Methylation of the Claudin 1 Promoter Is Associated with Loss of Expression in Estrogen Receptor Positive Breast Cancer

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Di Cello, Francescopaolo ^a   Cope, Leslie ^a   Li, Huili ^a   Jeschke, Jana ^a   Wang, Wei ^a   Baylin, Stephen B ^a   Zahnow, Cynthia A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; ESTROGEN RECEPTOR;

ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR SUPPRESSOR GENE; UPREGULATION;

EID: 84879741034     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068630     Document Type: Article

References (39)

1. Gupta IR, Ryan AK, (2010) Claudins: Unlocking the code to tight junction function during embryogenesis and in disease. Clin Genet 77: 314-325. doi:10.1111/j.1399-0004.2010.01397.x. PubMed: 20447145.
2. Myal Y, Leygue E, Blanchard AA, (2010) Claudin 1 in breast tumorigenesis: Revelation of a possible novel "claudin high" subset of breast cancers. J Biomed Biotechnol: pp. 2010: 956897.
3. Turksen K, Troy TC, (2011) Junctions gone bad: Claudins and loss of the barrier in cancer. Biochim Biophys Acta 1816: 73-79. PubMed: 21515339.
4. Saitou M, Fujimoto K, Doi Y, Itoh M, Fujimoto T, et al. (1998) Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J Cell Biol 141: 397-408. doi:10.1083/jcb.141.2.397. PubMed: 9548718.
5. Furuse M, Sasaki H, Fujimoto K, Tsukita S, (1998) A single gene product, claudin-1 or-2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143: 391-401. doi:10.1083/jcb.143.2.391. PubMed: 9786950.
6. Mineta K, Yamamoto Y, Yamazaki Y, Tanaka H, Tada Y, et al. (2011) Predicted expansion of the claudin multigene family. FEBS Lett 585: 606-612. doi:10.1016/j.febslet.2011.01.028. PubMed: 21276448.
7. Lu S, Singh K, Mangray S, Tavares R, Noble L, et al. (2013) Claudin expression in high-grade invasive ductal carcinoma of the breast: Correlation with the molecular subtype. Mod Pathol 26: 485-495. doi:10.1038/modpathol.2012.187. PubMed: 23222490.
8. Blanchard AA, Skliris GP, Watson PH, Murphy LC, Penner C, et al. (2009). Claudins 13 and 4 protein expression in ER negative breast cancer correlates with markers of the basal phenotype. Virchows Arch 454: 647-656.
9. Tokés AM, Kulka J, Paku S, Szik A, Páska C, et al. (2005) Claudin-1,-3 and-4 proteins and mRNA expression in benign and malignant breast lesions: A research study. Breast Cancer Res 7: R296-R305. doi:10.1186/bcr983. PubMed: 15743508.
10. Krämer F, White K, Kubbies M, Swisshelm K, Weber BH, (2000) Genomic organization of claudin-1 and its assessment in hereditary and sporadic breast cancer. Hum Genet 107: 249-256. doi:10.1007/s004390000375. PubMed: 11071387.
11. Gerhard R, Ricardo S, Albergaria A, Gomes M, Silva AR, et al. (2012) Immunohistochemical features of claudin-low intrinsic subtype in metaplastic breast carcinomas. Breast 21: 354-360. doi:10.1016/j.breast.2012.03.001. PubMed: 22464177.
12. Morohashi S, Kusumi T, Sato F, Odagiri H, Chiba H, et al. (2007) Decreased expression of claudin-1 correlates with recurrence status in breast cancer. Int J Mol Med 20: 139-143. PubMed: 17611630.
13. Szasz AM, Tokes AM, Micsinai M, Krenacs T, Jakab C, et al. (2011) Prognostic significance of claudin expression changes in breast cancer with regional lymph node metastasis. Clin Exp Metastasis 28: 55-63. doi:10.1007/s10585-010-9357-5. PubMed: 20963473.
14. Ricardo S, Gerhard R, Cameselle-Teijeiro JF, Schmitt F, Paredes J, (2012) Claudin expression in breast cancer: High or low, what to expect? Histol Histopathol 27: 1283-1295. PubMed: 22936447.
15. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, et al. (2007) Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 8: R76. doi:10.1186/gb-2007-8-5-r76. PubMed: 17493263.
16. Kulawiec M, Safina A, Desouki MM, Still I, Matsui S, et al. (2008) Tumorigenic transformation of human breast epithelial cells induced by mitochondrial DNA depletion. Cancer Biol Ther 7: 1732-1743. doi:10.4161/cbt.7.11.6729. PubMed: 19151587.
17. Hoevel T, Macek R, Swisshelm K, Kubbies M, (2004) Reexpression of the TJ protein CLDN1 induces apoptosis in breast tumor spheroids. Int J Cancer 108: 374-383. doi:10.1002/ijc.11571. PubMed: 14648703.
