Transcriptional implications of intragenic DNA methylation in the oestrogen receptor alpha gene in breast cancer cells and tissues

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Shenker, Natalie S ^a   Flower, Kirsty J ^a   Wilhelm Benartzi, Charlotte S ^a   Dai, Wei ^a,b   Bell, Emma ^a   Gore, Edmund ^a   Bahrawy, Mona ^a   Weaver, Gillian ^c   Brown, Robert ^a   Flanagan, James M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c QUEEN CHARLOTTE S AND CHELSEA HOSPITAL   (United Kingdom)

Author keywords

Breast cancer; Breast cancer campaign tissue bank; Breast epithelial cells; Breast milk; DNA methylation; ESR1; Intragenic

Indexed keywords

BISULFITE; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; ESTROGEN RECEPTOR ALPHA, HUMAN;

ARTICLE; BREAST CANCER; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; EPITHELIUM CELL; ESR1 GENE; GENE; GENE EXPRESSION; GENE INSERTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; PROMOTER REGION; PYROSEQUENCING; REAL TIME POLYMERASE CHAIN REACTION; TUMOR BIOPSY; TUMOR MICROENVIRONMENT; BREAST MILK; BREAST TUMOR; CYTOLOGY; DNA SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; MAMMARY GLAND; METABOLISM; PAGET NIPPLE DISEASE; TUMOR CELL LINE;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL LINE, TUMOR; DNA METHYLATION; EPIGENESIS, GENETIC; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAMMARY GLANDS, HUMAN; MILK, HUMAN; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC;

EID: 84929173797     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1335-5     Document Type: Article

References (50)

