Application of DNA methylation biomarkers for endometrial cancer management

Expert Review of Molecular Diagnostics

Volumn 8, Issue 5, 2008, Pages 607-616

  Jiang, Shi Wen ^a   Li, Jinping ^a   Podratz, Karl ^b   Dowdy, Sean ^b  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

Author keywords

Biomarker; Cancer diagnosis; Cancer treatment; DNA methylation; Endometrial cancer; Epigenetics; Intravaginal tampons

Indexed keywords

ACYLTRANSFERASE; BIOLOGICAL MARKER; CARBOPLATIN; CYTOTOXIC AGENT; DNA; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE INHIBITOR; DOXORUBICIN; ESTROGEN RECEPTOR; FLUOROURACIL; GESTAGEN; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; PACLITAXEL; PROGESTERONE RECEPTOR; PROTEIN MLH1; PROTEIN MSH2; SOMATOMEDIN; VORINOSTAT;

ACETYLATION; ANTINEOPLASTIC ACTIVITY; CANCER PATIENT; CANCER SCREENING; COLORECTAL CANCER; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; ENDOMETRIUM; ENDOMETRIUM BIOPSY; ENDOMETRIUM CANCER; ENDOMETRIUM HYPERPLASIA; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; HUMAN; HYSTERECTOMY; INFECTION RISK; MOUTH CANCER; NON INVASIVE PROCEDURE; NONHUMAN; OVARY POLYCYSTIC DISEASE; PHENOTYPE; RECURRENT CANCER; REVIEW; RISK ASSESSMENT; TAMPON; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CYTOLOGY; VAGINAL ULCER; VAGINITIS;

ANIMALS; BIOLOGICAL MARKERS; DNA; DNA METHYLATION; ENDOMETRIAL NEOPLASMS; FEMALE; HUMANS; RECURRENCE; RISK ASSESSMENT;

EID: 51849124647     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/14737159.8.5.607     Document Type: Review

References (106)

