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CpG Island Hypermethylation Changes during Prostate Cancer Progression and Metastasis

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DNA Methylation, Epigenetics and Metastasis

Part of the book series: Cancer Metastasis — Biology and Treatment ((CMBT,volume 7))

Abstract

Recent studies have implicated the dysregulation or maladaptation of epigenetic mechanisms to be a central feature of prostate carcinogenesis. Hypermethylation of CpG islands (CGI), clusters of CpG dinucleotides frequently found at gene regulatory regions, has been demonstrated to be one of the most frequent somatic genome alterations associated with prostate carcinogenesis. A few recent studies have explored the role of CGI hypermethylation during prostate cancer progression from the early precursor lesions to distant metastases. This chapter will focus on the time course of CGI hypermethylation changes that occur at each step during the development and progression of prostate cancer in an effort to understand how these epigenetic changes contribute to the formation of prostate cancer metastases. We will begin by giving an overview of the epidemiology, natural progression, and pathogenesis of prostate cancer, then detail the CGI hypermethylation changes that occur at each step along the progression, then postulate the molecular mechanisms that may be involved in generating and propagating these changes, and finally, use the pattern and timing of DNA methylation changes during the natural progression of prostate cancer to derive models that describe how prostate cancer metastases may form.

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References

  1. Jemal A., Tiwari R. C., Murray T., Ghafoor A., Samuels A., Ward E., Feuer E. J. and Thun M. J. Cancer statistics, 2004. CA Cancer J Clin, 2004; 54: 8–29.

    PubMed  Google Scholar 

  2. Sakr W. A., Grignon D. J., Crissman J. D., Heilbrun L. K., Cassin B. J., Pontes J. J. and Haas G. P. High grade prostatic intraepithelial neoplasia (HGPIN) and prostatic adenocarcinoma between the ages of 20–69: an autopsy study of 249 cases. In Vivo, 1994; 8: 439–443.

    Google Scholar 

  3. Etzioni R., Penson D. F., Legler J. M., di Tommaso D., Boer R., Gann P. H. and Feuer E. J. Overdiagnosis due to prostate-specific antigen screening: lessons from U.S. prostate cancer incidence trends. J Natl Cancer Inst, 2002; 94: 981–990.

    PubMed  Google Scholar 

  4. Platz E. A. and De Marzo A. M. Epidemiology of inflammation and prostate cancer. J Urol, 2004; 171: S36–40.

    Article  PubMed  Google Scholar 

  5. De Marzo A. M., Marchi V. L., Epstein J. I. and Nelson W. G. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol, 1999; 155: 1985–1992.

    PubMed  Google Scholar 

  6. Putzi M. J. and De Marzo A. M. Morphologic transitions between proliferative inflammatory atrophy and high-grade prostatic intraepithelial neoplasia. Urology, 2000; 56: 828–832.

    Article  PubMed  Google Scholar 

  7. Zha S., Gage W. R., Sauvageot J., Saria E. A., Putzi M. J., Ewing C. M., Faith D. A., Nelson W. G., De Marzo A. M. and Isaacs W. B. Cyclooxygenase-2 is up-regulated in proliferative inflammatory atrophy of the prostate, but not in prostate carcinoma. Cancer Res, 2001; 61: 8617–8623.

    Google Scholar 

  8. Parsons J. K., Nelson C. P., Gage W. R., Nelson W. G., Kensler T. W. and De Marzo A. M. GSTA1 expression in normal, preneoplastic, and neoplastic human prostate tissue. Prostate, 2001; 49: 30–37.

    Article  PubMed  Google Scholar 

  9. Nelson W. G., Carter H. B., DeWeese T. L., Bajaj G., Thompson T. L. and Eisenberger M. A. Prostate Cancer. In: M. D. Abeloff (ed.), Clinical Oncology, 2004; 3rd edition, pp. 2085–2148. Philadelphia, Pa.: Elsevier Churchill Livingstone.

    Google Scholar 

  10. Partin A. W., Kattan M. W., Subong E. N., Walsh P. C., Wojno K. J., Oesterling J. E., Scardino P. T. and Pearson J. D. 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: 1445–1451.

    Article  PubMed  Google Scholar 

  11. Han M., Partin A. W., Zahurak M., Piantadosi S., Epstein J. I. and Walsh P. C. Biochemical (prostate specific antigen) recurrence probability following radical prostatectomy for clinically localized prostate cancer. J Urol, 2003; 169: 517–523.

    Article  PubMed  Google Scholar 

  12. D'Amico A. V., Whittington R., Malkowicz S. B., Weinstein M., Tomaszewski J. E., Schultz D., Rhude M., Rocha S., Wein A. and Richie J. P. Predicting prostate specific antigen outcome preoperatively in the prostate specific antigen era. J Urol, 2001; 166:2185–2188.

