostate cancer by comparative genomic hybridization. Prostate 2008; 68: 1715 -1724.
8. Grönberg H,. Prostate cancer epidemiology. Lancet 2003; 361: 859 -864.
9. Edwards SM, Dearnaley DP, Ardern-Jones A, Hamoudi RA, Easton DF, Ford D, Shearer R, Dowe A, Eeles RA,. No germline mutations in the dimerization domain of MXI1 in prostate cancer clusters. The CRC/BPG UK Familial Prostate Cancer Study Collaborators. Cancer Research Campaign/British Prostate Group. Br J Cancer 1997; 76: 992 -1000.
10. Eeles RA, Kote-Jarai Z, Al Olama AA, Giles GG, Guy M, Severi G, Muir K, Hopper JL, Henderson BE, Haiman CA, Schleutker J, Hamdy FC, Neal DE, Donovan JL, Stanford JL, Ostrander EA, Ingles SA, John EM, Thibodeau SN, Schaid D, Park JY, Spurdle A, Clements J, Dickinson JL, Maier C, Vogel W, Dörk T, Rebbeck TR, Cooney KA, Cannon-Albright L, Chappuis PO, Hutter P, Zeegers M, Kaneva R, Zhang HW, Lu YJ, Foulkes WD, English DR, Leongamornlert DA, Tymrakiewicz M, Morrison J, Ardern-Jones AT, Hall AL, O'Brien LT, Wilkinson RA, Saunders EJ, Page EC, Sawyer EJ, Edwards SM, Dearnaley DP, Horwich A, Huddart RA, Khoo VS, Parker CC, Van As N, Woodhouse CJ, Thompson A, Christmas T, Ogden C, Cooper CS, Southey MC, Lophatananon A, Liu JF, Kolonel LN, Le Marchand L, Wahlfors T, Tammela TL, Auvinen A, Lewis SJ, Cox A, FitzGerald LM, Koopmeiners JS, Karyadi DM, Kwon EM, Stern MC, Corral R, Joshi AD, Shahabi A, McDonnell SK, Sellers TA, Pow-Sang J, Chambers S, Aitken J, Gardiner RA, Batra J, Kedda MA, Lose F, Polanowski A, Patterson B, Serth J, Meyer A, Luedeke M, Stefflova K, Ray AM, Lange EM, Farnham J, Khan H, Slavov C, Mitkova A, Cao G, UK Genetic Prostate Cancer Study Collaborators/British Association of Urological Surgeons' Section of Oncology, UK ProtecT Study Collaborators, PRACTICAL Consortium, Easton DF. Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat Genet 2009; 41: 1116 -1121.
11. Al Olama AA, Kote-Jarai Z, Giles GG, Guy M, Morrison J, Severi G, Leongamornlert DA, Tymrakiewicz M, Jhavar S, Saunders E, Hopper JL, Southey MC, Muir KR, English DR, Dearnaley DP, Ardern-Jones AT, Hall AL, O'Brien LT, Wilkinson RA, Sawyer E, Lophatananon A, UK Genetic Prostate Cancer Study Collaborators/British Association of Urological Surgeons' Section of Oncology, UK Prostate testing for cancer and Treatment study (ProtecT Study) Collaborators, Horwich A, Huddart RA, Khoo VS, Parker CC, Woodhouse CJ, Thompson A, Christmas T, Ogden C, Cooper C, Donovan JL, Hamdy FC, Neal DE, Eeles RA, Easton DF,. Multiple loci on 8q24 associated with prostate cancer susceptibility. Nat Genet 2009; 41: 1058 -1060.
12. Ragavan N, Grover PL, Balasubramanian SP, Hindley AC, Matanhelia SS, Martin FL,. An observational study of cancers among female partners of UK-resident prostate cancer patients. Cancer Lett 2006; 242: 88 -94.
13. Brooks JD,. Anatomy of lower urinary tract and male genitalia. In:, Wein AJ, Kavoussi LR, Novick AC, Partin AW, Peters CA, editors. Campbell-Walsh Urology 1. New York: Saunders; 2007. pp. 61 -63.
14. McNeal JE,. The zonal anatomy of the prostate. Prostate 1981; 2: 35 -49.
15. Noel EE, Ragavan N, Walsh MJ, James SY, Matanhelia SS, Nicholson CM, Lu YJ, Martin FL,. Differential gene expression in the peripheral zone compared to the transition zone of the human prostate gland. Prostate Cancer Prostatic Dis 2008; 11: 173 -180.
16. McNeal JE, Redwine EA, Freiha FS, Stamey TA,. Zonal distribution of prostatic adenocarcinoma. Correlation with histologic pattern and direction of spread. Am J Surg Pathol 1988; 12: 897 -906.