1. Jemal A, Siegel R, Ward E et al. Cancer statistics, 2008. CA Cancer J. Clin. 58, 71-96 (2008).
2. Creutzberg CL, van Putten WL, Koper PC et al. Surgery and postoperative radiotherapy versus surgery alone for patients with stage-1 endometrial carcinoma: multicentre randomised trial. PORTEC Study Group. Post Operative Radiation Therapy in Endometrial Carcinoma. Lancet 355, 1404-1411 (2000).
3. Jereczek-Fossa B, Badzio A, Jassem J. Surgery followed by radiotherapy in endometrial cancer. Analysis of survival and patterns of failure. Int. J. Gynecol. Cancer 9, 285-294 (1999).
4. Bocker T, Ruschoff J, Fishel R. Molecular diagnostics of cancer predisposition. Hereditary non-polyposis colorectal carcinoma and mismatch repair defects. Biochim. Biophys. Acta 1423, O1-O10 (1999).
5. Esteller M. Epigenetic lesions causing genetic lesions in human cancer. Promoter hypermethylation of DNA repair genes. Eur. J. Cancer 36, 2294-2300 (2000). • Detailed review on hypermethylation of DNA repair genes in cancer as well as the intricate connection between epigenetic events and genetic lesions.
6. Herman JG, Umar A, Polyak K et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl Acad. Sci. USA 95, 6870-6875 (1998). • hMLH1 promoter hypermethylation/silencing is associated with MSI+ phenotype and restoration of hMLH1 expression rescues the mismatch repair function.
7. Furlan D, Carnevali I, Marcomini B et al. The high frequency of de novo promoter methylation in synchronous primary endometrial and ovarian carcinomas. Clin. Cancer Res. 12, 3329-3336 (2006).
8. + and RER- sporadic endometrial carcinomas in a large population-based series. Int. J. Gynecol. Cancer 14, 957-965 (2004).
9. Salvesen HB, MacDonald N, Ryan A et al. PTEN methylation is associated with advanced stage and microsatellite instability in endometrial carcinoma. Int. J. Cancer 91, 22-26 (2001).
10. Ehrlich CE, Young PC, Stehman FB, Sutton GP, Alford WM. Steroid receptors and clinical outcome in patients with adenocarcinoma of the endometrium. Am. J. Obstet. Gynecol. 158, 796-807 (1988).
11. Sasaki M, Dharia A, Oh BR et al. Progesterone receptor B gene inactivation and CpG hypermethylation in human uterine endometrial cancer. Cancer Res. 61, 97-102 (2001).
12. Xiong Y, Dowdy SC, Gonzalez Bosquet J et al. Epigenetic-mediated upregulation of progesterone receptor B gene in endometrial cancer cell lines. Gynecol. Oncol. 99, 135-141 (2005).
13. Whitcomb BP, Mutch DG, Herzog TJ et al. Frequent HOXA11 and THBS2 promoter methylation, and a methylator phenotype in endometrial adenocarcinoma. Clin. Cancer Res. 9, 2277-2287 (2003).
14. Dowdy SC, Gostout BS, Shridhar V et al. Biallelic methylation and silencing of paternally expressed gene 3 (PEG3) in gynecologic cancer cell lines. Gynecol. Oncol. 99, 126-134 (2005).
15. Chan QK, Khoo US, Chan KY et al. Promoter methylation and differential expression of pi-class glutathione S-transferase in endometrial carcinoma. J. Mol. Diagn. 7, 8-16 (2005).
16. Grady WM, Willis J, Guilford PJ et al. Methylation of the CDH1 promoter as the second genetic hit in hereditary diffuse gastric cancer. Nat. Genet. 26, 16-17 (2000).
17. Esteller M, Silva JM, Dominguez G et al. Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J. Natl Cancer Inst. 92, 564-569 (2000).
18. Jolly CJ, Neuberger MS. Somatic hypermutation of immunoglobulin kappa transgenes. Association of mutability with demethylation. Immunol. Cell Biol. 79, 18-22 (2001).
19. Florl AR, Franke KH, Niederacher D et al. DNA methylation and the mechanisms of CDKN2A inactivation in transitional cell carcinoma of the urinary bladder. Lab. Invest. 80, 1513-1522 (2000).
20. Matias-Guiu X, Catasus L, Bussaglia E et al. Molecular pathology of endometrial hyperplasia and carcinoma. Hum. Pathol. 32, 569-577 (2001).