    Article  PubMed  Google Scholar 

  13. Fleming I. D. American Joint Committee on Cancer., American Cancer Society., and American College of Surgeons. AJCC cancer staging manual, 1997; 5th ed / edition, p. xv, 294 p. Philadelphia: Lippincott-Raven.

    Google Scholar 

  14. Hermanek P., Sobin L. H. and International Union against Cancer. TNM classification of malignant tumours, 1992; 4th edition, p. xiii, 217 p. Berlin; New York: Springer-Verlag.

    Google Scholar 

  15. Greene F. L., American Joint Committee on Cancer., and American Cancer Society. AJCC cancer staging manual, 2002; 6th edition, p. xiv, 421 p. New York: Springer-Verlag.

    Google Scholar 

  16. Allsbrook W. C., Jr., Mangold K. A., Johnson M. H., Lane R. B., Lane C. G., Amin M. B., Bostwick D. G., Humphrey P. A., Jones E. C., Reuter V. E., Sakr W., Sesterhenn I. A., Troncoso P., Wheeler T. M. and Epstein J. I. Interobserver reproducibility of Gleason grading of prostatic carcinoma: urologic pathologists. Hum Pathol, 2001; 32:74–80.

    Article  PubMed  Google Scholar 

  17. Allsbrook W. C., Jr., Mangold K. A., Johnson M. H., Lane R. B., Lane C. G. and Epstein J. I. Interobserver reproducibility of Gleason grading of prostatic carcinoma: general pathologist. Hum Pathol, 2001; 32: 81–88.

    Article  PubMed  Google Scholar 

  18. Kronz J. D., Silberman M. A., Allsbrook W. C., Jr., Bastacky S. I., Burks R. T., Cina S. J., Mills S. E., Ross J. S., Sakr W. A., Tomaszewski J. E., True L. D., Ulbright T. M., Weinstein M. W., Yantiss R. K., Young R. H. and Epstein J. I. Pathology residents’ use of a Web-based tutorial to improve Gleason grading of prostate carcinoma on needle biopsies. Hum Pathol, 2000; 31: 1044–1050.

    Article  PubMed  Google Scholar 

  19. Kronz J. D., Silberman M. A., Allsbrook W. C. and Epstein J. I. A web-based tutorial improves practicing pathologists’ Gleason grading of images of prostate carcinoma specimens obtained by needle biopsy: validation of a new medical education paradigm. Cancer, 2000; 89: 1818–1823.

    Article  PubMed  Google Scholar 

  20. Bubendorf L., Schopfer A., Wagner U., Sauter G., Moch H., Willi N., Gasser T. C. and Mihatsch M. J. Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol, 2000; 31: 578–583.

    Article  PubMed  Google Scholar 

  21. Rubin M. A., Putzi M., Mucci N., Smith D. C., Wojno K., Korenchuk S. and Pienta K. J. Rapid (“warm”) autopsy study for procurement of metastatic prostate cancer. Clin Cancer Res, 2000; 6: 1038–1045.

    PubMed  Google Scholar 

  22. Nelson W. G., De Marzo A. M. and Isaacs W. B. Prostate cancer. N Engl J Med, 2003;349: 366–381.

    Article  PubMed  Google Scholar 

  23. Meeker A. K., Gage W. R., Hicks J. L., Simon I., Coffman J. R., Platz E. A., March G. E. and De Marzo A. M. Telomere length assessment in human archival tissues: combined telomere fluorescence in situ hybridization and immunostaining. Am J Pathol, 2002; 160: 1259–1268.

    PubMed  Google Scholar 

  24. Meeker A. K., Hicks J. L., Platz E. A., March G. E., Bennett C. J., Delannoy M. J. and De Marzo A. M. Telomere shortening is an early somatic DNA alteration in human prostate tumorigenesis. Cancer Res, 2002; 62: 6405–6409.

    PubMed  Google Scholar 

  25. Bieberich C. J., Fujita K., He W. W. and Jay G. Prostate-specific and androgen-dependent expression of a novel homeobox gene. J Biol Chem, 1996; 271: 31779–31782.

    Article  PubMed  Google Scholar 

  26. Bhatia-Gaur R., Donjacour A. A., Sciavolino P. J., Kim M., Desai N., Young P., Norton C. R., Gridley T., Cardiff R. D., Cunha G. R., Abate-Shen C. and Shen M. M. Roles for Nkx3.1 in prostate development and cancer. Genes Dev, 1999; 13: 966–977.

    PubMed  Google Scholar 

  27. He W. W., Sciavolino P. J., Wing J., Augustus M., Hudson P., Meissner P. S., Curtis R. T., Shell B. K., Bostwick D. G., Tindal, D. J., Gelmann E. P., Abate-Shen C. and Carter K. C. A novel human prostate-specific, androgen-regulated homeobox gene (NKX3.1) that maps to 8p21, a region frequently deleted in prostate cancer. Genomics, 1997; 43:69–77.

