Skip to main content
Top
Published in: Breast Cancer Research 3/2013

01-06-2013 | Review

DNA methylation in ductal carcinoma in situof the breast

Authors: Jia-Min B Pang, Alexander Dobrovic, Stephen B Fox

Published in: Breast Cancer Research | Issue 3/2013

Login to get access

Abstract

Ductal carcinoma in situ (DCIS) is a non-obligate precursor lesion of invasive carcinoma of the breast. Current prognostic markers based on histopathological examination are unable to accurately predict which DCIS cases will progress to invasive carcinoma or recur after surgical excision. Epigenetic changes have been shown to be a significant driver of tumorigenesis, and DNA methylation of specific gene promoters provides predictive and prognostic markers in many types of cancer, including invasive breast cancer. In general, the spectrum of genes that are methylated in DCIS strongly resembles that seen in invasive ductal carcinoma. The identification of specific prognostic markers in DCIS remains elusive and awaits additional work investigating a large panel of methylatable genes by using sensitive and reproducible technologies. This review critically appraises the role of methylation in DCIS and its use as a biomarker.
Appendix
Available only for authorised users
Literature
1.
go back to reference Virnig BA, Tuttle TM, Shamliyan T, Kane RL: Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J Natl Cancer Inst. 2010, 102: 170-178. 10.1093/jnci/djp482.PubMedCrossRef Virnig BA, Tuttle TM, Shamliyan T, Kane RL: Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J Natl Cancer Inst. 2010, 102: 170-178. 10.1093/jnci/djp482.PubMedCrossRef
2.
go back to reference EORTC Breast Cancer Cooperative Group, EORTC Radiotherapy Group, Bijker N, Meijnen P, Peterse JL, Bogaerts J, Van Hoorebeeck I, Julien JP, Gennaro M, Rouanet P, Avril A, Fentiman IS, Bartelink H, Rutgers EJ: Breast-conserving treatment with or without radiotherapy in ductal carcinoma-in-situ: tenyear results of European Organisation for Research and Treatment of Cancer randomized phase III trial 10853--a study by the EORTC Breast Cancer Cooperative Group and EORTC Radiotherapy Group. J Clin Oncol. 2006, 24: 3381-3387. 10.1200/JCO.2006.06.1366.CrossRef EORTC Breast Cancer Cooperative Group, EORTC Radiotherapy Group, Bijker N, Meijnen P, Peterse JL, Bogaerts J, Van Hoorebeeck I, Julien JP, Gennaro M, Rouanet P, Avril A, Fentiman IS, Bartelink H, Rutgers EJ: Breast-conserving treatment with or without radiotherapy in ductal carcinoma-in-situ: tenyear results of European Organisation for Research and Treatment of Cancer randomized phase III trial 10853--a study by the EORTC Breast Cancer Cooperative Group and EORTC Radiotherapy Group. J Clin Oncol. 2006, 24: 3381-3387. 10.1200/JCO.2006.06.1366.CrossRef
3.
go back to reference Fisher B, Dignam J, Wolmark N, Wickerham DL, Fisher ER, Mamounas E, Smith R, Begovic M, Dimitrov NV, Margolese RG, Kardinal CG, Kavanah MT, Fehrenbacher L, Oishi RH: Tamoxifen in treatment of intraductal breast cancer: National Surgical Adjuvant Breast and Bowel Project B-24 randomised controlled trial. Lancet. 1999, 353: 1993-2000. 10.1016/S0140-6736(99)05036-9.PubMedCrossRef Fisher B, Dignam J, Wolmark N, Wickerham DL, Fisher ER, Mamounas E, Smith R, Begovic M, Dimitrov NV, Margolese RG, Kardinal CG, Kavanah MT, Fehrenbacher L, Oishi RH: Tamoxifen in treatment of intraductal breast cancer: National Surgical Adjuvant Breast and Bowel Project B-24 randomised controlled trial. Lancet. 1999, 353: 1993-2000. 10.1016/S0140-6736(99)05036-9.PubMedCrossRef
4.
go back to reference Houghton J, George WD, Cuzick J, Duggan C, Fentiman IS, Spittle M: Radiotherapy and tamoxifen in women with completely excised ductal carcinoma in situ of the breast in the UK, Australia, and New Zealand: randomised controlled trial. Lancet. 2003, 362: 95-102. 10.1016/S0140-6736(03)13859-7.PubMedCrossRef Houghton J, George WD, Cuzick J, Duggan C, Fentiman IS, Spittle M: Radiotherapy and tamoxifen in women with completely excised ductal carcinoma in situ of the breast in the UK, Australia, and New Zealand: randomised controlled trial. Lancet. 2003, 362: 95-102. 10.1016/S0140-6736(03)13859-7.PubMedCrossRef
5.
