RUNX3 promoter methylation in colorectal cancer: Its relationship with microsatellite instability and its suitability as a novel serum tumor marker

Anticancer Research

Volumn 30, Issue 7, 2010, Pages 2673-2682

  Nishio, Minoru ^a   Sakakura, Chouhei ^a   Nagata, Tomoyuki ^a   Komiyama, Sosuke ^a   Miyashita, Atsushi ^a   Hamada, Takuo ^a   Kuryu, Yoshiaki ^a   Ikoma, Hisashi ^a   Kubota, Takeshi ^a   Kimura, Akio ^a   Nakanishi, Masayoshi ^a   Ichikawa, Daisuke ^a   Fujiwara, Hitoshi ^a   Okamoto, Kazuma ^a   Ochiai, Toshiya ^a   Kokuba, Yukihito ^a   Sonoyama, Teruhisa ^a   Ida, Hiroshia ^b   Ito, Kosei ^c   Chiba, Tsutomu ^b   Ito, Yoshiaki ^d   Otsuji, Eigo ^a   more..

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c NAGASAKI UNIVERSITY   (Japan)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Colorectal cancer; Methylation; MSI; RUNX3

Indexed keywords

TRANSCRIPTION FACTOR RUNX3; TUMOR MARKER;

ADULT; ADVANCED CANCER; AGED; ARTICLE; BIOLOGICAL MONITORING; CANCER DIAGNOSIS; CANCER INVASION; CANCER PATIENT; CANCER STAGING; COLORECTAL CANCER; COLORECTAL TUMOR; CONTROLLED STUDY; CPG ISLAND; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; MALE; MICROSATELLITE INSTABILITY; MICROSATELLITE MARKER; POSTOPERATIVE PERIOD; PREOPERATIVE PERIOD; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN METHYLATION; QUANTITATIVE ANALYSIS; TUMOR DIFFERENTIATION;

AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; COLORECTAL NEOPLASMS; CORE BINDING FACTOR ALPHA 3 SUBUNIT; DNA METHYLATION; FEMALE; HUMANS; INTESTINAL MUCOSA; MALE; MICROSATELLITE INSTABILITY; MIDDLE AGED; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 77955783215     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Silva JM, Dominguez G, Garcia JM, Gonzalez R, Villanueva MJ, Navarro F, Provencio M, San Martin S, España P and Bonilla F: Presence of tumor DNA in plasma of breast cancer patients: clinicopathological correlations. Cancer Res 59: 3251-3256, 1999. (Pubitemid 29316030)
2. Mulcahy HE, Lyautey J, Lederrey C, qi Chen X, Anker P, Alstead EM, Ballinger A, Farthing MJ and Stroun M: A prospective study of K-ras mutations in the plasma of pancreatic cancer patients. Clin Cancer Res 4: 271-275, 1998.
3. Goebel G, Zitt M, Zitt M and Müller HM: Circulating nucleic acids in plasma or serum (CNAPS) as prognostic and predictive markers in patients with solid neoplasias. Dis Markers 21: 105-120, 2005. (Pubitemid 41566728)
4. Cottrell SE and Laird PW: Sensitive detection of DNA methylation. Ann N Y Acad Sci 983: 120-130, 2003.
5. Esteller M, Sanchez-Cespedes M, Rosell R, Sidransky D, Baylin SB and Herman JG: Detection of aberrant promoter hypermethylation of tumor suppressor genes in serum DNA from non-small cell lung cancer patients. Cancer Res 59: 67-70, 1999. (Pubitemid 29062958)
6. 23: 4198-4208, 2004.
7. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, Lee KY, Nomura S, Lee CW, Han SB, Kim HM, Kim WJ, Yamamoto H, Yamashita N, Yano T, Ikeda T, Itohara S, Inazawa J, Abe T, Hagiwara A, Yamagishi H, Ooe A, Kaneda A, Sugimura T, Ushijima T, Bae SC and Ito Y: Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109: 113-124, 2002.
8. Yanada M, Yaoi T, Shimada J, Sakakura C, Nishimura M, Ito K, Terauchi K, Nishiyama K, Itoh K and Fushiki S: Frequent hemizygous deletion at 1p36 and hypermethylation downregulate RUNX3 expression in human lung cancer cell lines. Oncol Rep 14: 817-822, 2005.
9. Sakakura C, Miyagawa K, Fukuda KI, Nakashima S, Yoshikawa T, Kin S, Nakase Y, Ida H, Yazumi S, Yamagishi H, Okanoue T, Chiba T, Ito K, Hagiwara A and Ito Y: Frequent silencing of RUNX3 in esophageal squamous cell carcinomas is associated with radioresistance and poor prognosis. Oncogene 26: 5927-5938, 2007.
10. Miyagawa K, Sakakura C, Nakashima S, Yoshikawa T, Kin S, Nakase Y, Ito K, Yamagishi H, Ida H, Yazumi S, Chiba T, Ito Y and Hagiwara A: Down-regulation of RUNX1, RUNX3 and CBFbeta in hepatocellular carcinomas in an early stage of hepatocarcinogenesis. Anticancer Res 26: 3633-3643, 2006.
11. Tan SH, Ida H, Lau QC, Goh BC, Chieng WS, Loh M and Ito Y: Detection of promoter hypermethylation in serum samples of cancer patients by methylation-specific polymerase chain reaction for tumour suppressor genes including RUNX3. Oncol Rep 18: 1225-1230, 2007.
12. Issa JP: CpG island methylator phenotype in cancer. Nat Rev Cancer 4: 988-993, 2004.
13. Wong JJ, Hawkins NJ and Ward RL: Colorectal cancer: a model for epigenetic tumorigenesis. Gut 56: 140-148, 2007. (Pubitemid 46044900)
14. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB and Issa JP: CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 96: 8681-8686, 1999. (Pubitemid 29354851)
15. Grady WM: CIMP and colon cancer gets more complicated. Gut 56: 1498-1500, 2007.
16. Toyota M, Ohe-Toyota M, Ahuja N and Issa JP: Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. Proc Natl Acad Sci USA 97: 710-715, 2000. (Pubitemid 30070374)
17. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, Faasse MA, Kang GH, Widschwendter M, Weener D, Buchanan D, Koh H, Simms L, Barker M, Leggett B, Levine J, Kim M, French AJ, Thibodeau SN, Jass J, Haile R and Laird PW: CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38: 787-793, 2006.
18. Jass JR: Towards a molecular classification of colorectal cancer. Int J Colorectal Dis 14: 194-200, 1999. (Pubitemid 30000267)
19. Gryfe R and Gallinger S: Microsatellite instability, mismatch repair deficiency, and colorectal cancer. Surgery 130: 17-21, 2001.
20. Goel A, Arnold CN and Boland CR: Multistep progression of colorectal cancer in the setting of microsatellite instability: new details and novel insights. Gastroenterology 121: 1497-1502, 2001.