    Article  PubMed  Google Scholar 

  28. Ornstein D. K., Cinquanta M., Weiler S., Duray P. H., Emmert-Buck M. R., Vocke C. D., Linehan W. M. and Ferretti J. A. Expression studies and mutational analysis of the androgen regulated homeobox gene NKX3.1 in benign and malignant prostate epithelium. J Urol, 2011; 165: 1329–1334.

    Google Scholar 

  29. Bowen C., Bubendorf L., Voeller H. J., Slack R., Willi N., Sauter G., Gasser T. C., Koivisto P., Lack E. E., Kononen J., Kallioniemi O. P. and Gelmann E. P. Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res, 2000; 60: 6111–6115.

    PubMed  Google Scholar 

  30. Wu X., Senechal K., Neshat M. S., Whang Y. E. and Sawyer, C. L. The PTEN/MMAC1 tumor suppressor phosphatase functions as a negative regulator of the phosphoinositide 3-kinase/Akt pathway. Proc Natl Acad Sci U S A, 1998; 95: 15587–15591.

    Article  PubMed  Google Scholar 

  31. Myers M. P., Stolarov J. P., Eng C., Li J., Wang S. I., Wigler M. H., Parsons R. and Tonks N. K. P-TEN, the tumor suppressor from human chromosome 10q23, is a dualspecificity phosphatase. Proc Natl Acad Sci U S A, 1997; 94: 9052–9057.

    Article  PubMed  Google Scholar 

  32. Myers M. P., Pass I., Batty I. H., Van der Kaay J., Stolarov J. P., Hemmings B. A., Wigler M. H., Downes C. P. and Tonks N. K. The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc Natl Acad Sci U S A, 1998; 95: 13513–13518.

    Article  PubMed  Google Scholar 

  33. Ramaswamy S., Nakamura N., Vazquez F., Batt D. B., Perera S., Roberts T. M. and Sellers W. R. Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci U S A, 1999; 96: 2110–2115.

    Article  PubMed  Google Scholar 

  34. Sun H., Lesche R., Li D. M., Liliental J., Zhang H., Gao J., Gavrilova N., Mueller B., Liu X. and Wu H. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci U S A, 1999; 96: 6199–6204.

    Article  PubMed  Google Scholar 

  35. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S. I., Puc J., Miliaresis C., Rodgers L., McCombie R., Bigner S. H., Giovanella B. C., Ittmann M., Tycko B., Hibshoosh H., Wigler M. H. and Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science, 1997;275: 1943–1947.

    Article  PubMed  Google Scholar 

  36. McMenamin M. E., Soung P., Perera S., Kaplan I., Loda M.. and Sellers W. R. Loss of PTEN expression in paraffin-embedded primary prostate cancer correlates with high Gleason score and advanced stage. Cancer Res, 1999; 59: 4291–4296.

    PubMed  Google Scholar 

  37. Suzuki H., Freije D., Nusskern D. R., Okami K., Cairns P., Sidransky D., Isaacs W. B., and Bova, G. S. Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res, 1998; 58: 204–209.

    PubMed  Google Scholar 

  38. Shi X. B., Ma A. H., Xia L., Kung H. J. and de Vere White, R. W. Functional analysis of 44 mutant androgen receptors from human prostate cancer. Cancer Res, 2002;62:1496–1502.

    PubMed  Google Scholar 

  39. Marcelli M., Ittmann M., Mariani S., Sutherland R., Nigam R., Murthy L., Zhao Y., DiConcini D., Puxeddu E., Esen A., Eastham J., Weigel N. L. and Lamb D. J. Androgen receptor mutations in prostate cancer. Cancer Res, 2000; 60: 944–949.

    PubMed  Google Scholar 

  40. Visakorpi T., Hyytinen E., Koivisto P., Tanner M., Keinanen R., Palmberg C., Palotie A., Tammela T., Isola J. and Kallioniemi O. P. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet, 1995; 9: 401–406.

    Article  PubMed  Google Scholar 

  41. Veldscholte J., Ris-Stalpers C., Kuiper G. G., Jenster G., Berrevoets C., Claassen E., van Rooij H. C., Trapman J., Brinkmann A. O. and Mulder E. A mutation in the ligand binding domain of the androgen receptor of human LNCaP cells affects steroid binding characteristics and response to anti-androgens. Biochem Biophys Res Commun, 1990;173: 534–540.

    PubMed  Google Scholar 

  42. Laufer M., Denmeade S. R., Sinibaldi V. J., Carducci M. A. and Eisenberger M. A. Complete androgen blockade for prostate cancer: what went wrong? J Urol, 2000; 164:3–9.

