Epigenetic-mediated tumor suppressor genes as diagnostic or prognostic biomarkers in gastric cancer

Expert Review of Molecular Diagnostics

Volumn 13, Issue 5, 2013, Pages 445-455

  Otani, Koji ^a,b   Li, Xiaoxing ^a   Arakawa, Tetsuo ^b   Chan, Francis K L ^a   Yu, Jun ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

ADAMTS9; BCL6B; gastric cancer; Helicobacter pylori; PCDH10; promoter methylation; RNF180; tumor suppressor gene; ZNF545

Indexed keywords

ADAMTS9 PROTEIN; BCL6B PROTEIN; CMTM3 PROTEIN; DACT1 PROTEIN; DKK3 PROTEIN; DLEC1 PROTEIN; FBLN1 PROTEIN; FBP1 PROTEIN; OPCML PROTEIN; PCDH10 PROTEIN; PROTEIN P53; RNF180 PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 2; SLC19A3 PROTEIN; TRANSCRIPTION FACTOR PAX5; TUMOR MARKER; TUMOR SUPPRESSOR PROTEIN; UCHL1 PROTEIN; UNCLASSIFIED DRUG; ZIC1 PROTEIN; ZNF331 PROTEIN; ZNF545 PROTEIN;

CANCER PROGNOSIS; CELL ADHESION; COLON CANCER; DISEASE MARKER; EPIGENETICS; GENE CONTROL; GENE SEQUENCE; GENETIC IDENTIFICATION; GENETIC SCREENING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PREDICTION; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION; STOMACH CANCER; TUMOR SUPPRESSOR GENE; UBIQUITINATION;

EARLY DETECTION OF CANCER; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HUMANS; PROGNOSIS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84879373553     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/erm.13.32     Document Type: Review