go back to reference Omlin A, Amichetti M, Azria D, Cole BF, Fourneret P, Poortmans P, Naehrig D, Miller RC, Krengli M, Gutierrez Miguelez C, Morgan D, Goldberg H, Scandolaro L, Gastelblum P, Ozsahin M, Dohr D, Christie D, Oppitz U, Abacioglu U, Gruber G: Boost radiotherapy in young women with ductal carcinoma in situ: a multicentre, retrospective study of the Rare Cancer Network. Lancet Oncol. 2006, 7: 652-656. 10.1016/S1470-2045(06)70765-3.PubMedCrossRef Omlin A, Amichetti M, Azria D, Cole BF, Fourneret P, Poortmans P, Naehrig D, Miller RC, Krengli M, Gutierrez Miguelez C, Morgan D, Goldberg H, Scandolaro L, Gastelblum P, Ozsahin M, Dohr D, Christie D, Oppitz U, Abacioglu U, Gruber G: Boost radiotherapy in young women with ductal carcinoma in situ: a multicentre, retrospective study of the Rare Cancer Network. Lancet Oncol. 2006, 7: 652-656. 10.1016/S1470-2045(06)70765-3.PubMedCrossRef
6.
go back to reference Vogel VG, Costantino JP, Wickerham DL, McCaskill-Stevens W, Clarfeld RB, Grant MD, Wolmark N: Carcinoma in situ outcomes in National Surgical Adjuvant Breast and Bowel Project Breast Cancer Chemoprevention Trials. J Natl Cancer Inst Monogr. 2010, 2010: 181-186. 10.1093/jncimonographs/lgq041.PubMedPubMedCentralCrossRef Vogel VG, Costantino JP, Wickerham DL, McCaskill-Stevens W, Clarfeld RB, Grant MD, Wolmark N: Carcinoma in situ outcomes in National Surgical Adjuvant Breast and Bowel Project Breast Cancer Chemoprevention Trials. J Natl Cancer Inst Monogr. 2010, 2010: 181-186. 10.1093/jncimonographs/lgq041.PubMedPubMedCentralCrossRef
7.
go back to reference Cuzick J, Sestak I, Pinder SE, Ellis IO, Forsyth S, Bundred NJ, Forbes JF, Bishop H, Fentiman IS, George WD: Effect of tamoxifen and radiotherapy in women with locally excised ductal carcinoma in situ: long-term results from the UK/ANZ DCIS trial. Lancet Oncol. 2011, 12: 21-29. 10.1016/S1470-2045(10)70266-7.PubMedCrossRef Cuzick J, Sestak I, Pinder SE, Ellis IO, Forsyth S, Bundred NJ, Forbes JF, Bishop H, Fentiman IS, George WD: Effect of tamoxifen and radiotherapy in women with locally excised ductal carcinoma in situ: long-term results from the UK/ANZ DCIS trial. Lancet Oncol. 2011, 12: 21-29. 10.1016/S1470-2045(10)70266-7.PubMedCrossRef
8.
go back to reference Staley H, McCallum I, Bruce J: Postoperative tamoxifen for ductal carcinoma in situ. Cochrane Database Syst Rev. 2012, 10: CD007847-PubMed Staley H, McCallum I, Bruce J: Postoperative tamoxifen for ductal carcinoma in situ. Cochrane Database Syst Rev. 2012, 10: CD007847-PubMed
9.
go back to reference Shapiro CL, Recht A: Side effects of adjuvant treatment of breast cancer. N Engl J Med. 2001, 344: 1997-2008. 10.1056/NEJM200106283442607.PubMedCrossRef Shapiro CL, Recht A: Side effects of adjuvant treatment of breast cancer. N Engl J Med. 2001, 344: 1997-2008. 10.1056/NEJM200106283442607.PubMedCrossRef
10.
go back to reference Hughes LL, Wang M, Page DL, Gray R, Solin LJ, Davidson NE, Lowen MA, Ingle JN, Recht A, Wood WC: Local excision alone without irradiation for ductal carcinoma in situof the breast: a trial of the Eastern Cooperative Oncology Group. J Clin Oncol. 2009, 27: 5319-5324. 10.1200/JCO.2009.21.8560.PubMedPubMedCentralCrossRef Hughes LL, Wang M, Page DL, Gray R, Solin LJ, Davidson NE, Lowen MA, Ingle JN, Recht A, Wood WC: Local excision alone without irradiation for ductal carcinoma in situof the breast: a trial of the Eastern Cooperative Oncology Group. J Clin Oncol. 2009, 27: 5319-5324. 10.1200/JCO.2009.21.8560.PubMedPubMedCentralCrossRef
11.