    Article  PubMed  Google Scholar 

  43. Koivisto P., Kononen J., Palmberg C., Tammela T., Hyytinen E., Isola J., Trapman J., Cleutjens K., Noordzij A., Visakorpi T. and Kallioniemi O. P. Androgen receptor gene amplification: a possible molecular mechanism for androgen deprivation therapy failure in prostate cancer. Cancer Res, 1997; 57: 314–319.

    PubMed  Google Scholar 

  44. Taplin M. E., Bubley G. J., Shuster T. D., Frantz M. E., Spooner A. E., Ogata G. K., Keer H. N. and Balk S. P. Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer. N Engl J Med, 1995; 332: 1393–1398.

    Article  PubMed  Google Scholar 

  45. Culig Z., Hobisch A., Cronauer M. V., Cato A. C., Hittmair A., Radmayr C., Eberle J., Bartsch G., and Klocker H. Mutant androgen receptor detected in an advanced-stage prostatic carcinoma is activated by adrenal androgens and progesterone. Mol Endocrinol, 1993; 7: 1541–1550.

    Article  PubMed  Google Scholar 

  46. Craft N., Shostak Y., Carey M., and Sawyers C. L. A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat Med, 1999; 5: 280–285.

    Article  PubMed  Google Scholar 

  47. Nazareth L. V. and Weigel N. L. Activation of the human androgen receptor through a protein kinase A signaling pathway. J Biol Chem, 1996; 271: 19900–19907.

    PubMed  Google Scholar 

  48. Cheville J. C., Tindall D., Boelter C., Jenkins R., Lohse C. M., Pankratz V. S., Sebo T. J., Davis B. and Blute M. L. Metastatic prostate carcinoma to bone: clinical and pathologic features associated with cancer-specific survival. Cancer, 2002; 95: 1028–1036.

    PubMed  Google Scholar 

  49. Lee W. H., Morton R. A., Epstein J. I., Brooks J. D., Campbell P. A., Bova G. S., Hsieh W. S., Isaacs W. B. and Nelson W. G. Cytidine methylation of regulatory sequences near the pi-class glutathione S-transferase gene accompanies human prostatic carcinogenesis. Proc Natl Acad Sci U S A, 1994; 91: 11733–11737.

    PubMed  Google Scholar 

  50. Lee W. H., Isaacs W. B., Bova G. S., and Nelson W. G. 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; 6:443–450.

    PubMed  Google Scholar 

  51. Henderson C. J., Smith A. G., Ure J., Brown K., Bacon E. J. and Wolf C. R. Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc Natl Acad Sci U S A, 1998; 95: 5275–5280.

    Article  PubMed  Google Scholar 

  52. Nelson C. P., Kidd, L. C., Sauvageot, J., Isaacs, W. B., De Marzo, A. M., Groopman, J. D., Nelson, W. G. and Kensler T. W. 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.

    PubMed  Google Scholar 

  53. Shirai T., Sano M., Tamano S., Takahashi S., Hirose M., Futakuchi M., Hasegawa R., Imaida K., Matsumoto K., Wakabayashi K., Sugimura T. and 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, 1997; 57: 195–198.

    PubMed  Google Scholar 

  54. Stuart G. R., Holcroft J., de Boer J. G. and Glickman B. W. Prostate mutations in rats induced by the suspected human carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine. Cancer Res, 2000; 60: 266–268.

    PubMed  Google Scholar 

  55. Lin X., Tascilar M., Lee W. H., Vles W. J., Lee B. H., Veeraswamy R., Asgari K., Freije D., van Rees B., Gage W. R., Bova G. S., Isaacs W. B., Brooks J. D., DeWeese T. L., De Marzo A. M. and Nelson W. G. GSTP1 CpG island hypermethylation is responsible for the absence of GSTP1 expression in human prostate cancer cells. Am J Pathol, 2001; 159: 1815–1826.

    PubMed  Google Scholar 

  56. Jeronimo C., Usadel H., Henrique R., Oliveira J., Lopes C., Nelson W. G. and Sidransky D. Quantitation of GSTP1 methylation in non-neoplastic prostatic tissue and organ-confined prostate adenocarcinoma. J Natl Cancer Inst, 2001; 93: 1747–1752.

    Article  PubMed  Google Scholar 

  57. Florl A. R., Steinhoff C., Muller M., Seifert H. H., Hader C., Engers R., Ackermann R. and Schulz, W. A. Coordinate hypermethylation at specific genes in prostate carcinoma precedes LINE-1 hypomethylation. Br J Cancer, 2004; 91: 985–994.

    PubMed  Google Scholar 

  58. Yamanaka M., Watanabe M., Yamada Y., Takagi A., Murata T., Takahashi, H., Suzuki H., Ito H., Tsukino H., Katoh T., Sugimura Y. and Shiraishi T. Altered methylation of multiple genes in carcinogenesis of the prostate. Int J Cancer, 2003; 106: 382–387.

