The Epigenetic promise for prostate cancer diagnosis

Prostate

Volumn 72, Issue 11, 2012, Pages 1248-1261

  Van Neste, Leander ^a   Herman, James G ^b   Otto, Gaëtan ^a   Bigley, Joseph W ^a   Epstein, Jonathan I ^b   Van Criekinge, Wim ^a,c  

^a MDxHealth   (Belgium)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

APC; cancer; diagnosis; DNA methylation; epigenetics; field effect; GSTP1; PCA3; prognosis; prostate; PSA; RARB; screening

Indexed keywords

MESSENGER RNA; PROSTATE SPECIFIC ANTIGEN;

CANCER DIAGNOSIS; CANCER PROGNOSIS; CANCER SCREENING; CANCER SURVIVAL; DIAGNOSTIC ACCURACY; DIGITAL RECTAL EXAMINATION; DNA METHYLATION; EARLY DIAGNOSIS; EPIGENETICS; GENE; GENE FREQUENCY; GSTP1 GENE; HISTOPATHOLOGY; HUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PROSTATE BIOPSY; PROSTATE CANCER; PROSTATE HYPERTROPHY; PROSTATECTOMY; REVIEW; SENSITIVITY AND SPECIFICITY;

BIOLOGICAL MARKERS; DNA METHYLATION; EARLY DETECTION OF CANCER; EPIGENOMICS; GLUTATHIONE S-TRANSFERASE PI; HUMANS; MALE; PROGNOSIS; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS;

EID: 84862870008     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.22459     Document Type: Review

References (129)

1. Jemal A, Siegel R, Xu J, Ward E,. Cancer statistics, 2010. CA Cancer J Clin 2010; 60 (5): 277-300.
2. Jemal A, Clegg LX, Ward E, Ries LA, Wu X, Jamison PM, Wingo PA, Howe HL, Anderson RN, Edwards BK,. Annual report to the nation on the status of cancer, 1975-2001, with a special feature regarding survival. Cancer 2004; 101 (1): 3-27.
3. Hankey BF, Feuer EJ, Clegg LX, Hayes RB, Legler JM, Prorok PC, Ries LA, Merrill RM, Kaplan RS,. Cancer surveillance series: Interpreting trends in prostate cancer-Part I: Evidence of the effects of screening in recent prostate cancer incidence, mortality, and survival rates. J Natl Cancer Inst 1999; 91 (12): 1017-1024.
4. Baade PD, Coory MD, Aitken JF,. International trends in prostate-cancer mortality: The decrease is continuing and spreading. Cancer Causes Control 2004; 15 (3): 237-241.
5. Oliver SE, May MT, Gunnell D,. International trends in prostate-cancer mortality in the "PSA ERA." Int J Cancer 2001; 92 (6): 893-898.
6. Espey DK, Wu XC, Swan J, Wiggins C, Jim MA, Ward E, Wingo PA, Howe HL, Ries LA, Miller BA, Jemal A, Ahmed F, Cobb N, Kaur JS, Edwards BK,. Annual report to the nation on the status of cancer, 1975-2004, featuring cancer in American Indians and Alaska Natives. Cancer 2007; 110 (10): 2119-2152.
7. Shaw PA, Etzioni R, Zeliadt SB, Mariotto A, Karnofski K, Penson DF, Weiss NS, Feuer EJ,. An ecologic study of prostate-specific antigen screening and prostate cancer mortality in nine geographic areas of the United States. Am J Epidemiol 2004; 160 (11): 1059-1069.
8. Feuer EJ, Mariotto A, Merrill R,. Modeling the impact of the decline in distant stage disease on prostate carcinoma mortality rates. Cancer 2002; 95 (4): 870-880.
9. Barry MJ, Clinical practice. Prostate-specific-antigen testing for early diagnosis of prostate cancer. N Engl J Med 2001; 344 (18): 1373-1377.
10. Feuer EJ, Merrill RM, Hankey BF,. Cancer surveillance series: Interpreting trends in prostate cancer-Part II: Cause of death misclassification and the recent rise and fall in prostate cancer mortality. J Natl Cancer Inst 1999; 91 (12): 1025-1032.
11. Etzioni R, Legler JM, Feuer EJ, Merrill RM, Cronin KA, Hankey BF,. Cancer surveillance series: Interpreting trends in prostate cancer-Part III: Quantifying the link between population prostate-specific antigen testing and recent declines in prostate cancer mortality. J Natl Cancer Inst 1999; 91 (12): 1033-1039.
12. Herman JG, Baylin SB,. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349 (21): 2042-2054.
13. Lock LF, Takagi N, Martin GR,. Methylation of the Hprt gene on the inactive X occurs after chromosome inactivation. Cell 1987; 48 (1): 39-46.