21. Feeley KM, Fullard JF, Heneghan MA, Smith T, Maher M, Murphy RP and O'Gorman TA: Microsatellite instability in sporadic colorectal carcinoma is not an indicator of prognosis. J Pathol 188: 14-17, 1999. (Pubitemid 29197308)
22. Salahshor S, Kressner U, Fischer H, Lindmark G, Glimelius B, Påhlman L and Lindblom A: Microsatellite instability in sporadic colorectal cancer is not an independent prognostic factor. Br J Cancer 81: 190-193, 1999. (Pubitemid 29423694)
23. Sakakura C, Hamada T, Miyagawa K, Nishio M, Miyashita A, Nagata H, Ida H, Yazumi S, Otsuji E, Chiba T, Ito K and Ito Y: Quantitative analysis of tumor-derived methylated RUNX3 sequences in the serum of gastric cancer patients. Anticancer Res 29: 2619-2625, 2009.
24. Boland CR, Thibodeau SN, Hamilton SR, Sidransky D, Eshelman JR, Burt RW, Meltzer SJ, Rodriguez-Bigas MA, Fodde R, Ranzani GN and Srivastava S: A National Cancer Institute workshop on microsatellite instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer. Cancer Res 58: 5248-5257, 1998.
25. Pisani P, Parkin DM and Ferlay J: Estimates of the worldwide mortality from eighteen major cancers in 1985. Implications for prevention and projections of future burden. Int J Cancer 55: 891-903, 1993.
26. Research Group for Population-Based Cancer Registration in Japan: Cancer incidence in Japan in 1990: estimates based on data from population-based cancer registries. Jpn J Clin Oncol 28: 450-453, 1998.
27. Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AM and Bos JL: Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532, 1998.
28. Yashiro M, Carethers JM, Laghi L, Saito K, Slezak P, Jaramillo E, Rubio C, Koizumi K, Hirakawa K and Boland CR: Genetic pathways in the evolution of morphologically distinct colorectal neoplasms. Cancer Res 61: 2676-2683, 2001.
29. Huang F, Hsu S, Yan Z, Winawer S and Friedman E: The capacity for growth stimulation by TGF beta 1 seen only in advanced colon cancers cannot be ascribed to mutations in APC, DCC, p53 or RAS. Oncogene 9: 3701-3706, 1994. (Pubitemid 24359410)
30. Bubb VJ, Curtis LJ, Cunningham C, Dunlop MG, Carothers AD, Morris RG, White S, Bird CC and Wyllie AH: Microsatellite instability and the role of hMSH2 in sporadic colorectalcancer. Oncogene 12: 2641-2649, 1996. (Pubitemid 26237793)
31. Gafà R, Maestri I, Matteuzzi M, Santini A, Ferretti S, Cavazzini L and Lanza G: Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability. Cancer 89: 2025-2037, 2000.
32. Ushijima T, Nakajima T and Maekita T: DNA methylation as a marker for the past and future. J Gastroenterol 41: 401-407, 2006. (Pubitemid 43941905)
33. Graziano F, Humar B and Guilford P: The role of the E-cadherin gene (CDH1) in diffuse gastric cancer susceptibility: from the laboratory to clinical practice. Ann Oncol 14: 1705-1713, 2003. (Pubitemid 38029040)
34. Shi H, Wang MX and Caldwell CW: CpG islands: their potential as biomarkers for cancer. Expert Rev Mol Diagn 7: 519-531, 2007. (Pubitemid 47547720)
35. Fackler MJ, McVeigh M, Mehrotra J, Blum MA, Lange J, Lapides A, Garrett E, Argani P and Sukumar S: Quantitative multiplex methylation-specific PCR assay for the detection of promoter hypermethylation in multiple genes in breast cancer. Cancer Res 64: 4442-4452, 2004. (Pubitemid 38856915)
36. Ogino S, Kawasaki T, Kirkner GJ, Kraft P, Loda M and Fuchs CS: Evaluation of markers for CpG island methylator phenotype (CIMP) in colorectal cancer by a large population-based sample. J Mol Diagn 9: 305-314, 2007. (Pubitemid 47305066)
37. Sakakura C, Hasegawa K, Miyagawa K, Nakashima S, Yoshikawa T, Kin S, Nakase Y, Yazumi S, Yamagishi H, Okanoue T, Chiba T and Hagiwara A: Possible involvement of RUNX3 silencing in the peritoneal metastases of gastric cancers. Clin Cancer Res 11: 6479-6488, 2005.
38. Wada M, Yazumi S, Takaishi S, Hasegawa K, Sawada M, Tanaka H, Ida H, Sakakura C, Ito K, Ito Y and Chiba T: Frequent loss of RUNX3 gene expression in human bile duct and pancreatic cancer cell lines. Oncogene 23: 2401-2407, 2004.
39. Hasegawa K, Yazumi S, Wada M, Sakurai T, Kida M, Yamauchi J, Hisatsune H, Tada S, Ida H, Nakase Y, Sakakura C, Hagiwara A and Chiba T: Restoration of RUNX3 enhances transforming growth factor-beta-dependent p21 expression in a biliary tract cancer cell line. Cancer Sci 98: 838-843, 2007.
