DNA methylation analyses of the connexin gene family reveal silencing of GJC1 (Connexin45) by promoter hypermethylation in colorectal cancer

Epigenetics

Volumn 6, Issue 5, 2011, Pages 602-609

  Sirnes, Solveig ^a,b   Honne, Hilde ^a,b   Ahmed, Deeqa ^a,b   Danielsen, Stine Aske ^a,b   Rognum, Torleiv O ^b,c   Meling, Gunn Iren ^c,d   Leithe, Edward ^a,b   Rivedal, Edgar ^a,b   Lothe, Ragnhild A ^a,b   Lind, Guro E ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d AKERSHUS UNIVERSITY HOSPITAL   (Norway)

Author keywords

Cell communication; Colorectal cancer; Connexin; Epigenetics; Gap junction; GJC1; Hypermethylation

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CONNEXIN 45; DNA;

ADULT; AGED; ARTICLE; CANCER CELL CULTURE; COLORECTAL CANCER; COLORECTAL CARCINOMA; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PROMOTER REGION;

EID: 79957575641     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.5.15237     Document Type: Article

References (46)

1. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC. Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 2003; 83: 1359-400.
2. Yamasaki H, Krutovskikh V, Mesnil M, Omori Y. Connexin genes and cell growth control. Arch Toxicol Suppl 1996; 18: 105-14.
3. Wei CJ, Xu X, Lo CW. Connexins and cell signaling in development and disease. Annu Rev Cell Dev Biol 2004; 20: 811-38.
4. Evans WH, Martin PE. Gap junctions: structure and function. Mol Membr Biol 2002; 19: 121-36.
5. Sohl G, Willecke K. An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 2003; 10: 173-80.
6. Kanczuga-Koda L, Sulkowski S, Koda M, Sulkowska M. Alterations in connexin26 expression during colorectal carcinogenesis. Oncology 2005; 68: 217-22.
7. Kanczuga-Koda L, Koda M, Sulkowski S, Wincewicz A, Zalewski B, Sulkowska M. Gradual loss of functional gap junction within progression of colorectal cancer-a shift from membranous CX32 and CX43 expression to cytoplasmic pattern during colorectal carcinogenesis. In Vivo 2010; 24: 101-7.
8. Saito T, Nishimura M, Kudo R, Yamasaki H. Suppressed gap junctional intercellular communication in carcinogenesis of endometrium. Int J Cancer 2001; 93: 317-23.
9. Ozawa H, Matsunaga T, Kamiya K, Tokumaru Y, Fujii M, Tomita T, et al. Decreased expression of connexin-30 and aberrant expression of connexin-26 in human head and neck cancer. Anticancer Res 2007; 27: 2189-95.
10. Tsai H, Werber J, Davia MO, Edelman M, Tanaka KE, Melman A, et al. Reduced connexin 43 expression in high grade, human prostatic adenocarcinoma cells. Biochem Biophys Res Commun 1996; 227: 64-9.
11. Aasen T, Graham S, Edward M, Hodgins M. Reduced expression of multiple gap junction proteins is a feature of cervical dysplasia. Mol Cancer 2005; 4: 31.
12. Huang RP, Fan Y, Hossain MZ, Peng A, Zeng ZL, Boynton AL. Reversion of the neoplastic phenotype of human glioblastoma cells by connexin 43 (cx43). Cancer Res 1998; 58: 5089-96.
13. King TJ, Fukushima LH, Hieber AD, Shimabukuro KA, Sakr WA, Bertram JS. Reduced levels of connexin43 in cervical dysplasia: inducible expression in a cervical carcinoma cell line decreases neoplastic potential with implications for tumor progression. Carcinogenesis 2000; 21: 1097-109.
14. Dubina MV, Iatckii NA, Popov DE, Vasil'ev SV, Krutovskikh VA. Connexin 43, but not connexin 32, is mutated at advanced stages of human sporadic colon cancer. Oncogene 2002; 21: 4992-6.
15. Krutovskikh V, Mazzoleni G, Mironov N, Omori Y, Aguelon AM, Mesnil M, et al. Altered homologous and heterologous gap-j unctional intercellular communication in primary human liver tumors associated with aberrant protein localization but not gene mutation of connexin 32. Int J Cancer 1994; 56: 87-94.
16. Krutovskikh V, Mironov N, Yamasaki H. Human connexin 37 is polymorphic but not mutated in tumours. Carcinogenesis 1996; 17: 1761-3.
17. 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 2010.
18. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, Goldman H, et al. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 1997; 57: 808-11.
19. INK4a gene promoter hypermethylation in mucosa as a prognostic factor for patients with colorectal cancer. Mol Med 2008; 14: 412-21.
20. Esteller M, Sparks A, Toyota M, Sanchez-Cespedes M, Capella G, Peinado MA, et al. Analysis of Adenomatous Polyposis Coli promoter hypermethylation in human cancer. Cancer Res 2000; 60: 4366-71.
21. Lind GE, Ahlquist T, Kolberg M, Berg M, Eknaes M, Alonso MA, et al. Hypermethylated MAL gene-a silent marker of early colon tumorigenesis. J Transl Med 2008; 6: 13.