14. Baylin SB, Fearon ER, Vogelstein B, de Bustros A, Sharkis SJ, Burke PJ, Staal SP, Nelkin BD,. Hypermethylation of the 5' region of the calcitonin gene is a property of human lymphoid and acute myeloid malignancies. Blood 1987; 70 (2): 412-417.
15. Schuebel KE, Chen W, Cope L, Glockner SC, Suzuki H, Yi JM, Chan TA, Van Neste L, Van Criekinge W, van den Bosch S, van Engeland M, Ting AH, Jair K, Yu W, Toyota M, Imai K, Ahuja N, Herman JG, Baylin SB,. Comparing the DNA hypermethylome with gene mutations in human colorectal cancer. PLoS Genet 2007; 3 (9): 1709-1723.
16. Chan TA, Glockner S, Yi JM, Chen W, Van Neste L, Cope L, Herman JG, Velculescu V, Schuebel KE, Ahuja N, Baylin SB,. Convergence of mutation and epigenetic alterations identifies common genes in cancer that predict for poor prognosis. PLoS Med 2008; 5 (5): e114.
17. Li LC, Carroll PR, Dahiya R,. Epigenetic changes in prostate cancer: Implication for diagnosis and treatment. J Natl Cancer Inst 2005; 97 (2): 103-115.
18. 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 1994; 91 (24): 11733-11737.
19. Ahmed H,. Promoter methylation in prostate cancer and its application for the early detection of prostate cancer using serum and urine samples. Biomark Cancer 2010; 2010 (2): 17-33.
20. Nadler RB, Humphrey PA, Smith DS, Catalona WJ, Ratliff TL,. Effect of inflammation and benign prostatic hyperplasia on elevated serum prostate specific antigen levels. J Urol 1995; 154 (2 Pt 1): 407-413.
21. Dalton DL,. Elevated serum prostate-specific antigen due to acute bacterial prostatitis. Urology 1989; 33 (6): 465.
22. Stamey TA, Yang N, Hay AR, McNeal JE, Freiha FS, Redwine E,. Prostate-specific antigen as a serum marker for adenocarcinoma of the prostate. N Engl J Med 1987; 317 (15): 909-916.
23. Brawn PN, Speights VO, Kuhl D, Riggs M, Spiekerman AM, McCord RG, Coffield KS, Stewart DT, Lind ML,. Prostate-specific antigen levels from completely sectioned, clinically benign, whole prostates. Cancer 1991; 68 (7): 1592-1599.
24. Epstein JI, Walsh PC, Carmichael M, Brendler CB,. Pathologic and clinical findings to predict tumor extent of nonpalpable (stage T1c) prostate cancer. JAMA 1994; 271 (5): 368-374.
25. Carter HB,. A PSA threshold of 4.0 ng/mL for early detection of prostate cancer: The only rational approach for men 50 years old and older. Urology 2000; 55 (6): 796-799.
26. Smith DS, Humphrey PA, Catalona WJ,. The early detection of prostate carcinoma with prostate specific antigen: The Washington University experience. Cancer 1997; 80 (9): 1852-1856.
27. Catalona WJ, Partin AW, Slawin KM, Brawer MK, Flanigan RC, Patel A, Richie JP, deKernion JB, Walsh PC, Scardino PT, Lange PH, Subong EN, Parson RE, Gasior GH, Loveland KG, Southwick PC,. Use of the percentage of free prostate-specific antigen to enhance differentiation of prostate cancer from benign prostatic disease: A prospective multicenter clinical trial. JAMA 1998; 279 (19): 1542-1547.
28. Catalona WJ, Richie JP, Ahmann FR, Hudson MA, Scardino PT, Flanigan RC, Dekernion JB, Ratliff TL, Kavoussi LR, Dalkin BL, Waters WB, Macfarlane MT, Southwick PC,. Comparison of digital rectal examination and serum prostate specific antigen in the early detection of prostate cancer: Results of a multicenter clinical trial of 6,630 men. J Urol 1994; 151 (5): 1283-1290.
29. Djavan B, Zlotta A, Remzi M, Ghawidel K, Basharkhah A, Schulman CC, Marberger M,. Optimal predictors of prostate cancer on repeat prostate biopsy: A prospective study of 1,051 men. J Urol 2000; 163 (4): 1144-1148 discussion 1148-1149.
30. Babaian RJ,. Extended field prostate biopsy enhances cancer detection. Urology 2000; 55 (4): 453-456.
31. Terris MK,. Extended field prostate biopsies: Too much of a good thing? Urology 2000; 55 (4): 457-460.
32. Klotz LH,. PSAdynia and other PSA-related syndromes: A new epidemic-A case history and taxonomy. Urology 1997; 50 (6): 831-832.
