Epigenetic changes induced by oxidative stress in colorectalcancer cells: Methylation of tumor suppressor RUNX3

Tumor Biology

Volumn 33, Issue 2, 2012, Pages 403-412

  Kang, Kyoung Ah ^a   Zhang, Rui ^b   Kim, Gi Young ^c   Bae, Suk Chul ^d   Hyun, Jin Won ^b  

^a Korea Institute of Radiation and Medical Science   (South Korea)

^b Jeju National University School of Medicine   (South Korea)

^c Jeju National University   (South Korea)

^d Chungbuk National University   (South Korea)

Author keywords

Colorectal cancer; Epigenetic alteration; Reactive oxygen species; Runt domain transcription factor 3; Tumor suppressor gene

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ACETYLCYSTEINE; DNA METHYLTRANSFERASE 1; HISTONE DEACETYLASE 1; HYDROGEN PEROXIDE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR RUNX3; CYTOSINE; DNA (CYTOSINE 5 ) METHYLTRANSFERASE 1; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; RUNX3 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CELL NUCLEUS; CELL STRESS; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INDUCTION; EPIGENETICS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; CELL STRAIN CACO 2; CHEMISTRY; COLORECTAL TUMOR; DNA METHYLATION; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; METABOLISM; METHODOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

CACO-2 CELLS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; CORE BINDING FACTOR ALPHA 3 SUBUNIT; CYTOSINE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HISTONE DEACETYLASE 1; HUMANS; HYDROGEN PEROXIDE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84860269756     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-012-0322-6     Document Type: Article

References (61)

1. Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat Rev Cancer. 2003;3:276-85.
2. Filomeno G, Rotilio G, Ciriolo MR. Disulfide relays and phosphorylative cascades: partners in redox-mediated signaling pathways. Cell Death Differ. 2005;12:1555-63.
3. Ballestar E, Paz MF, Valle L, Wei S, Fraga MF, Espada J, et al. Methyl-CpG binding proteins identify novel sites of epigenetic inactivation in human cancer. EMBO J. 2003;22:6335-45.
4. Cedar H. DNA methylation and gene activity. Cell. 1988;53:3-4.
5. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128:683-92.
6. Esteller M. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene. 2002;21:5427-40.
7. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med. 2003;349:2042-54.
8. Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J. Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem. 2004;266:37-56.
9. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160:1-40.
10. Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK, et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology. 2008;135:2128-40.
11. Bae SC, Choi JK. Tumor suppressor activity of RUNX3. Oncogene. 2004;23:4336-40.
12. Hiramatsu T, Osaki M, Ito Y, Tanji Y, Tokuyasu N, Ito H. Expression of RUNX3 protein in human esophageal mucosa and squamous cell carcinoma. Pathobiology. 2005;72:316-24.
13. Oshimo Y, Oue N, Mitani Y, Nakayama H, Kitadai Y, Yoshida K, et al. Frequent loss of RUNX3 expression by promoter hypermethylation in gastric carcinoma. Pathobiology. 2004;71:137-43.
14. Subramaniam MM, Chan JY, Yeoh GK, Quek T, Ito K, Salto- Tellez M. Molecular pathology of RUNX3 in human carcinogenesis. Biochim Biophys Acta. 2009;1796:315-31.
15. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, et al. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell. 2002;109:113-24.
16. Inoue K, Ozaki S, Shiga T, Ito K, Masuda T, Okado N, et al. Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat Neurosci. 2002;5:946-54.
17. Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R, et al. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J. 2002;21:3454-63.
18. Taniuchi I, Osato M, Egawa T, Sunshine MJ, Bae SC, Komori T, et al. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell. 2002;111:621-33.
19. Kim TY, Lee HJ, Hwang KS, Lee M, Kim JW, Bang YJ, et al. Methylation of RUNX3 in various types of human cancers and premalignant stages of gastric carcinoma. Lab Invest. 2004;84:479-84.
20. Nakase Y, Sakakura C, Miyagawa K, Kin S, Fukuda K, Yanagisawa A, et al. Frequent loss of RUNX3 gene expression in remnant stomach cancer and adjacent mucosa with special reference to topography. Br J Cancer. 2005;92:562-9.
21. Ito K, Liu Q, Salto-TellezM, Yano T, Tada K, Ida H, et al. RUNX3, a novel tumor suppressor, is frequently inactivated in gastric cancer by protein mislocalization. Cancer Res. 2005;65:7743-50.
22. Lau QC, Raja E, Salto-Tellez M, Liu Q, Ito K, Inoue M, et al. RUNX3 is frequently inactivated by dual mechanisms of protein mislocalization and promoter hypermethylation in breast cancer. Cancer Res. 2006;66:6512-20.
23. Subramaniam MM, Chan JY, Soong R, Ito K, Ito Y, Yeoh KG, et al. RUNX3 inactivation by frequent promoter hypermethylation and protein mislocalization constitute an early event in breast cancer progression. Breast Cancer Res Treat. 2009;113:113-21.
24. Subramaniam MM, Chan JY, Soong R, Ito K, Yeoh KG, Wong R, et al. RUNX3 inactivation in colorectal polyps arising through different pathways of colonic carcinogenesis. Am J Gastroenterol. 2009;104:426-36.
25. Ito K, Lim AC, Salto-Tellez M, Motoda L, Osato M, Chuang LS, et al. RUNX3 attenuates beta-catenin/T cell factors in intestinal tumorigenesis. Cancer Cell. 2008;14:226-37.
26. Blau S, Rubistein A, Bass P, Singaram C, Kohen R. Differences in the reducing power along the rat GI tract: lower antioxidant capacity of the colon. Mol Cell Biochem. 1999;194:185-91.
27. Hendricks CW, Kelly RW, Radley S, Donovan IA, Keighley MR, Neoptolemis JP. Lipid peroxidation and prostaglandins in colorectal cancer. British J of Surg. 1994;81:1219-23.
28. Van Driel BE, Lyon H, Hoogenraad DC, Anten S, Hansen U, Van Noorden CJ. Expression of CuZn- and Mn-superoxide dismutase in human colorectal neoplasms. Free Radic Biol Med. 1997;23:435-44.
29. Benhar M, Engelberg D, Levitzki A. ROS, stress-activated kinases and stress-signaling in cancer. EMBO Reports. 2002;3:420-5.
30. Skrzydlewska E, Sulkowski S, Koda M, Zalewski B, Kanczuga- Koda L, Sulkowska M. Lipid peroxidation and antioxidant status in colorectal cancer. World J Gastroenterol. 2005;11:403-6.
31. Chen JC, Huang KC, Lin WW. HMG-CoA reductase inhibitors upregulate heme oxygenase-1 expression in murine RAW264.7 macrophages via ERK, p38 MAPK and protein kinase G pathways. Cell Signal. 2006;18:32-9.