18. Jones PA, Baylin SB, (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428. PubMed: 12042769.
19. Boireau S, Buchert M, Samuel MS, Pannequin J, Ryan JL, et al. (2007) DNA-methylation-dependent alterations of claudin-4 expression in human bladder carcinoma. Carcinogenesis 28: 246-258. PubMed: 16829686.
20. Osanai M, Murata M, Chiba H, Kojima T, Sawada N, (2007) Epigenetic silencing of claudin-6 promotes anchorage-independent growth of breast carcinoma cells. Cancer Sci 98: 1557-1562. doi:10.1111/j.1349-7006.2007.00569.x. PubMed: 17645772.
21. Kominsky SL, Argani P, Korz D, Evron E, Raman V, et al. (2003) Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 22: 2021-2033. doi:10.1038/sj.onc.1206199. PubMed: 12673207.
22. Ogoshi K, Hashimoto S, Nakatani Y, Qu W, Oshima K, et al. (2011) Genome-wide profiling of DNA methylation in human cancer cells. Genomics 98: 280-287. doi:10.1016/j.ygeno.2011.07.003. PubMed: 21821115.
23. Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumours. Nature 490: 61-70.
24. Ignatoski KM, Ethier SP, (1999) Constitutive activation of pp125fak in newly isolated human breast cancer cell lines. Breast Cancer Res Treat 54: 173-182. doi:10.1023/A:1006135331912. PubMed: 10424408.
25. Debnath J, Muthuswamy SK, Brugge JS, (2003) Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30: 256-268. doi:10.1016/S1046-2023(03)00032-X. PubMed: 12798140.
26. Tsai HC, Li H, Van Neste L, Cai Y, Robert C, et al. (2012) Transient low doses of DNA-demethylating agents exert durable antitumor effects on hematological and epithelial tumor cells. Cancer Cell 21: 430-446. doi:10.1016/j.ccr.2011.12.029. PubMed: 22439938.
27. Smyth GK, Speed T, (2003) Normalization of cDNA microarray data. Methods 31: 265-273. doi:10.1016/S1046-2023(03)00155-5. PubMed: 14597310.
28. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB, (1996) Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 93: 9821-9826. doi:10.1073/pnas.93.18.9821. PubMed: 8790415.
29. Brandes JC, Carraway H, Herman JG, (2007) Optimal primer design using the novel primer design program: MSPprimer provides accurate methylation analysis of the ATM promoter. Oncogene 26: 6229-6237. doi:10.1038/sj.onc.1210433. PubMed: 17384671.
30. Martínez-Estrada OM, Cullerés A, Soriano FX, Peinado H, Bolós V, et al. (2006) The transcription factors slug and snail act as repressors of claudin-1 expression in epithelial cells. Biochem J 394: 449-457. doi:10.1042/BJ20050591. PubMed: 16232121.
31. Lewis CM, Cler LR, Bu DW, Zöchbauer-Müller S, Milchgrub S, et al. (2005) Promoter hypermethylation in benign breast epithelium in relation to predicted breast cancer risk. Clin Cancer Res 11: 166-172. PubMed: 15671542.
32. Yan PS, Venkataramu C, Ibrahim A, Liu JC, Shen RZ, et al. (2006) Mapping geographic zones of cancer risk with epigenetic biomarkers in normal breast tissue. Clin Cancer Res 12: 6626-6636. doi:10.1158/1078-0432.CCR-06-0467. PubMed: 17121881.
33. Cataldo VD, Cortes J, Quintás-Cardama A, (2009) Azacitidine for the treatment of myelodysplastic syndrome. Expert Rev Anticancer Ther 9: 875-884. doi:10.1586/era.09.61. PubMed: 19589026.
34. Saba HI, (2007) Decitabine in the treatment of myelodysplastic syndromes. Ther Clin Risk Manag 3: 807-817. PubMed: 18473005.
35. Yoo CB, Jones PA, (2006) Epigenetic therapy of cancer: Past, present and future. Nat Rev Drug Discov 5: 37-50. doi:10.1038/nrd1930. PubMed: 16485345.
36. Stresemann C, Bokelmann I, Mahlknecht U, Lyko F, (2008) Azacytidine causes complex DNA methylation responses in myeloid leukemia. Mol Cancer Ther 7: 2998-3005. doi:10.1158/1535-7163.MCT-08-0411. PubMed: 18790780.
37. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, et al. (2005) 5-aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Mol Cell Biol 25: 4727-4741. doi:10.1128/MCB.25.11.4727-4741.2005. PubMed: 15899874.
38. Stresemann C, Brueckner B, Musch T, Stopper H, Lyko F, (2006) Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines. Cancer Res 66: 2794-2800. doi:10.1158/0008-5472.CAN-05-2821. PubMed: 16510601.
39. Finn RS, Dering J, Conklin D, Kalous O, Cohen DJ, et al. (2009) PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res 11: R77. doi:10.1186/bcr2419. PubMed: 19874578.