33. Fujita K, Landis P, McNeil BK, Pavlovich CP,. Serial prostate biopsies are associated with an increased risk of erectile dysfunction in men with prostate cancer on active surveillance. J Urol 2009; 182 (6): 2664-2669.
34. Klein T, Palisaar RJ, Holz A, Brock M, Noldus J, Hinkel A,. The impact of prostate biopsy and periprostatic nerve block on erectile and voiding function: A prospective study. J Urol 2010; 184 (4): 1447-1452.
35. Harris R, Lohr KN,. Screening for prostate cancer: An update of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med 2002; 137 (11): 917-929.
36. Vickers AJ, Till C, Tangen CM, Lilja H, Thompson IM,. An empirical evaluation of guidelines on prostate-specific antigen velocity in prostate cancer detection. J Natl Cancer Inst 2011; 103 (6): 462-469.
37. Yao SL, Lu-Yao GL,. The science and art of prostate cancer screening. J Natl Cancer Inst 2011; 103 (6): 450-451.
38. Eichler K, Hempel S, Wilby J, Myers L, Bachmann LM, Kleijnen J,. Diagnostic value of systematic biopsy methods in the investigation of prostate cancer: A systematic review. J Urol 2006; 175 (5): 1605-1612.
39. Gann PH, Hennekens CH, Stampfer MJ,. A prospective evaluation of plasma prostate-specific antigen for detection of prostatic cancer. JAMA 1995; 273 (4): 289-294.
40. Jacobsen SJ, Bergstralh EJ, Guess HA, Katusic SK, Klee GG, Oesterling JE, Lieber MM,. Predictive properties of serum-prostate-specific antigen testing in a community-based setting. Arch Intern Med 1996; 156 (21): 2462-2468.
41. Mettlin CJ, Murphy GP, Babaian RJ, Chesley A, Kane RA, Littrup PJ, Mostofi FK, Ray PS, Somers WJ, Toi A,. Observations on the early detection of prostate cancer from the American Cancer Society National Prostate Cancer Detection Project. Cancer 1997; 80 (9): 1814-1817.
42. Schröder FH, van der Cruijsen-Koeter I, de Koning HJ, Vis AN, Hoedemaeker RF, Kranse R,. Prostate cancer detection at low prostate specific antigen. J Urol 2000; 163 (3): 806-812.
43. Thompson IM, Ankerst DP, Chi C, Lucia MS, Goodman PJ, Crowley JJ, Parnes HL, Coltman CA Jr., Operating characteristics of prostate-specific antigen in men with an initial PSA level of 3.0 ng/ml or lower. JAMA 2005; 294 (1): 66-70.
44. Okihara K, Cheli CD, Partin AW, Fritche HA, Chan DW, Sokoll LJ, Brawer MK, Schwartz MK, Vessella RL, Loughlin KR, Johnston DA, Babaian RJ,. Comparative analysis of complexed prostate specific antigen, free prostate specific antigen and their ratio in detecting prostate cancer. J Urol 2002; 167 (5): 2017-2023 discussion 2023-2014.
45. Partin AW, Brawer MK, Bartsch G, Horninger W, Taneja SS, Lepor H, Babaian R, Childs SJ, Stamey T, Fritsche HA, Sokoll L, Chan DW, Thiel RP, Cheli CD,. Complexed prostate specific antigen improves specificity for prostate cancer detection: Results of a prospective multicenter clinical trial. J Urol 2003; 170 (5): 1787-1791.
46. Farwell WR, Linder JA, Jha AK,. Trends in prostate-specific antigen testing from 1995 through 2004. Arch Intern Med 2007; 167 (22): 2497-2502.
47. Schröder FH, Hugosson J, Roobol MJ, Tammela TL, Ciatto S, Nelen V, Kwiatkowski M, Lujan M, Lilja H, Zappa M, Denis LJ, Recker F, Berenguer A, Maattanen L, Bangma CH, Aus G, Villers A, Rebillard X, van der Kwast T, Blijenberg BG, Moss SM, de Koning HJ, Auvinen A,. Screening and prostate-cancer mortality in a randomized European study. N Engl J Med 2009; 360 (13): 1320-1328.
48. Andriole GL, Crawford ED, Grubb RL III, Buys SS, Chia D, Church TR, Fouad MN, Gelmann EP, Kvale PA, Reding DJ, Weissfeld JL, Yokochi LA, O'Brien B, Clapp JD, Rathmell JM, Riley TL, Hayes RB, Kramer BS, Izmirlian G, Miller AB, Pinsky PF, Prorok PC, Gohagan JK, Berg CD,. Mortality results from a randomized prostate-cancer screening trial. N Engl J Med 2009; 360 (13): 1310-1319.