32. Ku JL, Kang SB, Shin YK, Kang HC, Hong SH, Kim IJ, et al. Promoter hypermethylation downregulates RUNX3 gene expression in colorectal cancer cell lines. Oncogene. 2004;23:6736-42.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402-8.
34. Lee SH, Kim J, Kim WH, Lee YM. Hypoxic silencing of tumor suppressor RUNX3 by histone modification in gastric cancer cells. Oncogene. 2009;28:184-94.
35. Kondo Y, Shen L, Issa JP. Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol Cell Biol. 2003;23:206-15.
36. Soong R, Shah N, Peh BK, Chong PY, Ng SS, Zeps N, et al. The expression of RUNX3 in colorectal cancer is associated with disease stage and patient outcome. Br J Cancer. 2009;100:676-9.
37. Kang DH. Oxidative stress, DNA damage, and breast cancer. AACN Clinical Issues. 2002;13:540-9.
38. Arsova-Sarafinovska Z, Eken A, Matevska N, Erdem O, Sayal A, Savaser A, et al. Increased oxidative/nitrosative stress and decreased antioxidant enzyme activities in prostate cancer. Clin Biochem. 2009;42:1228-35.
39. Lawless MW, O'Byrne KJ, Gray SG. Oxidative stress induced lung cancer and COPD: opportunities for epigenetic therapy. J Cell Mol Med. 2009;13:2800-21.
40. Fahrner JA, Eguchi S, Herman JG, Baylin SB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res. 2002;62:7213-8.
41. Li QL, Kim HR, Kim WJ, Choi JK, Lee YH, Kim HM, et al. Transcriptional silencing of the RUNX3 gene by CpG hypermethylation is associated with lung cancer. Biochem Biophys Res Commun. 2004;314:223-8.
42. Melki JR, Vincent PC, Brown RD, Clark SJ. Hypermethylation of E-cadherin in leukemia. Blood. 2000;95:3208-13.
43. Trojan J, Brieger A, Raedle J, Esteller M, Zeuzem S. 5'-CpG island methylation of the LKB1/STK11 promoter and allelic loss at chromosome 19p13.3 in sporadic colorectal cancer. Gut. 2000;47:272-6.
44. Esteller M, Fraga MF, Guo M, Garcia-Foncillas J, Hedenfalk I, Godwin AK. DNA methylation patterns in hereditary human cancers mimic sporadic tumorigenesis. Hum Mol Genet. 2001;10:3001-7.
45. Song SH, Jong HS, Choi HH, Inoue H, Tanabe T, Kim NK, et al. Transcriptional silencing of cyclooxygenase-2 by hypermethylation of the 5' CpG island in human gastric carcinoma cells. Cancer Res. 2001;61:4628-35.
46. Zöchbauer-Müller S, Fong KM, Maitra A, Lam S, Geradts J, Ashfaq R, et al. 5' CpG island methylation of the FHIT gene is correlated with loss of gene expression in lung and breast cancer. Cancer Res. 2001;61:3581-5.
47. Ku JL, Yoon KA, Kim IJ, Kim WH, Jang JY, Suh KS, et al. Establishment and characterisation of six human biliary tract cancer cell lines. Br J Cancer. 2002;87:187-93.
48. Suh ER, Ha CS, Rankin EB, Toyota M, Traber PG. DNA methylation down-regulates CDX1 gene expression in colorectal cancer cell lines. J Biol Chem. 2002;277:35759-800.
49. van Engeland M, Roemen GM, Brink M, Pachen MM, Weijenberg MP, de Bruïne AP, et al. K-ras mutations and RASSF1A promoter methylation in colorectal cancer. Oncogene. 2002;21:3792-5.
50. Yang Q, Nakamura M, Nakamura Y, Yoshimura G, Suzuma T, Umemura T, et al. Two-hit inactivation of FHIT by loss of heterozygosity and hypermethylation in breast cancer. Clin Cancer Res. 2002;8:2890-3.
51. Di Vinci A, Infusini E, Nigro S, Monaco R, Giaretti W. Intratumor distribution of 1p deletions in human colorectal adenocarcinoma is commonly homogeneous: indirect evidence of early involvement in colorectal tumorigenesis. Cancer. 1998;83:415-22.
52. Di Vinci A, Infusini E, Peveri C, Sciutto A, Geido E, Risio M, et al. Correlation between 1p deletions and aneusomy in human colorectal adenomas. Int J Cancer. 1998;75:45-50.
53. Tanaka K, Yanoshita R, Konishi M, Oshimura M, Maeda Y, Mori T, et al. Suppression of tumourigenicity in human colon carcinoma cells by introduction of normal chromosome 1p36 region. Oncogene. 1993;8:2253-8.
54. Praml C, Finke LH, Herfarth C, Schlag P, Schwab M, Amler L. Deletion mapping defines different regions in 1p34.2-pter that may harbor genetic information related to human colorectal cancer. Oncogene. 1995;11:1357-62.
55. Ogunbiyi OA, Goodfellow PJ, Gagliardi G, Swanson PE, Birnbaum EH, Fleshman JW, et al. Prognostic value of chromosome 1p allelic loss in colon cancer. Gastroenterology. 1997;113:761-6.
56. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer? A mechanism for early oncogenic pathway addiction? Nat Rev Cancer. 2006;6:107-16.
57. Pradhan S, Bacolla A, Wells RD, Roberts RJ. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J Biol Chem. 1999;274:33002-10.
58. Bestor TH, The DNA. methyltransferases of mammals. Hum Mol Genet. 2000;92:395-402.
59. Rountree MR, Bachman KE, Herman JG, Baylin SB. DNA methylation, chromatin inheritance, and cancer. Oncogene. 2001;20:3156-65.
60. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet. 2000;24:88-91.
61. Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev. 2005;15:490-538.