    Article  PubMed  Google Scholar 

  59. Yegnasubramanian S., Kowalski J., Gonzalgo M. L., Zahurak M., Piantadosi S., Walsh P. C., Bova G. S., De Marzo A. M., Isaacs W. B. and Nelson W. G. Hypermethylation of CpG islands in primary and metastatic human prostate cancer. Cancer Res, 2004; 64:1975–1986.

    Article  PubMed  Google Scholar 

  60. Foster C. S., Bostwick D. G., Bonkhoff H., Damber J. E. van der Kwast T., Montironi R. and Sakr W. A. Cellular and molecular pathology of prostate cancer precursors. Scand J Urol Nephrol Suppl 2000; 19–43.

    Google Scholar 

  61. Nakayama M., Bennett C. J., Hicks J. L., Epstein J. I., Platz E. A., Nelson W. G. and De Marzo A. M. 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 lasercapture microdissection. Am J Pathol, 2003; 163: 923–933.

    PubMed  Google Scholar 

  62. Nelson W. G., De Marzo A. M., Deweese T. L., Lin X., Brooks J. D., Putzi M. J., Nelson C. P., Groopman J. D. and Kensler T. W. Preneoplastic prostate lesions: an opportunity for prostate cancer prevention. Ann N Y Acad Sci, 2001; 952: 135–144.

    PubMed  Google Scholar 

  63. Brooks J. D., Weinstein M., Lin X., Sun Y., Pin S. S., Bova G. S., Epstein J. I., Isaacs W. B. and Nelson W. G. CG island methylation changes near the GSTP1 gene in prostatic intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev, 1998; 7: 531–536.

    PubMed  Google Scholar 

  64. Woodson K., Gillespie J., Hanson J., Emmert-Buck M., Phillips J. M., Linehan W. M. and Tangrea J. A. Heterogeneous gene methylation patterns among pre-invasive and cancerous lesions of the prostate: a histopathologic study of whole mount prostate specimens. Prostate, 20044; 60: 25–31.

    Article  Google Scholar 

  65. Konishi N., Nakamura M., Kishi M., Nishimine M., Ishida E. and Shimada K. DNA hypermethylation status of multiple genes in prostate adenocarcinomas. Jpn J Cancer Res, 2002; 93: 767–773.

    PubMed  Google Scholar 

  66. Liu L., Yoon J. H., Dammann R., and Pfeifer G. P. Frequent hypermethylation of the RASSF1A gene in prostate cancer. Oncogene, 2002; 21: 6835–6840.

    Article  PubMed  Google Scholar 

  67. Zhu X., Leav I., Leung Y. K., Wu M., Liu Q., Gao Y., McNeal J. E. and Ho S. M. Dynamic regulation of estrogen receptor-beta expression by DNA methylation during prostate cancer development and metastasis. Am J Pathol, 2004; 164: 2003–2012.

    PubMed  Google Scholar 

  68. Maruyama R., Toyooka S., Toyooka K. O., Virmani A. K., Zochbauer-Muller S., Farinas A. J., Minna J. D., McConnell J., Frenkel E. P. and Gazdar A. F. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin Cancer Res, 2002; 8: 514–519.

    PubMed  Google Scholar 

  69. Smith W. L., DeWitt D. L. and Garavito R. M. Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem, 2000; 69: 145–182.

    Article  PubMed  Google Scholar 

  70. Dammann R., Schagdarsurengin U., Strunnikova M., Rastetter M., Seidel C., Liu L., Tommasi S. and Pfeifer G. P. Epigenetic inactivation of the Ras-association domain family 1 (RASSF1A) gene and its function in human carcinogenesis. Histol Histopathol, 2003; 18: 665–677.

    PubMed  Google Scholar 

  71. Nagase H. and Nakamura Y. Mutations of the APC (adenomatous polyposis coli) gene. Hum Mutat, 1993; 2: 425–434.

    Article  PubMed  Google Scholar 

  72. Esteller M., Sparks A., Toyota M., Sanchez-Cespedes M., Capella G., Peinado M. A., Gonzalez S., Tarafa G., Sidransky D., Meltze, S. J., Baylin S. B. and Herman J. G. Analysis of adenomatous polyposis coli promoter hypermethylation in human cancer. 2000; Cancer Res, 60: 4366–4371.

    PubMed  Google Scholar 

  73. Esteller M., Corn P. G., Baylin S. B. and Herman J. G. A gene hypermethylation profile of human cancer. Cancer Res, 2001; 61: 3225–3229.

    PubMed  Google Scholar 

  74. Virmani A. K., Rathi A., Sathyanarayana U. G., Padar A., Huang C. X., Cunnigham H. T., Farinas A. J., Milchgrub S., Euhus D. M., Gilcrease M., Herman J., Minna J. D. and Gazdar A. F. Aberrant methylation of the adenomatous polyposis coli (APC) gene promoter 1A in breast and lung carcinomas. Clin Cancer Res, 2001; 7: 1998–2004.