22. Kim M, Lee J, Sidransky D. DNA methylation markers in colorectal cancer. Cancer Metastasis Rev 2010; 29: 181-206.
23. Chen Y, Huhn D, Knosel T, Pacyna-Gengelbach M, Deutschmann N, Petersen I. Downregulation of connexin 26 in human lung cancer is related to promoter methylation. Int J Cancer 2005; 113: 14-21.
24. Hagiwara H, Sato H, Ohde Y, Takano Y, Seki T, Ariga T, et al. 5-Aza-2'-deoxycytidine suppresses human renal carcinoma cell growth in a xenograft model via upregulation of the connexin 32 gene. Br J Pharmacol 2008; 153: 1373-81.
25. Hirai A, Yano T, Nishikawa K, Suzuki K, Asano R, Satoh H, et al. Downregulation of connexin 32 gene expression through DNA methylation in a human renal cell carcinoma cell. Am J Nephrol 2003; 23: 172-7.
26. King TJ, Fukushima LH, Donlon TA, Hieber AD, Shimabukuro KA, Bertram JS. Correlation between growth control, neoplastic potential and endogenous connexin43 expression in HeLa cell lines: implications for tumor progression. Carcinogenesis 2000; 21: 311-5.
27. Piechocki MP, Burk RD, Ruch RJ. Regulation of connexin32 and connexin43 gene expression by DNA methylation in rat liver cells. Carcinogenesis 1999; 20: 401-6.
28. Tan LW, Bianco T, Dobrovic A. Variable promoter region CpG island methylation of the putative tumor suppressor gene Connexin 26 in breast cancer. Carcinogenesis 2002; 23: 231-6.
29. Yi ZC, Wang H, Zhang GY, Xia B. Downregulation of connexin 43 in nasopharyngeal carcinoma cells is related to promoter methylation. Oral Oncol 2007; 43: 898-904.
30. Borinstein SC, Conerly M, Dzieciatkowski S, Biswas S, Washington MK, Trobridge P, et al. Aberrant DNA methylation occurs in colon neoplasms arising in the azoxymethane colon cancer model. Mol Carcinog 2010; 49: 94-103.
31. Leithe E, Sirnes S, Omori Y, Rivedal E. Downregulation of gap junctions in cancer cells. Crit Rev Oncog 2006; 12: 225-56.
32. Mesnil M, Crespin S, Avanzo JL, Zaidan-Dagli ML. Defective gap junctional intercellular communication in the carcinogenic process. Biochim Biophys Acta 2005; 1719: 125-45.
33. Maxeiner S, Kruger O, Schilling K, Traub O, Urschel S, Willecke K. Spatiotemporal transcription of connexin45 during brain development results in neuronal expression in adult mice. Neuroscience 2003; 119: 689-700.
34. van Veen AA, van Rijen HV, Opthof T. Cardiac gap junction channels: modulation of expression and channel properties. Cardiovasc Res 2001; 51: 217-29.
35. Coppen SR, Dupont E, Rothery S, Severs NJ. Connexin45 expression is preferentially associated with the ventricular conduction system in mouse and rat heart. Circ Res 1998; 82: 232-43.
36. Hanner F, von MJ, Maxeiner S, Toma I, Sipos A, Kruger O, et al. Connexin45 is expressed in the juxtaglomerular apparatus and is involved in the regulation of renin secretion and blood pressure. Am J Physiol Regul Integr Comp Physiol 2008; 295: 371-80.
37. Kumai M, Nishii K, Nakamura K, Takeda N, Suzuki M, Shibata Y. Loss of connexin45 causes a cushion defect in early cardiogenesis. Development 2000; 127: 3501-12.
38. Kruger O, Plum A, Kim JS, Winterhager E, Maxeiner S, Hallas G, et al. Defective vascular development in connexin 45-deficient mice. Development 2000; 127: 4179-93.
39. Loncarek J, Yamasaki H, Levillain P, Milinkevitch S, Mesnil M. The expression of the tumor suppressor gene connexin 26 is not mediated by methylation in human esophageal cancer cells. Mol Carcinog 2003; 36: 74-81.
40. Knosel T, Emde A, Schluns K, et al. Immunoprofiles of 11 biomarkers using tissue microarrays identify prognostic subgroups in colorectal cancer. Neoplasia 2005; 7: 741-7.
41. Hong R, Lim SC. Pathological significance of connexin 26 expression in colorectal adenocarcinoma. Oncol Rep 2008; 19: 913-9.
42. Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. PNAS 2002; 99: 3740-5.
43. Chen JT, Cheng YW, Chou MC, Sen-Lin T, Lai WW, Ho WL, et al. The correlation between aberrant connexin 43 mRNA expression induced by promoter methylation and nodal micrometastasis in non-small cell lung cancer. Clin Cancer Res 2003; 9: 4200-4.
44. Jinn Y, Inase N. Connexin 43, E-cadherin, beta-catenin and ZO-1 expression and aberrant methylation of the connexin 43 gene in NSCLC. Anticancer Res 2010; 30: 2271-8.
45. Kleivi K, Teixeira MR, Eknaes M, Diep CB, Jakobsen KS, Hamelin R, et al. Genome signatures of colon carcinoma cell lines. Cancer Genet Cytogenet 2004; 155: 119-31.
46. Melki JR, Vincent PC, Clark SJ. Concurrent DNA hypermethylation of multiple genes in acute myeloid leukemia. Cancer Res 1999; 59: 3730-40.