Detection of DNA Hypermethylation as a Potential Biomarker for Prostate Cancer

Česká verzia

Authors: P. Tilandyová ¹; K. Kajo ¹; J. Kliment ²; L. Plank ¹; Z. Lasabová ³
Authors place of work: Ústav patologickej anatómie JLF UK a VNM, Martin, Slovenská republika ¹; Urologická klinika JLF UK a VNM, Martin, Slovenská republika ²; Ústav molekulovej biológie JLF UK a VNM, Martin, Slovenská republika ³
Published in the journal: Klin Onkol 2010; 23(5): 293-299
Category: Přehledy

Summary

Prostate cancer is one of the most common malignant diseases in men above the age of 50. A genetic predisposition and/ or acquired genetic and epigenetic changes together with lifestyle contribute to the development of the disease. The most studied epigenetic modification in prostate cancer is the methylation of the cytosine located within the dinucleotide CpG of promoter regions of different genes by methylation specific PCR. The evidence of gene silencing by DNA methylation in genes like GSTP1, APC or RASF1 is a common and relatively specific event in prostate cancer. DNA methylation testing can be performed on tissue samples or urine, ejaculate or serum. Translational research is searching for new biomarkers for early detection and prognosis of prostate cancer, but because of large methodological differences in applied techniques and patient cohorts, the investigations have yielded promising, but also some controversial results. More prospective randomized trials and standardized methods are needed to assess the true value of methylation for the diagnosis and prognosis of prostate cancer.

Key words:
prostate cancer – biomarkery – DNA methylation – CpG islands – PCR

Zdroje

1. Incidencia zhubných nádorov v Slovenskej republike 2003. Bratislava: NCZI 2006: 31.

2. Partin AW, Kattan MW, Subong EN et al. Combination of prostate‑ specific antigen, clinical stage, and Gleason score to predict pathological stage of localized prostate cancer. A multi‑institutional update. JAMA 1997; 277(18): 1445– 1451.

3. Ondruš D. Karcinóm prostaty – Epidemiológia, Etiológia, Diagnostika, Klinické prejavy. Skríning. Onkológia 2006; 1(1): 14– 18.

4. Kajo K. Bioptické vyšetrenie prostaty I. Punkčná biopsia, transuretrálna resekcia a radikálna prostatektómia. Klin Urol 2005; 1(1): 8– 11.

5. Kajo K, Macháleková K. Bioptické vyšetrenie prostaty II. Histomorfologické ukazovatele pri karcinóme prostaty. Klin Urol 2005; 1(1): 13– 17.

6. Liska J, Repiska V, Galbavy S et al. Prostate tumours – histological classification and molecular aspects of prostate tumorigenesis. Endocr Regul 2007; 41(1): 45– 57.

7. Roberts WW, Bergstralh EJ, Blute ML et al. Contemporary identification of patients at high risk of early prostate cancer recurrence after radical retropubic prostatectomy. Urology 2001; 57(6): 1033– 1037.

8. Kajo K, Macháleková K, Tilandyová P et al. Molekulová patológia karcinómu prostaty (1. časť). Onkológia 2009; 4(3): 178– 180.

9. Hughes C, Murphy A, Martin C et al. Molecular pathology of prostate cancer. J Clin Pathol 2005; 58(7): 673– 684.

10. FitzGerald LM, Patterson B, Thomson R et al. Indetification of a prostate cancer susceptibility gene on chromosome 5p13q12 associated with risk of both familial and sporadic disease. Eur J Hum Genet 2009; 17(3): 368– 377.

11. Sivonova M, Waczulikova I, Dobrota D et al. Polymorphisms of glutathione‑ S‑ trasnferase M1, T1, P1 and the risk of prostate cancer: a case‑ control study. J Exp Clin Res 2009; 28: 32.

12. Perry AS, Foley R, Woodson K et al. The emerging roles of DNA methylation in the clinical management of prostate cancer. Endocr Relat Cancer 2006; 13(2): 357– 377.

13. Seligson DB, Horvath S, Shi T et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 2005; 435(7046): 1262– 1266.

14. Baylin S, Bestor TH. Altered methylation patterns in cancer cell genomes: cause or consequence? Cancer Cell 2002; 1(4): 299– 305.

15. Kurdistani SK. Histone modification as markers of cancer prognosis: a cellular view. Br J Cancer 2007; 97(1): 1– 5.

16. Das PM, Singal R. DNA methylation and cancer. J Clin Oncol 2004; 22(22): 4632– 4642.

17. Merlo A, Herman JG, Mao L et al. 5’CpG island methylation is associated with transcirptional silencing of the tumor suppressor gene p16/ CDKN2/ MTS1 in human cancers. Nat Med 1995; 1(7): 686– 692.