    PubMed  Google Scholar 

  75. Alberts B. Molecular biology of the cell, 2002, 4th edition. New York: Garland Science.

    Google Scholar 

  76. Chesire D. R., Ewing C. M., Sauvageot J., Bova G. S. and Isaacs W. B. Detection and analysis of beta-catenin mutations in prostate cancer. Prostate, 2000; 45: 323–334.

    Article  PubMed  Google Scholar 

  77. Ling V. Multidrug resistance: molecular mechanisms and clinical relevance. Cancer Chemother Pharmacol, 1997; 40Suppl: S3–8.

    PubMed  Google Scholar 

  78. Campain J. A., Padmanabhan R., Hwang J., Gottesman M. M. and Pastan I. Characterization of an unusual mutant of human melanoma cells resistant to anticancer drugs that inhibit topoisomerase II. J Cell Physiol, 1993; 155: 414–425.

    Article  PubMed  Google Scholar 

  79. Abu-Qare A. W., Elmasry E. and Abou-Donia M. B. A role for P-glycoprotein in environmental toxicology. J Toxicol Environ Health B Crit Rev, 2003; 6: 279–288.

    Article  PubMed  Google Scholar 

  80. van Tellingen O. The importance of drug-transporting P-glycoproteins in toxicology. Toxicol Lett, 2001; 120: 31–41.

    Article  PubMed  Google Scholar 

  81. Tada Y., Wada M., Kuroiwa K., Kinugawa N., Harada T., Nagayama J., Nakagawa M., Naito S. and Kuwano M. MDR1 gene overexpression and altered degree of methylation at the promoter region in bladder cancer during chemotherapeutic treatment. Clin Cancer Res, 2000; 6: 4618–4627.

    PubMed  Google Scholar 

  82. Nakayama M., Wada M., Harada T., Nagayama J., Kusaba H., Ohshima K., Kozuru M., Komatsu H., Ueda R. and Kuwano M. Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood, 1998; 92: 4296–4307.

    PubMed  Google Scholar 

  83. Kantharidis P., El-Osta A., deSilva M., Wall D. M., Hu X. F., Slater A., Nadalin G., Parkin J. D. and Zalcberg J. R. Altered methylation of the human MDR1 promoter is associated with acquired multidrug resistance. Clin Cancer Res, 1997; 3: 2025–2032.

    PubMed  Google Scholar 

  84. Desiderato L., Davey M. W. and Piper A. A. Demethylation of the human MDR1 5′ region accompanies activation of P-glycoprotein expression in a HL60 multidrug resistant subline. Somat Cell Mol Genet, 1997; 23: 391–400.

    PubMed  Google Scholar 

  85. Jeronimo C., Henrique R., Hoque M. O., Ribeiro F. R., Oliveira J., Fonseca D., Teixeira M. R., Lopes, C. and Sidransky D. Quantitative RARbeta2 hypermethylation: a promising prostate cancer marker. Clin Cancer Res, 2004; 10: 4010–4014.

    Article  PubMed  Google Scholar 

  86. Zhang J., Liu L. and Pfeifer G. P. Methylation of the retinoid response gene TIG1 in prostate cancer correlates with methylation of the retinoic acid receptor beta gene. Oncogene, 23: 2004; 2241–2249.

    Article  PubMed  Google Scholar 

  87. Bronner C. E., Baker S. M., Morrison P. T., Warren G., Smith L. G., Lescoe M. K., Kane M., Earabino C., Lipford J., Lindblom A. and et al. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature, 1994; 368: 258–261.

    Article  PubMed  Google Scholar 

  88. Li A. J. and Karlan B. Y. Genetic factors in ovarian carcinoma. Curr Oncol Rep, 2001;3: 27–32.

    PubMed  Google Scholar 

  89. Paech K., Webb P., Kuiper G. G., Nilsson S., Gustafsson J., Kushner P. J. and Scanlan, T. S. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science, 1997; 277: 1508–1510.

    Article  PubMed  Google Scholar 

  90. Krege J. H., Hodgin J. B., Couse J. F., Enmark E., Warner M., Mahler J. F., Sar M., Korach K. S., Gustafsson J. A. and Smithies, O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A, 1998;95: 15677–15682.

    Article  PubMed  Google Scholar 

  91. Leav I., Lau K. M., Adams J. Y., McNeal J. E., Taplin M. E., Wang J., Singh H. and Ho S. M. Comparative studies of the estrogen receptors beta and alpha and the androgen receptor in normal human prostate glands, dysplasia, and in primary and metastatic carcinoma. Am J Pathol, 2001; 159: 79–92.