References (88)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127(12), 2893-2917 (2010).
2. Yang L. Incidence and mortality of gastric cancer in China. World J. Gastroenterol. 12(1), 17-20 (2006).
3. Leung WK, Yu J, Ng EK et al. Concurrent hypermethylation of multiple tumor-related genes in gastric carcinoma and adjacent normal tissues. Cancer 91(12), 2294-2301 (2001).
4. Toyota M, Ahuja N, Suzuki H et al. Aberrant methylation in gastric cancer associated with the CpG island methylator phenotype. Cancer Res. 59(21), 5438-5442 (1999).
5. Lee YY, Kang SH, Seo JY et al. Alterations of p16INK4A and p15INK4B genes in gastric carcinomas. Cancer 80(10), 1889-1896 (1997).
6. Li QL, Ito K, Sakakura C et al. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109(1), 113-124 (2002).
7. Ushijima T, Yamashita S. Methylationsensitive representational difference analysis (MS-RDA). Methods Mol. Biol. 507, 117-130 (2009).
8. Kaneda A, Takai D, Kaminishi M, Okochi E, Ushijima T. Methylation-sensitive representational difference analysis and its application to cancer research. Ann. NY Acad. Sci. 983, 131-141 (2003).
9. Kaneda A, Kaminishi M, Nakanishi Y, Sugimura T, Ushijima T. Reduced expression of the insulin-induced protein 1 and p41 Arp2/3 complex genes in human gastric cancers. Int. J. Cancer 100(1), 57-62 (2002).
10. Kaneda A, Wakazono K, Tsukamoto T et al. Lysyl oxidase is a tumor suppressor gene inactivated by methylation and loss of heterozygosity in human gastric cancers. Cancer Res. 64(18), 6410-6415 (2004).
11. Thu KL, Pikor LA, Kennett JY, Alvarez CE, Lam WL. Methylation analysis by DNA immunoprecipitation. J. Cell. Physiol. 222(3), 522-531 (2010).
12. Fouse SD, Nagarajan RO, Costello JF. Genome-scale DNA methylation analysis. Epigenomics 2(1), 105-117 (2010).
13. Cheng YY, Yu J, Wong YP et al. Frequent epigenetic inactivation of secreted frizzled-related protein 2 (SFRP2) by promoter methylation in human gastric cancer. Br. J. Cancer 97(7), 895-901 (2007).
14. Yu J, Tao Q, Cheung KF et al. Epigenetic identification of ubiquitin carboxylterminal hydrolase L1 as a functional tumor suppressor and biomarker for hepatocellular carcinoma and other digestive tumors. Hepatology 48(2), 508-518 (2008).
15. Cheng YY, Jin H, Liu X et al. Fibulin 1 is downregulated through promoter hypermethylation in gastric cancer. Br. J. Cancer 99(12), 2083-2087 (2008).
16. Cui Y, Ying Y, van Hasselt A et al. OPCML is a broad tumor suppressor for multiple carcinomas and lymphomas with frequently epigenetic inactivation. PLoS ONE 3(8), e2990 (2008).
17. Yu J, Tao Q, Cheng YY et al. Promoter methylation of the Wnt/beta-catenin signaling antagonist Dkk-3 is associated with poor survival in gastric cancer. Cancer 115(1), 49-60 (2009).
18. Liu X, Lam EK, Wang X et al. Promoter hypermethylation mediates downregulation of thiamine receptor SLC19A3 in gastric cancer. Tumour Biol. 30(5-6), 242-248 (2009).
19. Wang Y, Li J, Cui Y et al. CMTM3, located at the critical tumor suppressor locus 16q22.1, is silenced by CpG methylation in carcinomas and inhibits tumor cell growth through inducing apoptosis. Cancer Res. 69(12), 5194-5201 (2009).
20. Wang LJ, Jin HC, Wang X et al. ZIC1 is downregulated through promoter hypermethylation in gastric cancer. Biochem. Biophys. Res. Commun. 379(4), 959-963 (2009).
21. Ying J, Poon FF, Yu J et al. DLEC1 is a functional 3p22.3 tumour suppressor silenced by promoter CpG methylation in colon and gastric cancers. Br. J. Cancer 100(4), 663-669 (2009).
22. Yu J, Cheng YY, Tao Q et al. Methylation of protocadherin 10, a novel tumor suppressor, is associated with poor prognosis in patients with gastric cancer. Gastroenterology 136(2), 640.e1-651.e1 (2009).
23. Liu X, Wang X, Zhang J et al. Warburg effect revisited: an epigenetic link between glycolysis and gastric carcinogenesis. Oncogene 29(3), 442-450 (2010).