18. Fraga MF, Esteller M. DNA methylation: a profile of methods and applications. Biotechniques 2002; 33(3): 632– 649.

19. Shames DS, Minna JD, Gazdar AF. Methods for detecting DNA methylation in tumors: from bench to bedside. Cancer Lett 2007; 251(2): 187– 198.

20. Frommer M, McDonald LE, Millar DS et al. A genomic sequencing protocol that yields a positive display of 5– methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 1992; 89(5): 1827– 1831.

21. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 1997; 25(12): 2532– 2534.

22. Herman JG, Graff JR, Myöhänen S et al. Methylation‑ specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996; 93(18): 9821– 9826.

23. Ho SM, Tang WY. Techniques used in studies of epigenome dysregulation due to abberant DNA methylation: an emphasis on fetal‑based adult diseases. Reprod Toxicol 2007; 23(3): 267– 282.

24. Colella S, Shen L, Baggerly KA et al. Sensitive and quantitative universal Pyrosequencing methylation analysis of CpG sites. Biotechniques 2003; 35(1): 146– 150.

25. Tost J, El Abdalaoui H, Gut IG. Serial pyrosequencing for quantitative DNA methylation analysis. Biotechniques 2006; 40(6): 721– 722.

26. Ehrich M, Nelson MR, Stanssens P et al. Quantitative high‑throughput analysis of DNA methylation patterns by base‑ specific cleavage and mass spectrometry. Proc Natl Acad Sci USA 2005; 102(44): 15785– 15790.

27. House MG, Guo M, Efron DT et al. Tumor suppressor gene hypermethylation as a predictor of gastric stromal tumor behaviour. J Gastrointest Surg 2003; 7(8): 1004– 1014.

28. Bian YS, Yan P, Osterheld MC et al. Promoter methylation analysis on microdissected paraffin‑embedded tissues using bisulfite treatment and PCR‑ SSCP. Biotechniques 2001; 30(1): 66– 72.

29. Eads CA, Danenberg KD, Kawakami K et al. MethyLight: a high‑throughput assay to measure DNA methylation. Nucleic Acids Res 2000; 28(8): E32.

30. Swift‑ Scanlan T, Blackford A, Argani P et al. Two‑ color quantitative multiplex methylation‑ specific PCR. Biotechniques 2006; 40(2): 210– 219.

31. Lee WH, Morton RA, Epstein JI et al. 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.

32. Nakayama M, Bennett CJ, Hicks JL et al. Hypermethylation of the human glutathione S‑ transferase‑ pi gene (GSTP1) CpG island is present in a subset of proliferative infammatory 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.

33. Brooks JD, Weinstein M, Lin X et al. CG Island methylation changes near the GSTP1 gene in prostatic intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev 1998; 7(6): 531– 536.

34. Maruyama R, Toyooka S, Toyooka KO et al. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin Cancer Res 2002; 8(2): 514– 519.

35. Woodson K, Gillespie J, Hanson J et al. Heterogeneous gene methylation patterns among pre‑invasive and cancerous lesions of the prostate: a histopathologic study of whole mount prostate specimens. Prostate 2004; 60(1): 25– 31.

36. Jerónimo C, Usadel H, Henrique R et al. Quantitation of GSTP1 methylation in non‑neoplastic prostatic tissue and organ‑ confined prostate adenocarcinoma. J Natl Cancer Inst 2001; 93(22): 1747– 1752.

37. Harden SV, Sanderson H, Goodman SN et al. Quantitative GSTP1 methylation and the detection of prostate adenocarcinoma in sextant biopsies. J Natl Cancer Inst 2003; 95(21): 1634– 1637.

38. Meiers I, Shanks JH, Bostwick DG. Glutathione S‑ transferase pi (GSTP1) hypermethylation in prostate cancer: review 2007. Pathology 2007; 39(3): 299– 304.

39. Jerónimo C, Henrique R, Hoque MO et al. A quantitative promoter methylation profile of prostate cancer. Clin Cancer Res 2004; 10(24): 8472– 8478.

40. Yegnasubramanian S, Kowalski J, Gonzalgo ML et al. Hypermethylation of CpG islands in primary and metastatic human prostate cancer. Cancer Res 2004; 64(6): 1975– 1986.