17. Zenzmaier C, Untergasser G, Berger P,. Aging of the prostate epithelial stem/progenitor cell. Exp Gerontol 2008; 43: 981 -985.
18. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D,. Estrogens as endogenous genotoxic agents-DNA adducts and mutations. J Natl Cancer Inst Monogr 2000; 27: 75 -93.
19. Nock NL, Tang D, Rundle A, Neslund-Dudas C, Savera AT, Bock CH, Monaghan KG, Koprowski A, Mitrache N, Yang JJ, Rybicki BA,. Associations between smoking, polymorphisms in polycyclic aromatic hydrocarbon (PAH) metabolism and conjugation genes and PAH-DNA adducts in prostate tumors differ by race. Cancer Epidemiol Biomarkers Prev 2007; 16: 1236 -1245.
20. Rybicki BA, Neslund-Dudas C, Bock CH, Rundle A, Savera AT, Yang JJ, Nock NL, Tang D,. Polycyclic aromatic hydrocarbon-DNA adducts in prostate and biochemical recurrence after prostatectomy. Clin Cancer Res 2008; 14: 750 -757.
21. Pfau W, Martin FL, Cole KJ, Venitt S, Phillips DH, Grover PL, Marquardt H,. Heterocyclic aromatic amines induce DNA strand breaks and cell transformation. Carcinogenesis 1999; 20: 545 -551.
22. Courter LA, Luch A, Musafia-Jeknic T, Arlt VM, Fischer K, Bildfell R, Pereira C, Phillips DH, Poirier MC, Baird WM,. The influence of diesel exhaust on polycyclic aromatic hydrocarbon-induced DNA damage, gene expression, and tumor initiation in Sencar mice in vivo. Cancer Lett 2008; 265: 135 -147.
23. Singh PB, Matanhelia SS, Martin FL,. A potential paradox in prostate adenocarcinoma progression: Oestrogen as the initiating driver. Eur J Cancer 2008; 44: 928 -936.
24. Al-Buheissi SZ, Patel HR, Meinl W, Hewer A, Bryan RL, Glatt H, Miller RA, Phillips DH,. N-Acetyltransferase and sulfotransferase activity in human prostate: Potential for carcinogen activation. Pharmacogenet Genomics 2006; 16: 391 -399.
25. Carnell DM, Smith RE, Daley FM, Barber PR, Hoskin PJ, Wilson GD, Murray GI, Everett SA,. Target validation of cytochrome P450 CYP1B1 in prostate carcinoma with protein expression in associated hyperplastic and premalignant tissue. Int J Radiat Oncol Biol Phys 2004; 58: 500 -509.
26. Muskhelishvili L, Thompson PA, Kusewitt DF, Wang C, Kadlubar FF,. In situ hybridization and immunohistochemical analysis of cytochrome P450 1B1 expression in human normal tissues. J Histochem Cytochem 2001; 49: 229 -236.
27. Di Paolo OA, Teitel CH, Nowell S, Coles BF, Kadlubar FF,. Expression of cytochromes P450 and glutathione S-transferases in human prostate, and the potential for activation of heterocyclic amine carcinogens via acetyl-coA-, PAPS-and ATP-dependent pathways. Int J Cancer 2005; 117: 8 -13.
28. Finnstrm N, Bjelfman C, Sderstrm TG, Smith G, Egevad L, Norln BJ, Wolf CR, Rane A,. Detection of cytochrome P450 mRNA transcripts in prostate samples by RT-PCR. Eur J Clin Invest 2001; 31: 880 -886.
29. Sun L, Caire AA, Robertson CN, George DJ, Polascik TJ, Maloney KE, Walther PJ, Stackhouse DA, Lack BD, Albala DM, Moul JW,. Men older than 70 years have higher risk prostate cancer and poorer survival in the early and late prostate specific antigen eras. J Urol 2009; 182: 2242 -2249.
30. Martin FL, Carmichael PL, Crofton-Sleigh C, Venitt S, Phillips DH, Grover PL,. Genotoxicity of human mammary lipid. Cancer Res 1996; 56: 5342 -5346.
31. Williams JA, Phillips DH,. Mammary expression of xenobiotic metabolizing enzymes and their potential role in breast cancer. Cancer Res 2000; 60: 4667 -4677.
32. Singh PB, Ragavan N, Ashton KM, Basu P, Nadeem SM, Nicholson CM, Gopala Krishna RK, Matanhelia SS, Martin FL,. Quantified gene expression levels for phase I/II metabolizing enzyme and estrogen receptor levels in benign prostate from cohorts designated as high-risk (UK) versus low-risk (India) for adenocarcinoma at this organ site: A preliminary study. Asian J Androl 2010; 12: 203 -214.