24. Cheung KF, Lam CN, Wu K et al. Characterization of the gene structure, functional significance, and clinical application of RNF180, a novel gene in gastric cancer. Cancer 118(4), 947-959 (2012).
25. Li X, Cheung KF, Ma X et al. Epigenetic inactivation of paired box gene 5, a novel tumor suppressor gene, through direct upregulation of p53 is associated with prognosis in gastric cancer patients. Oncogene 31(29), 3419-3430 (2012).
26. Yu J, Liang QY, Wang J et al. Zinc-finger protein 331, a novel putative tumor suppressor, suppresses growth and invasiveness of gastric cancer. Oncogene 32(3), 307-317 (2013).
27. Wang S, Cheng Y, Du W et al. Zinc-finger protein 545 is a novel tumour suppressor that acts by inhibiting ribosomal RNA transcription in gastric cancer. Gut PMID:22580414 (2012) (Epub ahead of print).
28. Du W, Wang S, Zhou Q et al. ADAMTS9 is a functional tumor suppressor through inhibiting AKT/mTOR pathway and associated with poor survival in gastric cancer. Oncogene doi:10.3410/f. 717956191.793461072 (2012) (Epub ahead of print).
29. Xu L, Li X, Chu ES et al. Epigenetic inactivation of BCL6B, a novel functional tumour suppressor for gastric cancer, is associated with poor survival. Gut 61(7), 977-985 (2012).
30. Wang S, Kang W, Go MY et al. Dapper homolog 1 is a novel tumor suppressor in gastric cancer through inhibiting the nuclear factor-B signaling pathway. Mol. Med. 18, 1402-1411 (2012).
31. Miotto E, Sabbioni S, Veronese A et al. Frequent aberrant methylation of the CDH4 gene promoter in human colorectal and gastric cancer. Cancer Res. 64(22), 8156-8159 (2004).
32. Hibi K, Kodera Y, Ito K, Akiyama S, Nakao A. Methylation pattern of CDH13 gene in digestive tract cancers. Br. J. Cancer 91(6), 1139-1142 (2004).
33. Ying J, Li H, Seng TJ et al. Functional epigenetics identifies a protocadherin PCDH10 as a candidate tumor suppressor for nasopharyngeal, esophageal and multiple other carcinomas with frequent methylation. Oncogene 25(7), 1070-1080 (2006).
34. Osaka H, Wang YL, Takada K et al. Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum. Mol. Genet. 12(16), 1945-1958 (2003).
35. Okochi-Takada E, Nakazawa K, Wakabayashi M et al. Silencing of the UCHL1 gene in human colorectal and ovarian cancers. Int. J. Cancer 119(6), 1338-1344 (2006).
36. Barberis A, Widenhorn K, Vitelli L, Busslinger M. A novel B-cell lineage-specific transcription factor present at early but not late stages of differentiation. Genes Dev. 4(5), 849-859 (1990).
37. Adams B, Dörfler P, Aguzzi A et al. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes Dev. 6(9), 1589-1607 (1992).
38. Nutt SL, Urbánek P, Rolink A, Busslinger M. Essential functions of Pax5 (BSAP) in pro-B cell development: difference between fetal and adult B lymphopoiesis and reduced V-to-DJ recombination at the IgH locus. Genes Dev. 11(4), 476-491 (1997).
39. Baumann Kubetzko FB, Di Paolo C, Maag C et al. The PAX5 oncogene is expressed in N-type neuroblastoma cells and increases tumorigenicity of a S-type cell line. Carcinogenesis 25(10), 1839-1846 (2004).
40. Meza JL, Anderson J, Pappo AS, Meyer WH; Children's Oncology Group. Analysis of prognostic factors in patients with nonmetastatic rhabdomyosarcoma treated on intergroup rhabdomyosarcoma studies III and IV: the Children's Oncology Group. J. Clin. Oncol. 24(24), 3844-3851 (2006).
41. Mhawech-Fauceglia P, Saxena R, Zhang S et al. Pax-5 immunoexpression in various types of benign and malignant tumours: a high-throughput tissue microarray analysis. J. Clin. Pathol. 60(6), 709-714 (2007).
42. Lazzi S, Bellan C, Onnis A et al. Rare lymphoid neoplasms coexpressing B-and T-cell antigens. The role of PAX-5 gene methylation in their pathogenesis. Hum. Pathol. 40(9), 1252-1261 (2009).