21. Dodge JE, Okano M, Dick F et al. Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem. 280, 17986-17991 (2005). •• DNA methylation mechanism and potential role of DNMT3B for the establishment of DNA methylation pattern in embryonic fibroblasts.
22. Pradhan M, Abeler VM, Danielsen HE et al. Image cytometry DNA ploidy correlates with histological subtypes in endometrial carcinomas. Mod. Pathol. 19, 1227-1235 (2006).
23. Umbricht CB, Evron E, Gabrielson E et al. Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene 20, 3348-3353 (2001).
24. Ibanez de Caceres I, Battagli C, Esteller M et al. Tumor cell-specific BRCA1 and RASSF1A hypermethylation in serum, plasma, and peritoneal fluid from ovarian cancer patients. Cancer Res. 64, 6476-6481 (2004).
25. Esteller M, Catasus L, Matias-Guiu X et al. hMLH1 promoter hypermethylation is an early event in human endometrial tumorigenesis. Am. J. Pathol. 155, 1767-1772 (1999).
26. Norris HJ, Connor MP, Kurman RJ. Preinvasive lesions of the endometrium. Clin. Obstet. Gynaecol. 13, 725-738 (1986).
27. Fox H, Buckley CH. The endometrial hyperplasias and their relationship to endometrial neoplasia. Histopathology 6, 493-510 (1982).
28. Nasir A, Boulware D, Kaiser HE et al. Cyclooxygenase-2 (COX-2) expression in human endometrial carcinoma and precursor lesions and its possible use in cancer chemoprevention and therapy. In Vivo 21, 35-43 (2007).
29. Horowitz N, Pinto K, Mutch DG et al. Microsatellite instability, MLH1 promoter methylation, and loss of mismatch repair in endometrial cancer and concomitant atypical hyperplasia. Gynecol. Oncol. 86, 62-68 (2002).
30. Wang C, Mirkin BL, Dwivedi RS. DNA (cytosine) methyltransferase overexpression is associated with acquired drug resistance of murine neuroblastoma cells. Int. J. Oncol. 18, 323-329 (2001).
31. Saito T, Nishimura M, Yamasaki H, Kudo R. Hypermethylation in promoter region of E-cadherin gene is associated with tumor dedifferention and myometrial invasion in endometrial carcinoma. Cancer 97, 1002-1009 (2003).
32. Nakayama H, Sano T, Motegi A et al. Increasing 14-3-3 sigma expression with declining estrogen receptor a and estrogen-responsive finger protein expression defines malignant progression of endometrial carcinoma. Pathol. Int. 55, 707-715 (2005).
33. Shames DS, Minna JD, Gazdar AF. Methods for detecting DNA methylation in tumors. From bench to bedside. Cancer Lett. 251, 187-198 (2007).
34. Shi H, Wang MX, Caldwell CW. CpG islands. Their potential as biomarkers for cancer. Expert Rev. Mol. Diagn. 7, 519-531 (2007).
35. Baylin SB. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2, S4-S11 (2005).
36. Laird PW. Cancer epigenetics. Hum. Mol. Genet. 14, R65-R76 (2005). •• Broad review covering the significance of DNA methylation in cancer progression as well as implication of epigenetic markers for cancer detection and assessment.
37. Issa JP. DNA methylation as a therapeutic target in cancer. Clin. Cancer Res. 13, 1634-1637 (2007).
38. Fiegl H, Elmasry K. Cancer diagnosis, risk assessment and prediction of therapeutic response by means of DNA methylation markers. Dis. Markers 23, 89-96 (2007).
39. Herranz M, Esteller M. DNA methylation and histone modifications in patients with cancer. Potential prognostic and therapeutic targets. Methods Mol. Biol. 361, 25-62 (2007).
40. Liu ZJ, Maekawa M. Polymerase chain reaction-based methods of DNA methylation analysis. Anal. Biochem. 317, 259-265 (2003).
41. Yang HJ, Liu VW, Wang Y et al. Differential DNA methylation profiles in gynecological cancers and correlation with clinico-pathological data. BMC Cancer 6, 212 (2006).
42. Zighelboim I, Goodfellow PJ, Schmidt AP et al. Differential methylation hybridization array of endometrial cancers reveals two novel cancer-specific methylation markers. Clin. Cancer Res. 13, 2882-2889 (2007).