49. Djulbegovic M, Beyth RJ, Neuberger MM, Stoffs TL, Vieweg J, Djulbegovic B, Dahm P,. Screening for prostate cancer: Systematic review and meta-analysis of randomised controlled trials. Br Med J 2010; 341: c4543.
50. Draisma G, Boer R, Otto SJ, van der Cruijsen IW, Damhuis RA, Schroder FH, de Koning HJ,. Lead times and overdetection due to prostate-specific antigen screening: Estimates from the European Randomized Study of Screening for Prostate Cancer. J Natl Cancer Inst 2003; 95 (12): 868-878.
51. Thompson IM, Pauler DK, Goodman PJ, Tangen CM, Lucia MS, Parnes HL, Minasian LM, Ford LG, Lippman SM, Crawford ED, Crowley JJ, Coltman CA Jr., Prevalence of prostate cancer among men with a prostate-specific antigen level
52. Kefi A, Koseoglu H, Celebi I, Yorukoglu K, Esen A,. Relation between acute urinary retention, chronic prostatic inflammation and accompanying elevated prostate-specific antigen. Scand J Urol Nephrol 2006; 40 (2): 155-160.
53. Scattoni V, Raber M, Montorsi F, Da Pozzo L, Brausi M, Calori G, Freschi M, Rigatti P,. Percent of free serum prostate-specific antigen and histological findings in patients undergoing open prostatectomy for benign prostatic hyperplasia. Eur Urol 1999; 36 (6): 621-630.
54. Hoekx L, Jeuris W, Van Marck E, Wyndaele JJ,. Elevated serum prostate specific antigen (PSA) related to asymptomatic prostatic inflammation. Acta Urol Belg 1998; 66 (3): 1-2.
55. Haese A, de la Taille A, van Poppel H, Marberger M, Stenzl A, Mulders PF, Huland H, Abbou CC, Remzi M, Tinzl M, Feyerabend S, Stillebroer AB, van Gils MP, Schalken JA,. Clinical utility of the PCA3 urine assay in European men scheduled for repeat biopsy. Eur Urol 2008; 54 (5): 1081-1088.
56. Auprich M, Haese A, Walz J, Pummer K, de la Taille A, Graefen M, de Reijke T, Fisch M, Kil P, Gontero P, Irani J, Chun FK,. External validation of urinary pca3-based nomograms to individually predict prostate biopsy outcome. Eur Urol 2010; 58 (5): 727-732.
57. de la Taille A, Irani J, Graefen M, Chun F, de Reijke T, Kil P, Gontero P, Mottaz A, Haese A,. Clinical evaluation of the PCA3 assay in guiding initial biopsy decisions. J Urol 2011; 185 (6): 2119-2125.
58. Roobol MJ, Haese A, Bjartell A,. Tumour markers in prostate cancer III: Biomarkers in urine. Acta Oncol 2011; 50 (Suppl 1): 85-89.
59. Tsui NB, Ng EK, Lo YM,. Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin Chem 2002; 48 (10): 1647-1653.
60. Tomlins SA, Aubin SM, Siddiqui J, Lonigro RJ, Sefton-Miller L, Miick S, Williamsen S, Hodge P, Meinke J, Blase A, Penabella Y, Day JR, Varambally R, Han B, Wood D, Wang L, Sanda MG, Rubin MA, Rhodes DR, Hollenbeck B, Sakamoto K, Silberstein JL, Fradet Y, Amberson JB, Meyers S, Palanisamy N, Rittenhouse H, Wei JT, Groskopf J, Chinnaiyan AM,. Urine TMPRSS2:ERG fusion transcript stratifies prostate cancer risk in men with elevated serum PSA. Sci Transl Med 2011; 3 (94): 94ra72.
61. Zhang S, Pavlovitz B, Tull J, Wang Y, Deng FM, Fuller C,. Detection of TMPRSS2 gene deletions and translocations in carcinoma, intraepithelial neoplasia, and normal epithelium of the prostate by direct fluorescence in situ hybridization. Diagn Mol Pathol 2010; 19 (3): 151-156.
62. Clark JP, Cooper CS,. ETS gene fusions in prostate cancer. Nat Rev Urol 2009; 6 (8): 429-439.
63. Dong JT,. Prevalent mutations in prostate cancer. J Cell Biochem 2006; 97 (3): 433-447.
64. Silan F, Gultekin Y, Atik S, Kilinc D, Alan C, Yildiz F, Uludag A, Ozdemir O,. Combined point mutations in codon 12 and 13 of KRAS oncogene in prostate carcinomas. Mol Biol Rep 2011. Epub ahead of print.