43. Tsuji T, Nozaki I, Miyazaki M et al. Antiproliferative activity of REIC/Dkk-3 and its significant down-regulation in nonsmall-cell lung carcinomas. Biochem. Biophys. Res. Commun. 289(1), 257-263 (2001).
44. Kurose K, Sakaguchi M, Nasu Y et al. Decreased expression of REIC/Dkk-3 in human renal clear cell carcinoma. J. Urol. 171(3), 1314-1318 (2004).
45. Nozaki I, Tsuji T, Iijima O et al. Reduced expression of REIC/Dkk-3 gene in nonsmall cell lung cancer. Int. J. Oncol. 19(1), 117-121 (2001).
46. Roman-Gomez J, Jimenez-Velasco A, Agirre X et al. Transcriptional silencing of the Dickkopfs-3 (Dkk-3) gene by CpG hypermethylation in acute lymphoblastic leukaemia. Br. J. Cancer 91(4), 707-713 (2004).
47. Kobayashi K, Ouchida M, Tsuji T et al. Reduced expression of the REIC/Dkk-3 gene by promoter-hypermethylation in human tumor cells. Gene 282(1-2), 151-158 (2002).
48. Urrutia R. KRAB-containing zinc-finger repressor proteins. Genome Biol. 4(10), 231 (2003).
49. Zeng W, Ball AR Jr, Yokomori K. HP1: heterochromatin binding proteins working the genome. Epigenetics 5(4), 287-292 (2010).
50. Cheng Y, Geng H, Cheng SH et al. KRAB zinc finger protein ZNF382 is a proapoptotic tumor suppressor that represses multiple oncogenes and is commonly silenced in multiple carcinomas. Cancer Res. 70(16), 6516-6526 (2010).
51. Pederson T. The nucleolus. Cold Spring Harb. Perspect. Biol. 3(3), pii: a000638 (2011).
52. Lo PH, Lung HL, Cheung AK et al. Extracellular protease ADAMTS9 suppresses esophageal and nasopharyngeal carcinoma tumor formation by inhibiting angiogenesis. Cancer Res. 70(13), 5567-5576 (2010).
53. Kang GH, Lee S, Kim JS, Jung HY. Profile of aberrant CpG island methylation along the multistep pathway of gastric carcinogenesis. Lab. Invest. 83(5), 635-641 (2003).
54. Sarbia M, Geddert H, Klump B, Kiel S, Iskender E, Gabbert HE. Hypermethylation of tumor suppressor genes (p16INK4A, p14ARF and APC) in adenocarcinomas of the upper gastrointestinal tract. Int. J. Cancer 111(2), 224-228 (2004).
55. To KF, Leung WK, Lee TL et al. Promoter hypermethylation of tumor-related genes in gastric intestinal metaplasia of patients with and without gastric cancer. Int. J. Cancer 102(6), 623-628 (2002).
56. Tsuchiya T, Tamura G, Sato K et al. Distinct methylation patterns of two APC gene promoters in normal and cancerous gastric epithelia. Oncogene 19(32), 3642-3646 (2000).
57. Lee TL, Leung WK, Chan MW et al. Detection of gene promoter hypermethylation in the tumor and serum of patients with gastric carcinoma. Clin. Cancer Res. 8(6), 1761-1766 (2002).
58. Leung WK, To KF, Chu ES et al. Potential diagnostic and prognostic values of detecting promoter hypermethylation in the serum of patients with gastric cancer. Br. J. Cancer 92(12), 2190-2194 (2005).
59. Ogawa M, Mizugishi K, Ishiguro A et al. Rines/RNF180, a novel RING finger gene-encoded product, is a membranebound ubiquitin ligase. Genes Cells 13(4), 397-409 (2008).
60. Reddy BA, Etkin LD, Freemont PS. A novel zinc finger coiled-coil domain in a family of nuclear proteins. Trends Biochem. Sci. 17(9), 344-345 (1992).
61. Fanelli M, Fantozzi A, De Luca P et al. The coiled-coil domain is the structural determinant for mammalian homologues of Drosophila Sina-mediated degradation of promyelocytic leukemia protein and other tripartite motif proteins by the proteasome. J. Biol. Chem. 279(7), 5374-5379 (2004).
62. Lee TH, Montalvo L, Chrebtow V, Busch MP. Quantitation of genomic DNA in plasma and serum samples: higher concentrations of genomic DNA found in serum than in plasma. Transfusion 41(2), 276-282 (2001).
63. Issa JP. Methylation and prognosis: of molecular clocks and hypermethylator phenotypes. Clin. Cancer Res. 9(8), 2879-2881 (2003).
64. Chang CC, Ye BH, Chaganti RS, Dalla-Favera R. BCL-6, a POZ/zinc-finger protein, is a sequence-specific transcriptional repressor. Proc. Natl Acad. Sci. USA 93(14), 6947-6952 (1996).