go back to reference Wang SY, Shamliyan T, Virnig BA, Kane R: Tumor characteristics as predictors of local recurrence after treatment of ductal carcinoma in situ: a meta-analysis. Breast Cancer Res Treat. 2011, 127: 1-14. 10.1007/s10549-011-1387-4.PubMedCrossRef Wang SY, Shamliyan T, Virnig BA, Kane R: Tumor characteristics as predictors of local recurrence after treatment of ductal carcinoma in situ: a meta-analysis. Breast Cancer Res Treat. 2011, 127: 1-14. 10.1007/s10549-011-1387-4.PubMedCrossRef
13.
go back to reference Rakovitch E, Nofech-Mozes S, Hanna W, Narod S, Thiruchelvam D, Saskin R, Spayne J, Taylor C, Paszat L: HER2/neu and Ki-67 expression predict noninvasive recurrence following breast-conserving therapy for ductal carcinoma in situ. Br J Cancer. 2012, 106: 1160-1165. 10.1038/bjc.2012.41.PubMedPubMedCentralCrossRef Rakovitch E, Nofech-Mozes S, Hanna W, Narod S, Thiruchelvam D, Saskin R, Spayne J, Taylor C, Paszat L: HER2/neu and Ki-67 expression predict noninvasive recurrence following breast-conserving therapy for ductal carcinoma in situ. Br J Cancer. 2012, 106: 1160-1165. 10.1038/bjc.2012.41.PubMedPubMedCentralCrossRef
14.
go back to reference Holmes P, Lloyd J, Chervoneva I, Pequinot E, Cornfield DB, Schwartz GF, Allen KG, Palazzo JP: Prognostic markers and long-term outcomes in ductal carcinoma in situ of the breast treated with excision alone. Cancer. 2011, 117: 3650-3657. 10.1002/cncr.25942.PubMedCrossRef Holmes P, Lloyd J, Chervoneva I, Pequinot E, Cornfield DB, Schwartz GF, Allen KG, Palazzo JP: Prognostic markers and long-term outcomes in ductal carcinoma in situ of the breast treated with excision alone. Cancer. 2011, 117: 3650-3657. 10.1002/cncr.25942.PubMedCrossRef
15.
go back to reference Pinder SE, Duggan C, Ellis IO, Cuzick J, Forbes JF, Bishop H, Fentiman IS, George WD: A new pathological system for grading DCIS with improved prediction of local recurrence: results from the UKCCCR/ANZ DCIS trial. Br J Cancer. 2010, 103: 94-100. 10.1038/sj.bjc.6605718.PubMedPubMedCentralCrossRef Pinder SE, Duggan C, Ellis IO, Cuzick J, Forbes JF, Bishop H, Fentiman IS, George WD: A new pathological system for grading DCIS with improved prediction of local recurrence: results from the UKCCCR/ANZ DCIS trial. Br J Cancer. 2010, 103: 94-100. 10.1038/sj.bjc.6605718.PubMedPubMedCentralCrossRef
16.
go back to reference Dunne C, Burke JP, Morrow M, Kell MR: Effect of margin status on local recurrence after breast conservation and radiation therapy for ductal carcinoma in situ. J Clin Oncol. 2009, 27: 1615-1620. 10.1200/JCO.2008.17.5182.PubMedCrossRef Dunne C, Burke JP, Morrow M, Kell MR: Effect of margin status on local recurrence after breast conservation and radiation therapy for ductal carcinoma in situ. J Clin Oncol. 2009, 27: 1615-1620. 10.1200/JCO.2008.17.5182.PubMedCrossRef
17.
go back to reference Provenzano E, Hopper JL, Giles GG, Marr G, Venter DJ, Armes JE: Biological markers that predict clinical recurrence in ductal carcinoma in situ of the breast. Eur J Cancer. 2003, 39: 622-630. 10.1016/S0959-8049(02)00666-4.PubMedCrossRef Provenzano E, Hopper JL, Giles GG, Marr G, Venter DJ, Armes JE: Biological markers that predict clinical recurrence in ductal carcinoma in situ of the breast. Eur J Cancer. 2003, 39: 622-630. 10.1016/S0959-8049(02)00666-4.PubMedCrossRef
18.