43. Paz MF, Wei S, Cigudosa JC et al. Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases. Hum. Mol. Genet. 12, 2209-2219 (2003).
44. Hoque MO, Kim MS, Ostrow KL et al. Genome-wide promoter analysis uncovers portions of the cancer methylome. Cancer Res. 68, 2661-2670 (2008).
45. Suzuki H, Itoh F, Toyota M et al. Distinct methylation pattern and microsatellite instability in sporadic gastric cancer. Int. J. Cancer 83, 309-313 (1999).
46. Eads CA, Laird PW. Combined bisulfite restriction analysis (COBRA). Methods Mol. Biol. 200, 71-85 (2002).
47. Uhlmann K, Brinckmann A, Toliat MR et al. Evaluation of a potential epigenetic biomarker by quantitative methyl-single nucleotide polymorphism analysis. Electrophoresis 23, 4072-4079 (2002).
48. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R. Sensitive and quantitative universal pyrosequencing methylation analysis of CpG sites. Biotechniques 35, 146-150 (2003).
49. Brena RM, Huang TH, Plass C. Quantitative assessment of DNA methylation. Potential applications for disease diagnosis, classification, and prognosis in clinical settings. J. Mol. Med. 84, 365-377 (2006). • Comprehensive review on different methods used for quantitative analysis of DNA methylation.
50. Bearzatto A, Conte D, Frattini M et al. p16(INK4A) hypermethylation detected by fluorescent methylation-specific PCR in plasmas from non-small cell lung cancer. Clin. Cancer Res. 8, 3782-3787 (2002).
51. Ulivi P, Zoli W, Calistri D et al. p16INK4A and CDH13 hypermethylation in tumor and serum of non-small cell lung cancer patients. J. Cell Physiol. 206, 611-615 (2006).
52. Xie GS, Hou AR, Li LY et al. Aberrant p16 promoter hypermethylation in bronchial mucosae as a biomarker for the early detection of lung cancer. Chin. Med. J. 119, 1469-1472 (2006).
53. Chuang CK, Chu DC, Tzou RD et al. Hypermethylation of the CpG islands in the promoter region flanking GSTP1 gene is a potential plasma DNA biomarker for detecting prostate carcinoma. Cancer Detect. Prev. 31, 59-63 (2007).
54. Herman JG. Circulating methylated DNA. Ann. NY Acad. Sci. 1022, 33-39 (2004).
55. Schmiemann V, Bocking A, Kazimirek M et al. Methylation assay for the diagnosis of lung cancer on bronchial aspirates. A cohort study. Clin. Cancer Res. 11, 7728-7734 (2005).
56. Jiang P, Watanabe H, Okada G et al. Diagnostic utility of aberrant methylation of tissue factor pathway inhibitor 2 in pure pancreatic juice for pancreatic carcinoma. Cancer Sci. 97, 1267-1273 (2006).
57. Watanabe H, Okada G, Ohtsubo K et al. Aberrant methylation of secreted apoptosis-related protein 2 (SARP2) in pure pancreatic juice in diagnosis of pancreatic neoplasms. Pancreas 32, 382-389 (2006).
58. Hoque MO, Begum S, Topaloglu O et al. Quantitation of promoter methylation of multiple genes in urine DNA and bladder cancer detection. J. Natl Cancer Inst. 98, 996-1004 (2006).
59. Belinsky SA, Palmisano WA, Gilliland FD et al. Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res. 6, 2370-2377 (2002). • Identification of multiple hypermethylated genes in sputum from former and current smokers.
60. Smith RA, von Eschenbach AC, Wender R et al. American Cancer Society guidelines for the early detection of cancer. Update of early detection guidelines for prostate, colorectal, and endometrial cancers. Also Update 2001 - testing for early lung cancer detection. CA Cancer J. Clin. 51, 38-75; quiz 77-80 (2001).
61. Bader GM, Simon TR, Koss LG, Day E. A study of the detection-tampon method as a screening device for uterine cancer. Cancer 10, 332-337 (1957).
62. Brunschwig A. Detection of endometrial adenocarcinoma by tampon-smear method. Cancer 10, 120-123 (1957).
63. Brunschwig A. A method for mass screening for cytological detection of carcinoma of the cervix uteri. Cancer 7, 1182-1184 (1954).