65. Okabe S, Fukuda T, Ishibashi K et al. BAZF, a novel Bcl6 homolog, functions as a transcriptional repressor. Mol. Cell. Biol. 18(7), 4235-4244 (1998).
66. Sakashita C, Fukuda T, Okabe S et al. Cloning and characterization of the human BAZF gene, a homologue of the BCL6 oncogene. Biochem. Biophys. Res. Commun. 291(3), 567-573 (2002).
67. Manders PM, Hunter PJ, Telaranta AI et al. BCL6b mediates the enhanced magnitude of the secondary response of memory CD8+ T lymphocytes. Proc. Natl Acad. Sci. USA 102(21), 7418-7425 (2005).
68. Zhang H, Okada S, Hatano M, Okabe S, Tokuhisa T. A new functional domain of Bcl6 family that recruits histone deacetylases. Biochim. Biophys. Acta 1540(3), 188-200 (2001).
69. Maekita T, Nakazawa K, Mihara M et al. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin. Cancer Res. 12(3 Pt 1), 989-995 (2006).
70. Leung WK, Man EP, Yu J et al. Effects of Helicobacter pylori eradication on methylation status of E-cadherin gene in noncancerous stomach. Clin. Cancer Res. 12(10), 3216-3221 (2006).
71. Chan AO, Peng JZ, Lam SK et al. Eradication of Helicobacter pylori infection reverses E-cadherin promoter hypermethylation. Gut 55(4), 463-468 (2006).
72. Graziano F, Humar B, Guilford P. The role of the E-cadherin gene (CDH1) in diffuse gastric cancer susceptibility: from the laboratory to clinical practice. Ann. Oncol. 14(12), 1705-1713 (2003).
73. Ushijima T, Nakajima T, Maekita T. DNA methylation as a marker for the past and future. J. Gastroenterol. 41(5), 401-407 (2006).
74. Cheng AS, Li MS, Kang W et al. Helicobacter pylori causes epigenetic dysregulation of FOXD3 to promote gastric carcinogenesis. Gastroenterology 144(1), 122.e9-133.e9 (2013).
75. Keates S, Hitti YS, Upton M, Kelly CP. Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells. Gastroenterology 113(4), 1099-1109 (1997).
76. Liu Y, Mayo MW, Nagji AS et al. Phosphorylation of RelA/p65 promotes DNMT-1 recruitment to chromatin and represses transcription of the tumor metastasis suppressor gene BRMS1. Oncogene 31(9), 1143-1154 (2012).
77. Yoo CB, Jones PA. Epigenetic therapy of cancer: past, present and future. Nat. Rev. Drug Discov. 5(1), 37-50 (2006).
78. Zhao J, Liang Q, Cheung KF et al. Genome-wide identification of Epstein-Barr virus-driven promoter methylation profiles of human genes in gastric cancer cells. Cancer 119(2), 304-312 (2012).
79. Farazi TA, Spitzer JI, Morozov P, Tuschl T. miRNAs in human cancer. J. Pathol. 223(2), 102-115 (2011).
80. Scaria V, Hariharan M, Maiti S, Pillai B, Brahmachari SK. Host-virus interaction: a new role for microRNAs. Retrovirology 3, 68 (2006).
81. Tsuchiya S, Okuno Y, Tsujimoto G. microRNA: biogenetic and functional mechanisms and involvements in cell differentiation and cancer. J. Pharmacol. Sci. 101(4), 267-270 (2006).
82. Cai Y, Yu X, Hu S, Yu J. A brief review on the mechanisms of miRNA regulation. Genomics. Proteomics Bioinformatics 7(4), 147-154 (2009).
83. Takagi T, Iio A, Nakagawa Y, Naoe T, Tanigawa N, Akao Y. Decreased expression of microRNA-143 and-145 in human gastric cancers. Oncology 77(1), 12-21 (2009).
84. Du Y, Xu Y, Ding L et al. Down-regulation of miR-141 in gastric cancer and its involvement in cell growth. J. Gastroenterol. 44(6), 556-561 (2009).
85. Zhang Y, Guo J, Li D et al. Downregulation of miR-31 expression in gastric cancer tissues and its clinical significance. Med. Oncol. 27(3), 685-689 (2010).
86. Xiao B, Guo J, Miao Y et al. Detection of miR-106a in gastric carcinoma and its clinical significance. Clin. Chim. Acta 400(1-2), 97-102 (2009).
87. Liu T, Tang H, Lang Y, Liu M, Li X. microRNA-27a functions as an oncogene in gastric adenocarcinoma by targeting prohibitin. Cancer Lett. 273(2), 233-242 (2009).
88. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell 150(1), 12-27 (2012).