go back to reference de Roos MA, de Bock GH, de Vries J, van der Vegt B, Wesseling J: p53 overexpression is a predictor of local recurrence after treatment for both in situ and invasive ductal carcinoma of the breast. J Surg Res. 2007, 140: 109-114. 10.1016/j.jss.2006.10.045.PubMedCrossRef de Roos MA, de Bock GH, de Vries J, van der Vegt B, Wesseling J: p53 overexpression is a predictor of local recurrence after treatment for both in situ and invasive ductal carcinoma of the breast. J Surg Res. 2007, 140: 109-114. 10.1016/j.jss.2006.10.045.PubMedCrossRef
19.
go back to reference Nofech-Mozes S, Spayne J, Rakovitch E, Kahn HJ, Seth A, Pignol JP, Lickley L, Paszat L, Hanna W: Biological markers predictive of invasive recurrence in DCIS. Clin Med Oncol. 2008, 2: 7-18.PubMedPubMedCentral Nofech-Mozes S, Spayne J, Rakovitch E, Kahn HJ, Seth A, Pignol JP, Lickley L, Paszat L, Hanna W: Biological markers predictive of invasive recurrence in DCIS. Clin Med Oncol. 2008, 2: 7-18.PubMedPubMedCentral
20.
go back to reference Gauthier ML, Berman HK, Miller C, Kozakeiwicz K, Chew K, Moore D, Rabban J, Chen YY, Kerlikowske K, Tlsty TD: Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell. 2007, 12: 479-491. 10.1016/j.ccr.2007.10.017.PubMedPubMedCentralCrossRef Gauthier ML, Berman HK, Miller C, Kozakeiwicz K, Chew K, Moore D, Rabban J, Chen YY, Kerlikowske K, Tlsty TD: Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell. 2007, 12: 479-491. 10.1016/j.ccr.2007.10.017.PubMedPubMedCentralCrossRef
21.
go back to reference Kerlikowske K, Molinaro AM, Gauthier ML, Berman HK, Waldman F, Bennington J, Sanchez H, Jimenez C, Stewart K, Chew K, Ljung BM, Tlsty TD: Biomarker expression and risk of subsequent tumors after initial ductal carcinoma in situ diagnosis. J Natl Cancer Inst. 2010, 102: 627-637. 10.1093/jnci/djq101.PubMedPubMedCentralCrossRef Kerlikowske K, Molinaro AM, Gauthier ML, Berman HK, Waldman F, Bennington J, Sanchez H, Jimenez C, Stewart K, Chew K, Ljung BM, Tlsty TD: Biomarker expression and risk of subsequent tumors after initial ductal carcinoma in situ diagnosis. J Natl Cancer Inst. 2010, 102: 627-637. 10.1093/jnci/djq101.PubMedPubMedCentralCrossRef
22.
go back to reference Witkiewicz AK, Rivadeneira DB, Ertel A, Kline J, Hyslop T, Schwartz GF, Fortina P, Knudsen ES: Association of RB/p16-pathway perturbations with DCIS recurrence: dependence on tumor versus tissue microenvironment. Am J Pathol. 2011, 179: 1171-1178. 10.1016/j.ajpath.2011.05.043.PubMedPubMedCentralCrossRef Witkiewicz AK, Rivadeneira DB, Ertel A, Kline J, Hyslop T, Schwartz GF, Fortina P, Knudsen ES: Association of RB/p16-pathway perturbations with DCIS recurrence: dependence on tumor versus tissue microenvironment. Am J Pathol. 2011, 179: 1171-1178. 10.1016/j.ajpath.2011.05.043.PubMedPubMedCentralCrossRef
23.
go back to reference Hieken TJ, Cheregi J, Farolan M, Kim J, Velasco JM: Predicting relapse in ductal carcinoma in situ patients: an analysis of biologic markers with long-term follow-up. Am J Surg. 2007, 194: 504-506. 10.1016/j.amjsurg.2007.07.002.PubMedCrossRef Hieken TJ, Cheregi J, Farolan M, Kim J, Velasco JM: Predicting relapse in ductal carcinoma in situ patients: an analysis of biologic markers with long-term follow-up. Am J Surg. 2007, 194: 504-506. 10.1016/j.amjsurg.2007.07.002.PubMedCrossRef
24.