40. Ito K, Lim AC, Salto-Tellez M, Motoda L, Osato M, Chuang LS, Lee CW, Voon DC, Koo JK, Wang H, Fukamachi H and Ito Y: RUNX3 attenuates beta-catenin/T-cell factors in intestinal tumorigenesis. Cancer Cell 14: 226-237, 2008.
41. Soong R, Shah N, Peh BK, Chong PY, Ng SS, Zeps N, Joseph D, Salto-Tellez M, Iacopetta B and Ito Y: The expression of RUNX3 in colorectal cancer is associated with disease stage and patient outcome. Br J Cancer 100: 676-679, 2009.
42. Ku JL, Kang SB, Shin YK, Kang HC, Hong SH, Kim IJ, Shin JH, Han IO and Park JG: Promoter hypermethylation downregulates RUNX3 gene expression in colorectal cancer cell lines. Oncogene 23: 6736-6742, 2004. (Pubitemid 39280005)
43. Lee S, Cho N, Choi M, Yoo EJ, Kim JH and Kang GH: Clinicopathological features of CpG island methylator phenotype-positive colorectal cancer and its adverse prognosis in relation to KRAS/BRAF mutation. Pathology Int 58: 104-113, 2008.
44. Cunningham JM, Christensen ER, Tester DJ, Kim CY, Roche PC, Burgart LJ and Thibodeau SN: Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. Cancer Res 58: 3455-3460, 1998.
45. Herfarth KK, Kodner IJ, Whelan AJ, Ivanovich JL, Bracamontes JR, Wells SA Jr and Goodfellow PJ: Mutations in MLH1 are more frequent than in MSH2 in sporadic colorectal cancers with microsatellite instability. Genes Chromosomes Cancer 18: 42-49, 1997.
46. Gafà R, Maestri I, Matteuzzi M, Santini A, Ferretti S, Cavazzini L and Lanza G: Sporadic colorectal adenocarcinomas with high-frequency microsatellite instability. Cancer 89: 2025-2037, 2000.
47. Wright CM, Dent OF, Barker M, Newland RC, Chapuis PH, Bokey EL, Young JP, Leggett BA, Jass JR and Macdonald GA: Prognostic significance of extensive microsatellite instability in sporadic clinicopathological stage C colorectal cancer. Br J Surg 87: 1197-1202, 2000.
48. Goel A, Arnold CN, Tassone P, Chang DK, Niedzwiecki D, Dowell JM, Wasserman L, Compton C, Mayer RJ, Bertagnolli MM and Boland CR: Epigenic inactivation of RUNX3 in microsatellite unstable sporadic colon cancers. Int J Cancer 112: 754-759, 2004.
49. Hiramatsu T, Osaki M, Ito Y, Tanji Y, Tokuyasu N and Ito H: Expression of RUNX3 protein in human esophageal mucosa and squamous cell carcinoma. Pathobiology 72: 316-324, 2005.
50. Araki K, Osaki M, Nagahama Y, Hiramatsu T, Nakamura H, Ohgi S and Ito H: Expression of RUNX3 protein in human lung adenocarcinoma: implications for tumor progression and prognosis. Cancer Sci 96: 227-231, 2005. (Pubitemid 40767060)
51. Wei D, Gong W, Oh SC, Li Q, Kim WD, Wang L, Le X, Yao J, Wu TT, Huang S and Xie K: Loss of RUNX3 expression significantly affects the clinical outcome of gastric cancer patients and its restoration causes drastic suppression of tumor growth and metastasis. Cancer Res 65: 4809-4816, 2005.
52. Jiang Y, Tong D, Lou G, Zhang Y and Geng J: Expression of RUNX3 gene, methylation status and clinicopathological significance in breast cancer and breast cancer cell lines. Pathobiology 75: 244-251, 2008. (Pubitemid 351918429)
53. Nomoto S, Kinoshita T, Mori T, Kato K, Sugimoto H, Kanazumi N, Takeda S and Nakao A: Adverse prognosis of epigenetic inactivation in RUNX3 gene at 1p36 in human pancreatic cancer. Br J Cancer 98: 1690-1695, 2008. (Pubitemid 351684677)
54. Hsu PI, Hsieh HL, Lee J, Lin LF, Chen HC, Lu PJ and Hsiao M: Loss of RUNX3 expression correlates with differentiation, nodal metastasis, and poor prognosis of gastric cancer. Ann Surg Oncol 16: 1686-1694, 2009.
55. Soong R, Shah N, Peh BK, Chong PY, Ng SS, Zeps N, Joseph D, Salto-Tellez M, Iacopetta B and Ito Y: The expression of RUNX3 in colorectal cancer is associated with disease stage and patient outcome. Br J Cancer 100: 676-679, 2009.
56. Yamamoto H, Miyake Y, Noura S, Ogawa M, Yasui M, Ikenaga M, Sekimoto M and Monden M: Tumor marker for colorectal cancer. Gan To Kagaku Ryoho 28: 1299-1305, 2001 (in Japanese).
57. Zamcheck N, Doos WG, Prudente R, Lurie BB and Gottlieb LS: Prognostic factors in colon carcinoma: correlation of serum carcinoembryonic antigen level and tumor histopathology. Hum Pathol 6: 31-45, 1975.