64. Papanicolaou GN. Cytological evaluation of smears prepared by the tampon method for the detection of carcinoma of the uterine cervix. Cancer 7, 1185-1190 (1954).
65. Barrett KF, Bledsoe S, Greer BE et al. Tampon-induced vaginal or cervical ulceration. Am. J. Obstet. Gynecol. 127, 332-333 (1977).
66. Weissberg SM, Dodson MG. Recurrent vaginal and cervical ulcers associated with tampon use. JAMA 250, 1430-1431 (1983).
67. Kehrberg MW, Latham RH, Haslam BT et al. Risk factors for staphylococcal toxic-shock syndrome. Am. J. Epidemiol. 114, 873-879 (1981).
68. Fox H. The pathology of tampon usage and of the toxic shock syndrome. Postgrad. Med. J. 61(Suppl. 1), 31-33 (1985).
69. Widschwendter A, Gattringer C, Ivarsson L et al. Analysis of aberrant DNA methylation and human papillomavirus DNA in cervicovaginal specimens to detect invasive cervical cancer and its precursors. Clin. Cancer Res. 10, 3396-3400 (2004). •• Methylation patterns of multiple methylation target genes are documented and found to be useful for prediction of invasive cervical cancers.
70. Fiegl H, Gattringer C, Widschwendter A et al. Methylated DNA collected by tampons - a new tool to detect endometrial cancer. Cancer Epidemiol. Biomarkers Prev. 13, 882-888 (2004).
71. Campan M, Weisenberger DJ, Laird PW. DNA methylation profiles of female steroid hormone-driven human malignancies. Curr. Top. Microbiol. Immunol. 310, 141-178 (2006).
72. Kang S, Kim JW, Kang GH et al. Comparison of DNA hypermethylation patterns in different types of uterine cancer. Cervical squamous cell carcinoma, cervical adenocarcinoma and endometrial adenocarcinoma. Int. J. Cancer 118, 2168-2171 (2006).
73. Toyota M, Issa JP. CpG island methylator phenotypes in aging and cancer. Semin. Cancer Biol. 9, 349-357 (1999).
74. Issa JP. CpG island methylator phenotype in cancer. Nat. Rev. Cancer 4, 988-993 (2004).
75. Ogino S, Kawasaki T, Kirkner GJ et al. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer. Possible associations with male sex and KRAS mutations. J. Mol. Diagn. 8, 582-588 (2006).
76. Ogino S, Kawasaki T, Kirkner GJ et al. 18q loss of heterozygosity in microsatellite stable colorectal cancer is correlated with CpG island methylator phenotype-negative (CIMP-0) and inversely with CIMP-low and CIMP-high. BMC Cancer 7, 72 (2007).
77. Goel A, Nagasaka T, Arnold CN et al. The CpG island methylator phenotype and chromosomal instability are inversely correlated in sporadic colorectal cancer. Gastroenterology 132, 127-138 (2007).
78. Curtin K, Slattery ML, Ulrich CM et al. Genetic polymorphisms in one-carbon metabolism. associations with CpG island methylator phenotype (CIMP) in colon cancer and the modifying effects of diet. Carcinogenesis 28, 1672-1679 (2007).
79. Slattery ML, Curtin K, Sweeney C et al. Diet and lifestyle factor associations with CpG island methylator phenotype and BRAF mutations in colon cancer. Int. J. Cancer 120, 656-563 (2007).
80. Shen L, Catalano PJ, Benson AB III et al. Association between DNA methylation and shortened survival in patients with advanced colorectal cancer treated with 5-fluorouracil based chemotherapy. Clin. Cancer Res. 13, 6093-6098 (2007).
81. Ogino S, Meyerhardt JA, Kawasaki T et al. CpG island methylation, response to combination chemotherapy, and patient survival in advanced microsatellite stable colorectal carcinoma. Virchows Arch. 450, 529-537 (2007).
82. Shaw RJ, Hall GL, Lowe D et al. CpG island methylation phenotype (CIMP) in oral cancer. associated with a marked inflammatory response and less aggressive tumour biology. Oral. Oncol. 43, 878-886 (2007).
83. Mell LK, Meyer JJ, Tretiakova M et al. Prognostic significance of E-cadherin protein expression in pathological stage I-III endometrial cancer. Clin. Cancer Res. 10, 5546-5553 (2004).