1. Benson JR, Jatoi I, Keisch M, Esteva FJ, Makris A, Jordan VC. Early breast cancer. Lancet. 2009;373(9673):1463-79.
2. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128(4):683-92.
3. Baylin SB, Esteller M, Rountree MR, Bachman KE, Schuebel K, Herman JG. Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum Mol Genet. 2001;10(7):687-92.
4. Baylin S, Herman J, Graff J, Vertino P, Issa J. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res. 1998;72:141-96.
5. Nathan D, Crothers DM. Bending and flexibility of methylated and unmethylated EcoRI DNA. J Mol Biol. 2002;316(1):7-17.
6. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet. 2009;10(5):295-304.
7. Ehrlich M, Lacey M. DNA methylation and differentiation: silencing, upregulation and modulation of gene expression. Epigenomics. 2013;5(5):553-68.
8. Blattler A, Yao L, Witt H, Guo Y, Nicolet CM, Berman BP, et al. Global loss of DNA methylation uncovers intronic enhancers in genes showing expression changes. Genome Biol. 2014;15(9):469.
9. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010;466(7303):253-7.
10. Malousi A, Kouidou S. DNA hypermethylation of alternatively spliced and repeat sequences in humans. Mol Genet Genomics. 2012;287(8):631-42.
11. Brenet F, Moh M, Funk P, Feierstein E, Viale AJ, Socci ND, et al. DNA methylation of the first exon is tightly linked to transcriptional silencing. PLoS One. 2011;6(1):e14524.
12. Cleator SJ, Ahamed E, Coombes RC, Palmieri C. A 2009 update on the treatment of patients with hormone receptor-positive breast cancer. Clin Breast Cancer. 2009;9 Suppl 1:S6-17.
13. Sorlie T, Wang Y, Xiao C, Johnsen H, Naume B, Samaha RR, et al. Distinct molecular mechanisms underlying clinically relevant subtypes of breast cancer: gene expression analyses across three different platforms. BMC Genomics. 2006;7:127.
14. Carey LA. Through a glass darkly: advances in understanding breast cancer biology, 2000-2010. Clin Breast Cancer. 2010;10(3):188-95.
15. Flanagan JM, Munoz-Alegre M, Henderson S, Tang T, Sun P, Johnson N, et al. Gene-body hypermethylation of ATM in peripheral blood DNA of bilateral breast cancer patients. Human Molecular Genetics. 2009;18(7):1332-42.
16. Zemach A, Zilberman D. Evolution of eukaryotic DNA methylation and the pursuit of safer sex. Curr Biol. 2010;20(17):R780-5.
17. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature Genetics. 2007;39(1):61-9.
18. Zemach A, McDaniel IE, Silva P, Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science. 2010;328(5980):916-9.
19. Aran D, Toperoff G, Rosenberg M, Hellman A. Replication timing-related and gene body-specific methylation of active human genes. Hum Mol Genet. 2011;20(4):670-80.
20. Tost J. DNA methylation: an introduction to the biology and the disease-associated changes of a promising biomarker. Molecular Biotechnology. 2010;44(1):71-81.
21. Royo JL, Hidalgo M, Ruiz A. Pyrosequencing protocol using a universal biotinylated primer for mutation detection and SNP genotyping. Nature Protocols. 2007;2(7):1734-9.
22. Madureira PA, Varshochi R, Constantinidou D, Francis RE, Coombes RC, Yao KM, et al. The Forkhead box M1 protein regulates the transcription of the estrogen receptor alpha in breast cancer cells. J Biol Chem. 2006;281(35):25167-76.
23. Chan TA, Glockner S, Yi JM, Chen W, Van Neste L, Cope L, et al. Convergence of mutation and epigenetic alterations identifies common genes in cancer that predict for poor prognosis. PLoS Med. 2008;5(5):e114.
24. Miranda TB, Cortez CC, Yoo CB, Liang G, Abe M, Kelly TK, et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol Cancer Ther. 2009;8(6):1579-88.
25. Feinberg A, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature. 1983;301(5895):89-92.
26. Yang X, Han H, De Carvalho DD, Lay FD, Jones PA, Liang G. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell. 2014;26(4):577-90.
27. Kulis M, Queiros AC, Beekman R, Martin-Subero JI. Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer. Biochim Biophys Acta. 2013;1829(11):1161-74.
28. Zemach A, Kim MY, Silva P, Rodrigues JA, Dotson B, Brooks MD, et al. Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA. 2010;107(43):18729-34.
29. Maunakea AK, Chepelev I, Cui K, Zhao K. Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. Cell Res. 2013;23(11):1256-69.
30. Schor IE, Fiszbein A, Petrillo E, Kornblihtt AR. Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation. Embo J. 2013;32(16):2264-74.
31. Lorincz M, Dickerson D, Schmitt M, Groudine M. Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat Struct Mol Biol. 2004;11(11):1068-75.
32. Pleyer L, Greil R. Digging deep into "dirty" drugs - modulation of the methylation machinery. Drug Metab Rev. 2015:1-28.
33. Shenker N, Flanagan JM. Intragenic DNA methylation: implications of this epigenetic mechanism for cancer research. Br J Cancer. 2012;106(2):248-53.
34. Velicescu M, Weisenberger DJ, Gonzales FA, Tsai YC, Nguyen CT, Jones PA. Cell division is required for de novo methylation of CpG islands in bladder cancer cells. Cancer Res. 2002;62(8):2378-84.
35. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, et al. Transient cyclical methylation of promoter DNA. Nature. 2008;452(7183):112-5.
36. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature. 2008;452(7183):45-50.
37. Ooi SK, Bestor TH. The colorful history of active DNA demethylation. Cell. 2008;133(7):1145-8.
38. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nature Reviews Genetics. 2002;3(6):415-28.
39. Feinberg AP, Tycko B. The history of cancer epigenetics. Nature Reviews Cancer. 2004;4(2):143-53.
40. Kanai Y. Genome-wide DNA, methylation profiles in precancerous conditions and cancers. Cancer Sci. 2010;101(1):36-45.
41. Veeck J, Esteller M. Breast cancer epigenetics: from DNA methylation to microRNAs. J Mammary Gland Biol Neoplasia. 2010;15(1):5-17.
42. Mulero-Navarro S, Esteller M. Epigenetic biomarkers for human cancer: the time is now. Crit Rev Oncol Hematol. 2008;68(1):1-11.
43. Michels KB. The promises and challenges of epigenetic epidemiology. Experimental gerontology. 2010;45(4):297-301.
44. Huang Z, Murphy SK. Increased Intragenic IGF2 Methylation is Associated with Repression of Insulator Activity and Elevated Expression in Serous Ovarian Carcinoma. Front Oncol. 2013;3:131.
45. Wild L, Flanagan JM. Genome-wide hypomethylation in cancer may be a passive consequence of transformation. Biochim Biophys Acta. 2010;1806(1):50-7.
46. Heijmans BT, Mill J. Commentary: The seven plagues of epigenetic epidemiology. Int J Epidemiol. 2012;41(1):74-8.
47. Hassiotou F, Geddes DT, Hartmann PE. Cells in human milk: state of the science. J Hum Lact. 2013;29(2):171-82.
48. Faupel-Badger JM, Arcaro KF, Balkam JJ, Eliassen AH, Hassiotou F, Lebrilla CB, et al. Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute-sponsored workshop. J Natl Cancer Inst. 2013;105(3):166-74.
49. Gur-Dedeoglu B, Konu O, Bozkurt B, Ergul G, Seckin S, Yulug IG. Identification of endogenous reference genes for qRT-PCR analysis in normal matched breast tumor tissues. Oncol Res. 2009;17(8):353-65.
50. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819-23.