33. Martin FL, Cole KJ, Muir GH, Kooiman GG, Williams JA, Sherwood RA, Grover PL, Phillips DH,. Primary cultures of prostate cells and their ability to activate carcinogens. Prostate Cancer Prostatic Dis 2002; 5: 96 -104.
34. Arlt VM, Stiborov M, Henderson CJ, Osborne MR, Bieler CA, Frei E, Martinek V, Sopko B, Wolf CR, Schmeiser HH, Phillips DH,. Environmental pollutant and potent mutagen 3-nitrobenzanthrone forms DNA adducts after reduction by NAD(P)H:quinone oxidoreductase and conjugation by acetyltransferases and sulfotransferases in human hepatic cytosols. Cancer Res 2005; 65: 2644 -2652.
35. Stiborov M, Dracinska H, Hajkova J, Kaderabkova P, Frei E, Schmeiser HH, Soucek P, Phillips DH, Arlt VM,. The environmental pollutant and carcinogen 3-nitrobenzanthrone and its human metabolite 3-aminobenzanthrone are potent inducers of rat hepatic cytochromes P450 1A1 and -1A2 and NAD(P)H:quinone oxidoreductase. Drug Metab Dispos 2006; 34: 1398 -1405.
36. Stiborov M, Frei E, Arlt VM, Schmeiser HH,. Metabolic activation of carcinogenic aristolochic acid, a risk factor for Balkan endemic nephropathy. Mutat Res 2008; 658: 55 -67.
37. Stiborov M, Arlt VM, Henderson CJ, Wolf CR, Kotrbov V, Moserov M, Hudecek J, Phillips DH, Frei E,. Role of hepatic cytochromes P450 in bioactivation of the anticancer drug ellipticine: Studies with the hepatic NADPH:cytochrome P450 reductase null mouse. Toxicol Appl Pharmacol 2008; 226: 318 -327.
38. Arlt VM, Stiborov M, Hewer A, Schmeiser HH, Phillips DH,. Human enzymes involved in the metabolic activation of the environmental contaminant 3-nitrobenzanthrone: Evidence for reductive activation by human NADPH:cytochrome p450 reductase. Cancer Res 2003; 63: 2752 -2761.
39. Yared E, McMillan TJ, Martin FL,. Genotoxic effects of oestrogens in breast cells detected by the micronucleus assay and the Comet assay. Mutagenesis 2002; 17: 345 -352.
40. Taylor SE, Martin-Hirsch PL, Martin FL,. Oestrogen receptor splice variants in the pathogenesis of disease. Cancer Lett 2010; 288: 133 -148.
41. Arlt VM, Stiborov M, Henderson CJ, Thiemann M, Frei E, Aimov D, Singh R, Gamboa da Costa G, Schmitz OJ, Farmer PB, Wolf CR, Phillips DH,. Metabolic activation of benzo[a]pyrene in vitro by hepatic cytochrome P450 contrasts with detoxification in vivo: Experiments with hepatic cytochrome P450 reductase null mice. Carcinogenesis 2008; 29: 656 -665.
42. Muckel E, Frandsen H, Glatt HR,. Heterologous expression of human N-acetyltransferases 1 and 2 and sulfotransferase 1A1 in Salmonella typhimurium for mutagenicity testing of heterocyclic amines. Food Chem Toxicol 2002; 40: 1063 -1068.
43. Teubner W, Meinl W, Florian S, Kretzschmar M, Glatt H,. Identification and localization of soluble sulfotransferases in the human gastrointestinal tract. Biochem J 2007; 404: 207 -215.
44. Arlt VM, Glatt H, Gamboa da Costa G, Reynisson J, Takamura-Enya T, Phillips DH,. Mutagenicity and DNA adduct formation by the urban air pollutant 2-nitrobenzanthrone. Toxicol Sci 2007; 98: 445 -457.
45. White IN,. A continuous fluorometric assay for cytochrome P-450-dependent mixed function oxidases using 3-cyano-7-ethoxycoumarin. Anal Biochem 1988; 172: 304 -310.
46. Gleason DF,. The Veterans Administration Cooperative Urologic Research Group: Histologic grading and clinical staging of prostatic carcinoma. In:, Tannenbaum M, editor. Urologic pathology: the prostate. Philadelphia, PA: Lea and Febiger; 1977. pp. 171 -198.
47. Grover PL, Martin FL,. The initiation of breast and prostate cancer. Carcinogenesis 2002; 23: 1095 -1102.
48. Hewitt R, Forero A, Luncsford PJ, Martin FL,. Enhanced micronucleus formation and modulation of BCL-2:BAX in MCF-7 cells after exposure to binary mixtures. Environ Health Perspect 2007; 115: 129 -136.
49. Saini S, Hirata H, Majid S, Dahiya R,. Functional significance of cytochrome P450 1B1 in endometrial carcinogenesis. Cancer Res 2009; 69: 7038 -7045.