65. Yi JM, Dhir M, Van Neste L, Downing SR, Jeschke J, Glockner SC, de Freitas Calmon M, Hooker CM, Funes JM, Boshoff C, Smits KM, van Engeland M, Weijenberg MP, Iacobuzio-Donahue CA, Herman JG, Schuebel KE, Baylin SB, Ahuja N,. Genomic and epigenomic integration identifies a prognostic signature in colon cancer. Clin Cancer Res 2011; 17 (6): 1535-1545.
66. Jerõnimo C, Varzim G, Henrique R, Oliveira J, Bento MJ, Silva C, Lopes C, Sidransky D,. I105V polymorphism and promoter methylation of the GSTP1 gene in prostate adenocarcinoma. Cancer Epidemiol Biomarkers Prev 2002; 11 (5): 445-450.
67. 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 2001; 159 (5): 1815-1826.
68. Yamanaka M, Watanabe M, Yamada Y, Takagi A, Murata T, Takahashi H, Suzuki H, Ito H, Tsukino H, Katoh T, Sugimura Y, Shiraishi T,. Altered methylation of multiple genes in carcinogenesis of the prostate. Int J Cancer 2003; 106 (3): 382-387.
69. Zhou M, Tokumaru Y, Sidransky D, Epstein JI,. Quantitative GSTP1 methylation levels correlate with Gleason grade and tumor volume in prostate needle biopsies. J Urol 2004; 171 (6 Pt 1): 2195-2198.
70. Bastian PJ, Yegnasubramanian S, Palapattu GS, Rogers CG, Lin X, De Marzo AM, Nelson WG,. Molecular biomarker in prostate cancer: The role of CpG island hypermethylation. Eur Urol 2004; 46 (6): 698-708.
71. Maruyama R, Toyooka S, Toyooka KO, Virmani AK, Zochbauer-Muller S, Farinas AJ, Minna JD, McConnell J, Frenkel EP, Gazdar AF,. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin Cancer Res 2002; 8 (2): 514-519.
72. Troyer DA, Lucia MS, de Bruine AP, Mendez-Meza R, Baldewijns MM, Dunscomb N, Van Engeland M, McAskill T, Bierau K, Louwagie J, Bigley JW,. Prostate cancer detected by methylated gene markers in histopathologically cancer-negative tissues from men with subsequent positive biopsies. Cancer Epidemiol Biomarkers Prev 2009; 18 (10): 2717-2722.
73. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria R: Foundation for Statistical Computing 2009.
74. Henrique R, Jeronimo C, Teixeira MR, Hoque MO, Carvalho AL, Pais I, Ribeiro FR, Oliveira J, Lopes C, Sidransky D,. Epigenetic heterogeneity of high-grade prostatic intraepithelial neoplasia: Clues for clonal progression in prostate carcinogenesis. Mol Cancer Res 2006; 4 (1): 1-8.
75. Jerõnimo C, Henrique R, Hoque MO, Mambo E, Ribeiro FR, Varzim G, Oliveira J, Teixeira MR, Lopes C, Sidransky D,. A quantitative promoter methylation profile of prostate cancer. Clin Cancer Res 2004; 10 (24): 8472-8478.
76. Nelson WG, De Marzo AM, Isaacs WB,. Prostate cancer. N Engl J Med 2003; 349 (4): 366-381.
77. Grover AC, Tangrea MA, Woodson KG, Wallis BS, Hanson JC, Chuaqui RF, Gillespie JW, Erickson HS, Bonner RF, Pohida TJ, Emmert-Buck MR, Libutti SK,. Tumor-associated endothelial cells display GSTP1 and RARbeta2 promoter methylation in human prostate cancer. J Transl Med 2006; 4: 13.
78. Hanson JA, Gillespie JW, Grover A, Tangrea MA, Chuaqui RF, Emmert-Buck MR, Tangrea JA, Libutti SK, Linehan WM, Woodson KG,. Gene promoter methylation in prostate tumor-associated stromal cells. J Natl Cancer Inst 2006; 98 (4): 255-261.
79. Rodriguez-Canales J, Hanson JC, Tangrea MA, Erickson HS, Albert PS, Wallis BS, Richardson AM, Pinto PA, Linehan WM, Gillespie JW, Merino MJ, Libutti SK, Woodson KG, Emmert-Buck MR, Chuaqui RF,. Identification of a unique epigenetic sub-microenvironment in prostate cancer. J Pathol 2007; 211 (4): 410-419.