41. Enokida H, Shiina H, Igawa M et al. CpG hypermethylation of MDR1 gene contributes to the pathogenesis and progression of human prostate cancer. Cancer Res 2004; 64(17): 5956– 5962.

42. Sasaki M, Tanaka Y, Perinchery G et al. Methylation and inactivation of estrogen, progesterone, and androgen receptors in prostate cancer. J Natl Cancer Inst 2002; 94(5): 384– 390.

43. Zhu X, Leav I, Leung YK et al. Dynamic regulation of estrogen receptor‑beta expression by DNA methylation during prostate cancer development and metastasis. Am J Pathol 2004; 164(6): 2003– 2012.

44. Jerónimo C, Henrique R, Hoque MO et al. Quantitative RARbeta2 hypermethylation: a promising prostate cancer marker. Clin Cancer Res 2004; 10(12 Pt 1): 4010– 4014.

45. Zhang J, Liu L, Pfeifer GP. Methylation of the retinoid response gene TIG1 in prostate cancer correlates with methylation of the retinoic acid receptor beta gene. Oncogene 2004; 23(12): 2241– 2249.

46. Kito H, Suzuki H, Ichikawa T et al. Hypermethylation of the CD44 gene is associated with progression and metastasis of human prostate cancer. Prostate 2001; 49(2): 110– 115.

47. Kang GH, Lee S, Lee HJ et al. Aberrant CpG island hypermethylation of multiple genes in prostate cancer and prostatic intraepithelial neoplasia. J Pathol 2004; 202(2): 233– 240.

48. Vanaja DK, Cheville JC, Iturria SJ et al. Transcriptional silencing of zinc finger protein 185 identified by expression profiling is associated with prostate cancer progression. Cancer Res 2003; 63(14): 3877– 3882.

49. Yamada Y, Toyota M, Hirokawa Y et al. Identification of diferentially methylated CpG islands in prostate cancer. Int J Cancer 2004; 112(5): 840– 845.

50. Jerónimo C, Henrique R, Oliveira J et al. Abberant cellular retinol binding protein 1 (CRBP1) gene expression and promoter methylation in prostate cacner. J Clin Pathol 2004; 57(8): 872– 876.

51. Murphy TM, Perry AS, Lawler M. The emergence of DNA methylation as a key modulator of aberrant cell death in prostate cancer. Endocr Relat Cancer 2008; 15(1): 11– 25.

52. Chung W, Kwabi‑ Addo B, Ittmann M et al. Identification of novel tumor markers in prostate, colon and breast cancer by unbiased methylation profiling. PLoS One 2008; 30(4): e2079.

53. Perry AS, Loftus B, Moroose R et al. In silico mining identifies IGFBP3 as a novel target of methylation in prostate cancer. Cancer 2007; 96(10): 1587– 1594.

54. Esteller M, Corn PG, Baylin SB et al. A gene hypermethylation profile of human cancer. Cancer Res 2001; 61(8): 3225– 3229.

55. Jerónimo C, Henrique R, Hoque MO et al. Quantitative RARbeta2 hypermethylation: a promising prostate cancer marker. Clin Cancer Res 2004; 10(12 Pt 1): 4010– 4014.

56. Tokumaru Y, Harden SV, Sun DI et al. 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.

57. Yamanaka M, Watanabe M, Yamada Y et al. Altered methylation of multiple genes in carcinogenesis of the prostate. Int J Cancer 2003; 106(3): 382– 387.

58. Henrique R, Ribeiro FR, Fonseca D et al. High promoter methylation levels of APC predict poor prognosis in sextant biopises from prostate cancer patients. Clin Cancer Res 2007; 13(20): 6122– 6129.

59. Sørensen KD, Borre M, Ørntof TF et al. Chromosomal deletion, promoter hypermethylation and downregulation of FYN in prostate cancer. Int J Cancer 2008; 122(3): 509– 519.

60. Bastian PJ, Ellinger J, Heukamp LC et al. Prognostic value of CpG island hypermethylation at PTGS2, RAR‑beta, EDNRB, and other gene loci in patients undergoing radical prostatectomy. Urology 2007; 51(3): 665– 674.

61. Woodson K, O’Reilly KJ, Ward DE et al. CD44 and PTGS2 methylation are independent prognostic markers for biochemical recurrence among prostate cancer patients with clinically localized disease. Epigenetics 2006; 1(4): 183– 186.

62. Ellinger J, Bastian PJ, Jurgan T et al. CpG island hypermethylation at multiple gene sites in diagnosis and prognosis of prostate cancer. Urology 2008; 71(1): 161– 167.