    PubMed  Google Scholar 

  92. Horvath L. G., Henshall S. M., Lee C. S., Head D. R., Quinn D. I., Makela S., Delprado W., Golovsky D., Brenner P. C., O'Neill G., Kooner R., Stricker P. D., Grygiel J. J., Gustafsson J. A. and Sutherland R. L. Frequent loss of estrogen receptor-beta expression in prostate cancer. Cancer Res, 2001; 61: 5331–5335.

    PubMed  Google Scholar 

  93. Lin X., Asgari K., Putzi M. J., Gage W. R., Yu X., Cornblatt B. S., Kumar A., Piantadosi S., DeWeese T. L., De Marzo A. M. and Nelson W. G. 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, 2001; 61: 8611–8616.

    PubMed  Google Scholar 

  94. De Weese T. L. and Nelson W. G. Unpublished Data. 2004.

    Google Scholar 

  95. Henderson C. J., Wolf C. R., Kitteringham N., Powell H., Otto D. and Park B. K. Increased resistance to acetaminophen hepatotoxicity in mice lacking glutathione S-transferase Pi. Proc Natl Acad Sci U S A, 2000; 97: 12741–12745.

    Article  PubMed  Google Scholar 

  96. Morrow C. S., Diah S., Smitherman P. K., Schneider E. and Townsend A. J. Multidrug resistance protein and glutathione S-transferase P1-1 act in synergy to confer protection from 4-nitroquinoline 1-oxide toxicity. Carcinogenesis, 1998; 19: 109–115,.

    Article  PubMed  Google Scholar 

  97. Lorico A., Nesland J., Emilsen E., Fodstad O. and Rappa G. Role of the multidrug resistance protein 1 gene in the carcinogenicity of aflatoxin B1: investigations using mrp1-null mice. Toxicology, 2002; 171: 201–205.

    Article  PubMed  Google Scholar 

  98. Loe D. W., Stewart R. K., Massey T. E., Deeley R. G. and Cole S. P. ATP-dependent transport of aflatoxin B1 and its glutathione conjugates by the product of the multidrug resistance protein (MRP) gene. Mol Pharmacol, 1997; 51: 1034–1041.

    PubMed  Google Scholar 

  99. Diah S. K., Smitherman P. K., Townsend A. J. and Morrow C. S. Detoxification of 1-chloro-2,4-dinitrobenzene in MCF7 breast cancer cells expressing glutathione Stransferase P1-1 and/or multidrug resistance protein 1. Toxicol Appl Pharmacol, 1999;157: 85–93.

    Article  PubMed  Google Scholar 

  100. Lin X. and Nelson W. G. Methyl-CpG-binding domain protein-2 mediates transcriptional repression associated with hypermethylated GSTP1 CpG islands in MCF-7 breast cancer cells. Cancer Res, 2003; 63: 498–504.

    PubMed  Google Scholar 

  101. David G. L., Yegnasubramanian S., Kumar A., Marchi V. L., De Marzo A. M., Lin X. and Nelson W. G. MDR1 Promoter Hypermethylation in MCF-7 Human Breast Cancer Cells: Changes in Chromatin Structure Induced by Treatment with 5-Aza-Cytidine. Cancer Biol Ther, 2004; 3: 540–548.

    PubMed  Google Scholar 

  102. Holst C. R., Nuovo G. J., Esteller M., Chew K., Baylin S. B., Herman J. G. and Tlsty T. D. Methylation of p16(INK4a) promoters occurs in vivo in histologically normal human mammary epithelia. Cancer Res, 2003; 63: 1596–1601.

    PubMed  Google Scholar 

  103. Pradhan S., Bacolla A., Wells R. D. and Roberts R. J. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J Biol Chem, 1999; 274: 33002–33010.

    Article  PubMed  Google Scholar 

  104. Gowher H. and Jeltsch A. Enzymatic properties of recombinant Dnmt3a DNA methyltransferase from mouse: the enzyme modifies DNA in a non-processive manner and also methylates non-CpG [correction of non-CpA] sites. J Mol Biol, 2001; 309:1201–1208.

    Article  PubMed  Google Scholar 

  105. Okano M., Xie S., and Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet, 1998; 19: 219–220.

    Article  PubMed  Google Scholar 

  106. Jeltsch A. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem, 2002; 3: 274–293.

    Article  PubMed  Google Scholar 

  107. Okano M., Bell D. W., Haber D. A. and Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell, 1999; 99: 247–257.

    Article  PubMed  Google Scholar 

  108. Rhee I., Jair K. W., Yen R. W., Lengauer C., Herman J. G., Kinzler K. W., Vogelstein B., Baylin S. B. and Schuebel K. E. CpG methylation is maintained in human cancer cells lacking DNMT1. Nature, 2000; 404: 1003–1007.