80. Steiner I, Jung K, Schatz P, Horns T, Wittschieber D, Lein M, Dietel M, Erbersdobler A,. Gene promoter methylation and its potential relevance in early prostate cancer diagnosis. Pathobiology 2010; 77 (5): 260-266.
81. Bastian PJ, Palapattu GS, Lin X, Yegnasubramanian S, Mangold LA, Trock B, Eisenberger MA, Partin AW, Nelson WG,. Preoperative serum DNA GSTP1 CpG island hypermethylation and the risk of early prostate-specific antigen recurrence following radical prostatectomy. Clin Cancer Res 2005; 11 (11): 4037-4043.
82. Tokumaru Y, Harden SV, Sun DI, Yamashita K, Epstein JI, Sidransky D,. Optimal use of a panel of methylation markers with GSTP1 hypermethylation in the diagnosis of prostate adenocarcinoma. Clin Cancer Res 2004; 10 (16): 5518-5522.
83. Yegnasubramanian S, Kowalski J, Gonzalgo ML, Zahurak M, Piantadosi S, Walsh PC, Bova GS, De Marzo AM, Isaacs WB, Nelson WG,. Hypermethylation of CpG islands in primary and metastatic human prostate cancer. Cancer Res 2004; 64 (6): 1975-1986.
84. Kang GH, Lee S, Lee HJ, Hwang KS,. Aberrant CpG island hypermethylation of multiple genes in prostate cancer and prostatic intraepithelial neoplasia. J Pathol 2004; 202 (2): 233-240.
85. Cho NY, Kim BH, Choi M, Yoo EJ, Moon KC, Cho YM, Kim D, Kang GH,. Hypermethylation of CpG island loci and hypomethylation of LINE-1 and Alu repeats in prostate adenocarcinoma and their relationship to clinicopathological features. J Pathol 2007; 211 (3): 269-277.
86. Enokida H, Shiina H, Urakami S, Igawa M, Ogishima T, Li LC, Kawahara M, Nakagawa M, Kane CJ, Carroll PR, Dahiya R,. Multigene methylation analysis for detection and staging of prostate cancer. Clin Cancer Res 2005; 11 (18): 6582-6588.
87. Mehrotra J, Varde S, Wang H, Chiu H, Vargo J, Gray K, Nagle RB, Neri JR, Mazumder A,. Quantitative, spatial resolution of the epigenetic field effect in prostate cancer. Prostate 2008; 68 (2): 152-160.
88. Wu T, Giovannucci E, Welge J, Mallick P, Tang WY, Ho SM,. Measurement of GSTP1 promoter methylation in body fluids may complement PSA screening: A meta-analysis. Br J Cancer 2011; 105 (1): 65-73.
89. Thompson IM, Tangen CM, Ankerst DP, Chi C, Lucia MS, Goodman P, Parnes H, Coltman CA Jr., The performance of prostate specific antigen for predicting prostate cancer is maintained after a prior negative prostate biopsy. J Urol 2008; 180 (2): 544-547.
90. Remzi M, Fong YK, Dobrovits M, Anagnostou T, Seitz C, Waldert M, Harik M, Marihart S, Marberger M, Djavan B,. The Vienna nomogram: Validation of a novel biopsy strategy defining the optimal number of cores based on patient age and total prostate volume. J Urol 2005; 174 (4 Pt 1): 1256-1260 discussion 1260-1251; author reply 1261.
91. Singh H, Canto EI, Shariat SF, Kadmon D, Miles BJ, Wheeler TM, Slawin KM,. Predictors of prostate cancer after initial negative systematic 12 core biopsy. J Urol 2004; 171 (5): 1850-1854.
92. Kronz JD, Allan CH, Shaikh AA, Epstein JI,. Predicting cancer following a diagnosis of high-grade prostatic intraepithelial neoplasia on needle biopsy: Data on men with more than one follow-up biopsy. Am J Surg Pathol 2001; 25 (8): 1079-1085.
93. Eggener SE, Roehl KA, Catalona WJ,. Predictors of subsequent prostate cancer in men with a prostate specific antigen of 2.6 to 4.0 ng/ml and an initially negative biopsy. J Urol 2005; 174 (2): 500-504.
94. Rabets JC, Jones JS, Patel A, Zippe CD,. Prostate cancer detection with office based saturation biopsy in a repeat biopsy population. J Urol 2004; 172 (1): 94-97.
95. O'Dowd GJ, Miller MC, Orozco R, Veltri RW,. Analysis of repeated biopsy results within 1 year after a noncancer diagnosis. Urology 2000; 55 (4): 553-559.
96. Lopez-Corona E, Ohori M, Scardino PT, Reuter VE, Gonen M, Kattan MW,. A nomogram for predicting a positive repeat prostate biopsy in patients with a previous negative biopsy session. J Urol 2003; 170 (4 Pt 1): 1184-1188 discussion 1188.