63. Cho NY, Kim JH, Moon KC et al. Genomic hypomethylation and CpG island hypermethylation in prostatic intraepitehelial neoplasm. Virchows Arch 2009; 454(1): 17– 23.

64. Cottrell S, Jung K, Kristiansen G et al. Discovery and validation of 3 novel DNA methylation markers of prostate cancer prognosis. Urology 2007: 177(5): 1753– 1758.

65. Liu JW, Nagpal JK, Jeronimo C et al. Hypermethylation of MCAM gene is associated with advanced tumor stage in prostate cancer. Prostate 2008; 68(4): 418– 26.

66. Higuchi T, Nakamura M, Shimada K et al. HRK inactivation associated with promoter methylation and LOH in prostate cancer. Prostate 2008; 68(1): 105– 113.

67. Shah JN, Shao G, Hei TK et al. Methylation screening of the TGFBI promoter in human lung and prostate cancer by methylation‑ specific PCR. BMC Cancer 2008; 8: 284.

68. Guan M, Xu C, Zhang F et al. Aberrant methylation of EphA7 in human prostate cancer and its relation to clinicopathological features. Int J Cancer 2009; 124(1): 88– 94.

69. Liu JW, Nagpal JK, Sun W et al. ssDNA‑binding protein 2 is frequently hypermethylated and suppresses cell growth in human prostate cancer. Clin Cancer Res 2008; 14(12): 3754– 3760.

70. Weiss G, Cottrell S, Distler J et al. DNA methylation of the PITX2 gene promote region is strong independent prognostic marker of biochemical recurrence in patients with prostate cancer after radical prostatectomy. J Urol 2009; 181(4): 1678– 1685.

71. Jerónimo C, Usadel H, Henrique R et al. Quantitative GSTP1 hypermethylation in bodily fluids of patients with prostate cancer. Urology 2002; 60(6): 1131– 1135.

72. Goessl C, Müller M, Heicappell R et al. DNA‑based detection of prostate cancer in blood, urine, and ejaculates. Ann N Y Acad Sci 2001; 945: 51– 58.

73. Reibenwein J, Pils D, Horak P et al. Promoter hypermethylation of GSTP1, AR, and 14- 3- 3sigma in serum of prostate cancer patients and its clinical relevance. Prostate 2007; 67(4): 427– 432.

74. Ellinger J, Haan K, Heukamp LC et al. CpG island hypermethylation in cell‑free serum DNA identifies patients with localized prostate cancer. Prostate 2008; 68(1): 42– 49.

75. Goessl C, Krause H, Müller M et al. Fluorescent methylation‑ specific polymerase chain reaction for DNA‑based detection of prostate cancer in bodily fluids. Cancer Res 2000; 60(21): 5941– 5945.

76. Rouprêt M, Hupertan V, Catto JW et al. Promoter hypermethylation in circulating blood cells identifies prostate cancer progression. Int J Cancer 2008; 122(4): 952– 956.

77. Gonzalgo ML, Pavlovich CP, Lee SM et al. Prostate cancer detection by GSTP1 methylation analysis of postbiopsy urine specimens. Clin Cancer Res 2003; 9(7): 2673– 2677.

78. Bastian PJ, Palapattu GS, Yegnasubramanian S et al. CpG island hypermethylation profile in the serum of men with clinically localized and hormone refractory metastatic prostate cancer. Urology 2008; 179(2): 529– 534.

79. Woodson K, O’Reilly KJ, Hanson JC et al. The usefulness of the detection of GSTP1 methylation in urine as a biomarker in the diagnosis of prostate cancer. Urology 2008; 179(2): 508– 511.

80. Vener T, Derecho C, Baden J et al. Development of a multiplexed urine assay for prostate cancer diagnosis. Clin Chem 2009; 54(5): 874– 882.

81. Hoque MO, Topaloglu O, Begum S et al. Quantitative methylation‑ specific polymerase chain reaction gene patterns in urine sediment distinguish prostate cancer patients from control subjects. J Clin Oncol 2005; 23(27): 6569– 6575.

82. Duffy MJ, Napieralski R, Martens JW et al. Methylated genes as new cancer biomarkers. Eur J Cancer 2009; 45(3): 335– 346.

83. Pepe MS, Feng Z, Janes H et al. Pivotal evaluation of the accuracy of a biomarker used for classification ore prediction: standards for study design. J Natl Cancer Inst 2008; 100(20): 1432– 1438.