    Article  PubMed  Google Scholar 

  109. Rhee I., Bachman K. E., Park B. H., Jair K. W., Yen R. W., Schuebel K. E., Cui H., Feinberg A. P., Lengauer C., Kinzler K. W., Baylin S. B. and Vogelstein B. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature, 2002; 416:552–556.

    Article  PubMed  Google Scholar 

  110. Hmadcha, A., Bedoya, F. J., Sobrino, F., and Pintado, E. Methylation-dependent gene silencing induced by interleukin 1beta via nitric oxide production. J Exp Med, 190:1595–1604, 1999.

    Article  PubMed  Google Scholar 

  111. Paget S. The distribution of secondary growths in cancer of the breast. Lancet, 1889; 1:571.

    Article  Google Scholar 

  112. Tantivejkul K., Kalikin L. M. and Pienta K. J. Dynamic process of prostate cancer metastasis to bone. J Cell Biochem, 2004; 91: 706–717.

    Article  PubMed  Google Scholar 

  113. Nelson J., Bagnato A., Battistini B. and Nisen P. The endothelin axis: emerging role in cancer. Nat Rev Cancer, 2003; 3: 110–116.

    Article  PubMed  Google Scholar 

  114. Nelson J. B., Chan-Tack K., Hedican S. P., Magnuson S. R., Opgenorth T. J., Bova G. S. and Simons J. W. Endothelin-1 production and decreased endothelin B receptor expression in advanced prostate cancer. Cancer Res, 1996; 56: 663–668.

    PubMed  Google Scholar 

  115. Mohammad K. S. and Guise T. A. Mechanisms of osteoblastic metastases: role of endothelin-1. Clin Orthop 2003; S67–74.

    Google Scholar 

  116. Yin J. J., Mohammad K. S., Kakonen S. M., Harris S., Wu-Wong J. R., Wessale J. L., Padley R. J., Garrett I. R., Chirgwin J. M. and Guise T. A. A causal role for endothelin-1 in the pathogenesis of osteoblastic bone metastases. Proc Natl Acad Sci U S A, 2003;100: 10954–10959.

    Article  PubMed  Google Scholar 

  117. Carducci M. A., Padley R. J., Breul J., Vogelzang N. J., Zonnenberg B. A., Daliani D. D., Schulman C. C., Nabulsi A. A., Humerickhouse R. A., Weinberg M. A., Schmitt J. L. and Nelson J. B. Effect of endothelin-A receptor blockade with atrasentan on tumor progression in men with hormone-refractory prostate cancer: a randomized, phase II, placebo-controlled trial. J Clin Oncol, 2003; 21: 679–689.

    Article  PubMed  Google Scholar 

  118. Goessl C., Muller M., Heicappell R., Krause H. and Miller K. DNA-based detection of prostate cancer in blood, urine, and ejaculates. Ann N Y Acad Sci, 2001; 945: 51–58.

    PubMed  Google Scholar 

  119. Goessl C., Krause H., Muller M., Heicappell R., Schrader M., Sachsinger J. and Miller K. Fluorescent methylation-specific polymerase chain reaction for DNA-based detection of prostate cancer in bodily fluids. Cancer Res, 2000; 60: 5941–5945.

    PubMed  Google Scholar 

  120. Jeronimo C., Usadel H., Henrique R., Silva C., Oliveira J., Lopes C. and Sidransky D. Quantitative GSTP1 hypermethylation in bodily fluids of patients with prostate cancer. Urology, 2002; 60: 1131–1135.

    Article  PubMed  Google Scholar 

  121. Bastian P. J., Palapattu G. S., Lin X. S., Yegnasubramanian S., Mangold L. A., Trock B., Eisenberger C. F., Partin A. W. and Nelson W. G. Preoperative Serum DNA GSTP1 CpG Island Hypermethylation and the Risk of Early PSA Recurrence Following Radical Prostatectomy. Unpublished Data, 2004.

    Google Scholar 

  122. Goessl C., Muller M. and Miller K. Methylation-specific PCR (MSP) for detection of tumour DNA in the blood plasma and serum of patients with prostate cancer. Prostate Cancer Prostatic Dis, 2000; 3: S17.

    Article  PubMed  Google Scholar 

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  1. The Sidney Kimmel Comprehensive Cancer Center, The Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Srinivasan Yegnasubramanian & William G. Nelson

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  1. Srinivasan Yegnasubramanian
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  1. Spanish National Cancer Centre (CNIO), Madrid, Spain

    Manel Esteller

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Yegnasubramanian, S., Nelson, W.G. (2005). CpG Island Hypermethylation Changes during Prostate Cancer Progression and Metastasis. In: Esteller, M. (eds) DNA Methylation, Epigenetics and Metastasis. Cancer Metastasis — Biology and Treatment, vol 7. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3642-6_4

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