97. Eilers T, Machtens S, Tezval H, Blaue C, Lichtinghagen R, Hagemann J, Jonas U, Serth J,. Prospective diagnostic efficiency of biopsy washing DNA GSTP1 island hypermethylation for detection of adenocarcinoma of the prostate. Prostate 2007; 67 (7): 757-763.
98. Henrique R, Ribeiro FR, Fonseca D, Hoque MO, Carvalho AL, Costa VL, Pinto M, Oliveira J, Teixeira MR, Sidransky D, Jeronimo C,. High promoter methylation levels of APC predict poor prognosis in sextant biopsies from prostate cancer patients. Clin Cancer Res 2007; 13 (20): 6122-6129.
99. Richiardi L, Fiano V, Vizzini L, De Marco L, Delsedime L, Akre O, Tos AG, Merletti F,. Promoter methylation in APC, RUNX3, and GSTP1 and mortality in prostate cancer patients. J Clin Oncol 2009; 27 (19): 3161-3168.
100. Rosenbaum E, Hoque MO, Cohen Y, Zahurak M, Eisenberger MA, Epstein JI, Partin AW, Sidransky D,. Promoter hypermethylation as an independent prognostic factor for relapse in patients with prostate cancer following radical prostatectomy. Clin Cancer Res 2005; 11 (23): 8321-8325.
101. Bastian PJ, Ellinger J, Heukamp LC, Kahl P, Muller SC, von Rucker A,. Prognostic value of CpG island hypermethylation at PTGS2, RAR-beta, EDNRB, and other gene loci in patients undergoing radical prostatectomy. Eur Urol 2007; 51 (3): 665-674 discussion 674.
102. Woodson K, Hanson J, Tangrea J,. A survey of gene-specific methylation in human prostate cancer among black and white men. Cancer Lett 2004; 205 (2): 181-188.
103. Macefield RC, Metcalfe C, Lane JA, Donovan JL, Avery KN, Blazeby JM, Down L, Neal DE, Hamdy FC, Vedhara K,. Impact of prostate cancer testing: An evaluation of the emotional consequences of a negative biopsy result. Br J Cancer 2010; 102 (9): 1335-1340.
104. Harden SV, Sanderson H, Goodman SN, Partin AA, Walsh PC, Epstein JI, Sidransky D,. Quantitative GSTP1 methylation and the detection of prostate adenocarcinoma in sextant biopsies. J Natl Cancer Inst 2003; 95 (21): 1634-1637.
105. Nakayama M, Gonzalgo ML, Yegnasubramanian S, Lin X, De Marzo AM, Nelson WG,. GSTP1 CpG island hypermethylation as a molecular biomarker for prostate cancer. J Cell Biochem 2004; 91 (3): 540-552.
106. Aubin SM, Reid J, Sarno MJ, Blase A, Aussie J, Rittenhouse H, Rittmaster R, Andriole GL, Groskopf J,. PCA3 molecular urine test for predicting repeat prostate biopsy outcome in populations at risk: Validation in the placebo arm of the dutasteride REDUCE trial. J Urol 2010; 184 (5): 1947-1952.
107. Marks LS, Fradet Y, Deras IL, Blase A, Mathis J, Aubin SM, Cancio AT, Desaulniers M, Ellis WJ, Rittenhouse H, Groskopf J,. PCA3 molecular urine assay for prostate cancer in men undergoing repeat biopsy. Urology 2007; 69 (3): 532-535.
108. Wolf AM, Wender RC, Etzioni RB, Thompson IM, D'Amico AV, Volk RJ, Brooks DD, Dash C, Guessous I, Andrews K, DeSantis C, Smith RA,. American Cancer Society guideline for the early detection of prostate cancer: Update 2010. CA Cancer J Clin 2010; 60 (2): 70-98.
109. Ablin RJ,. A retrospective and prospective overview of prostate-specific antigen. J Cancer Res Clin Oncol 1997; 123 (11-12): 583-594.
110. Greene KL, Albertsen PC, Babaian RJ, Carter HB, Gann PH, Han M, Kuban DA, Sartor AO, Stanford JL, Zietman A, Carroll P,. Prostate specific antigen best practice statement: 2009 update. J Urol 2009; 182 (5): 2232-2241.
111. Devaney J, Stirzaker C, Qu W, Song JZ, Statham AL, Patterson KI, Horvath LG, Tabor B, Coolen MW, Hulf T, Kench JG, Henshall SM, Pe Benito R, Haynes AM, Mayor R, Peinado MA, Sutherland RL, Clark SJ,. Epigenetic deregulation across chromosome 2q14.2 differentiates normal from prostate cancer and provides a regional panel of novel DNA methylation cancer biomarkers. Cancer Epidemiol Biomarkers Prev 2011; 20 (1): 148-159.