84. Salvesen HB, Stefansson I, Kretzschmar EI et al. Significance of PTEN alterations in endometrial carcinoma. A population-based study of mutations, promoter methylation and PTEN protein expression. Int. J. Oncol. 25, 1615-1623 (2004).
85. Dowdy SC, Jiang S, Zhou XC et al. Histone deacetylase inhibitors and paclitaxel cause synergistic effects on apoptosis and microtubule stabilization in papillary serous endometrial cancer cells. Mol. Cancer Ther. 5, 2767-2776 (2006).
86. Takai N, Desmond JC, Kumagai T et al. Histone deacetylase inhibitors have a profound antigrowth activity in endometrial cancer cells. Clin. Cancer Res. 10, 1141-1149 (2004).
87. Ahn MY, Jung JH, Na YJ, Kim HS. A natural histone deacetylase inhibitor, Psammaplin A, induces cell cycle arrest and apoptosis in human endometrial cancer cells. Gynecol. Oncol. 108, 27-33 (2008).
88. Jiang S, Dowdy SC, Meng XW et al. Histone deacetylase inhibitors induce apoptosis in both type I and type II endometrial cancer cells. Gynecol. Oncol. 105, 493-500 (2007).
89. Podratz KC. Hormonal therapy in endometrial carcinoma. Recent Results Cancer Res. 118, 242-251 (1990).
90. Lentz SS. Endocrine therapy of endometrial cancer. Cancer Treat. Res. 94, 89-106 (1998).
91. Dai D, Wolf DM, Litman ES et al. Progesterone inhibits human endometrial cancer cell growth and invasiveness. down-regulation of cellular adhesion molecules through progesterone B receptors. Cancer Res. 62, 881-886 (2002).
92. Dai D, Albitar L, Nguyen T et al. A therapeutic model for advanced endometrial cancer. Systemic progestin in combination with local adenoviral-mediated progesterone receptor expression. Mol. Cancer Ther. 4, 169-175 (2005).
93. Lentz SS, Brady MF, Major FJ et al. High-dose megestrol acetate in advanced or recurrent endometrial carcinoma. A Gynecologic Oncology Group Study. J. Clin. Oncol. 14, 357-361 (1996).
94. Suter CM, Martin DI, Ward RL. Germline epimutation of MLH1 in individuals with multiple cancers. Nat. Genet. 36, 497-501 (2004).
95. Hitchins MP, Wong JJ, Suthers G et al. Inheritance of a cancer-associated MLH1 germ-line epimutation. N. Engl. J. Med. 356, 697-705 (2007).
96. Martin DI, Ward R, Suter CM. Germline epimutation. A basis for epigenetic disease in humans. Ann. NY Acad. Sci. 1054, 68-77 (2005).
97. Valle L, Carbonell P, Fernandez V et al. MLH1 germline epimutations in selected patients with early-onset non-polyposis colorectal cancer. Clin. Genet. 71, 232-237 (2007).
98. Chan TL, Yuen ST, Kong CK et al. Heritable germline epimutation of MSH2 in a family with hereditary nonpolyposis colorectal cancer. Nat. Genet. 38, 1178-1183 (2006).
99. Horsthemke B. Epimutations in human disease. Curr. Top. Microbiol. Immunol. 310, 45-59 (2006).
100. Richardson B. Impact of aging on DNA methylation. Ageing Res. Rev. 2, 245-261 (2003).
101. Rath PC, Kanungo MS. Methylation of repetitive DNA sequences in the brain during aging of the rat. FEBS Lett. 244, 193-198 (1989).
102. Romanov GA, Vanyushin BF. Methylation of reiterated sequences in mammalian DNAs. Effects of the tissue type, age, malignancy and hormonal induction. Biochim. Biophys. Acta 653, 204-218 (1981).
103. Lengauer C, Kinzler KW, Vogelstein B. DNA methylation and genetic instability in colorectal cancer cells. Proc. Natl Acad. Sci. USA 94, 2545-2550 (1997). • Mechanistic investigation on how DNA methylation changes may lead to alterations in gene expression and genomic instability.
104. Issa JP, Vertino PM, Boehm CD et al. Switch from monoallelic to biallelic human IGF2 promoter methylation during aging and carcinogenesis. Proc. Natl Acad. Sci. USA 93, 11757-11762 (1996).
105. Ahuja N, Li Q, Mohan AL et al. Aging and DNA methylation in colorectal mucosa and cancer. Cancer Res. 58, 5489-5494 (1998).
106. Toyota M, Ahuja N, Ohe-Toyota M et al. CpG island methylator phenotype in colorectal cancer. Proc. Natl Acad. Sci. USA 96, 8681-8686 (1999).