112. Zon G, Barker MA, Kaur P, Groshen S, Jones LW, Imam SA, Boyd VL,. Formamide as a denaturant for bisulfite conversion of genomic DNA: Bisulfite sequencing of the GSTPi and RARbeta2 genes of 43 formalin-fixed paraffin-embedded prostate cancer specimens. Anal Biochem 2009; 392 (2): 117-125.
113. Ahmed H, Cappello F, Rodolico V, Vasta GR,. Evidence of heavy methylation in the galectin 3 promoter in early stages of prostate adenocarcinoma: Development and validation of a methylated marker for early diagnosis of prostate cancer. Transl Oncol 2009; 2 (3): 146-156.
114. Perry AS, Loftus B, Moroose R, Lynch TH, Hollywood D, Watson RW, Woodson K, Lawler M,. In silico mining identifies IGFBP3 as a novel target of methylation in prostate cancer. Br J Cancer 2007; 96 (10): 1587-1594.
115. Vanaja DK, Ballman KV, Morlan BW, Cheville JC, Neumann RM, Lieber MM, Tindall DJ, Young CY,. PDLIM4 repression by hypermethylation as a potential biomarker for prostate cancer. Clin Cancer Res 2006; 12 (4): 1128-1136.
116. Yegnasubramanian S, Lin X, Haffner MC, DeMarzo AM, Nelson WG,. Combination of methylated-DNA precipitation and methylation-sensitive restriction enzymes (COMPARE-MS) for the rapid, sensitive and quantitative detection of DNA methylation. Nucleic Acids Res 2006; 34 (3): e19.
117. Bernardini S, Miano R, Iori R, Finazzi-Agro E, Palmieri G, Ballerini S, Angeloni C, Orlandi A, Bellincampi L, Cortese C, Federici G,. Hypermethylation of the CpG islands in the promoter region of the GSTP1 gene in prostate cancer: A useful diagnostic and prognostic marker? Clin Chim Acta 2004; 350 (1-2): 181-188.
118. Florl AR, Steinhoff C, Muller M, Seifert HH, Hader C, Engers R, Ackermann R, Schulz WA,. Coordinate hypermethylation at specific genes in prostate carcinoma precedes LINE-1 hypomethylation. Br J Cancer 2004; 91 (5): 985-994.
119. Woodson K, Hayes R, Wideroff L, Villaruz L, Tangrea J,. Hypermethylation of GSTP1, CD44, and E-cadherin genes in prostate cancer among US Blacks and Whites. Prostate 2003; 55 (3): 199-205.
120. Harden SV, Guo Z, Epstein JI, Sidransky D,. Quantitative GSTP1 methylation clearly distinguishes benign prostatic tissue and limited prostate adenocarcinoma. J Urol 2003; 169 (3): 1138-1142.
121. Nakayama M, Bennett CJ, Hicks JL, Epstein JI, Platz EA, Nelson WG, De Marzo AM,. Hypermethylation of the human glutathione S-transferase-pi gene (GSTP1) CpG island is present in a subset of proliferative inflammatory atrophy lesions but not in normal or hyperplastic epithelium of the prostate: A detailed study using laser-capture microdissection. Am J Pathol 2003; 163 (3): 923-933.
122. Chu DC, Chuang CK, Fu JB, Huang HS, Tseng CP, Sun CF,. The use of real-time quantitative polymerase chain reaction to detect hypermethylation of the CpG islands in the promoter region flanking the GSTP1 gene to diagnose prostate carcinoma. J Urol 2002; 167 (4): 1854-1858.
123. Goessl C, Muller M, Heicappell R, Krause H, Schostak M, Straub B, Miller K,. Methylation-specific PCR for detection of neoplastic DNA in biopsy washings. J Pathol 2002; 196 (3): 331-334.
124. Konishi N, Nakamura M, Kishi M, Nishimine M, Ishida E, Shimada K,. DNA hypermethylation status of multiple genes in prostate adenocarcinomas. Jpn J Cancer Res 2002; 93 (7): 767-773.
125. Jerõnimo 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 2001; 93 (22): 1747-1752.
126. 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 1998; 7 (6): 531-536.
127. 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 1997; 6 (6): 443-450.
128. 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 2000; 60 (21): 5941-5945.
129. Santourlidis S, Florl A, Ackermann R, Wirtz HC, Schulz WA,. High frequency of alterations in DNA methylation in adenocarcinoma of the prostate. Prostate 1999; 39 (3): 166-174.