go back to reference Tan EY, Campo L, Han C, Turley H, Pezzella F, Gatter KC, Harris AL, Fox SB: BNIP3 as a progression marker in primary human breast cancer; opposing functions in in situ versus invasive cancer. Clin Cancer Res. 2007, 13: 467-474. 10.1158/1078-0432.CCR-06-1466.PubMedCrossRef Tan EY, Campo L, Han C, Turley H, Pezzella F, Gatter KC, Harris AL, Fox SB: BNIP3 as a progression marker in primary human breast cancer; opposing functions in in situ versus invasive cancer. Clin Cancer Res. 2007, 13: 467-474. 10.1158/1078-0432.CCR-06-1466.PubMedCrossRef
25.
go back to reference Ma XJ, Salunga R, Tuggle JT, Gaudet J, Enright E, McQuary P, Payette T, Pistone M, Stecker K, Zhang BM, Zhou YX, Varnholt H, Smith B, Gadd M, Chatfield E, Kessler J, Baer TM, Erlander MG, Sgroi DC: Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA. 2003, 100: 5974-5979. 10.1073/pnas.0931261100.PubMedPubMedCentralCrossRef Ma XJ, Salunga R, Tuggle JT, Gaudet J, Enright E, McQuary P, Payette T, Pistone M, Stecker K, Zhang BM, Zhou YX, Varnholt H, Smith B, Gadd M, Chatfield E, Kessler J, Baer TM, Erlander MG, Sgroi DC: Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA. 2003, 100: 5974-5979. 10.1073/pnas.0931261100.PubMedPubMedCentralCrossRef
26.
go back to reference Porter D, Lahti-Domenici J, Keshaviah A, Bae YK, Argani P, Marks J, Richardson A, Cooper A, Strausberg R, Riggins GJ, Schnitt S, Gabrielson E, Gelman R, Polyak K: Molecular markers in ductal carcinoma in situ of the breast. Mol Cancer Res. 2003, 1: 362-375.PubMed Porter D, Lahti-Domenici J, Keshaviah A, Bae YK, Argani P, Marks J, Richardson A, Cooper A, Strausberg R, Riggins GJ, Schnitt S, Gabrielson E, Gelman R, Polyak K: Molecular markers in ductal carcinoma in situ of the breast. Mol Cancer Res. 2003, 1: 362-375.PubMed
27.
go back to reference Balleine RL, Webster LR, Davis S, Salisbury EL, Palazzo JP, Schwartz GF, Cornfield DB, Walker RL, Byth K, Clarke CL, Meltzer PS: Molecular grading of ductal carcinoma in situ of the breast. Clin Cancer Res. 2008, 14: 8244-8252. 10.1158/1078-0432.CCR-08-0939.PubMedCrossRef Balleine RL, Webster LR, Davis S, Salisbury EL, Palazzo JP, Schwartz GF, Cornfield DB, Walker RL, Byth K, Clarke CL, Meltzer PS: Molecular grading of ductal carcinoma in situ of the breast. Clin Cancer Res. 2008, 14: 8244-8252. 10.1158/1078-0432.CCR-08-0939.PubMedCrossRef
28.
go back to reference Lambert K, Patani N, Mokbel K: Ductal carcinoma in situ: recent advances and future prospects. Int J Surg Oncol. 2012, 2012: 347385-PubMedPubMedCentral Lambert K, Patani N, Mokbel K: Ductal carcinoma in situ: recent advances and future prospects. Int J Surg Oncol. 2012, 2012: 347385-PubMedPubMedCentral
29.
go back to reference Mikeska T, Bock C, Do H, Dobrovic A: DNA methylation biomarkers in cancer: progress towards clinical implementation. Expert Rev Mol Diagn. 2012, 12: 473-487. 10.1586/erm.12.45.PubMedCrossRef Mikeska T, Bock C, Do H, Dobrovic A: DNA methylation biomarkers in cancer: progress towards clinical implementation. Expert Rev Mol Diagn. 2012, 12: 473-487. 10.1586/erm.12.45.PubMedCrossRef
30.
go back to reference Mikeska T, Candiloro IL, Dobrovic A: The implications of heterogeneous DNA methylation for the accurate quantification of methylation. Epigenomics. 2010, 2: 561-573. 10.2217/epi.10.32.PubMedCrossRef Mikeska T, Candiloro IL, Dobrovic A: The implications of heterogeneous DNA methylation for the accurate quantification of methylation. Epigenomics. 2010, 2: 561-573. 10.2217/epi.10.32.PubMedCrossRef
32.
go back to reference Kristensen LS, Hansen LL: PCR-based methods for detecting single-locus DNA methylation biomarkers in cancer diagnostics, prognostics, and response to treatment. Clin Chem. 2009, 55: 1471-1483. 10.1373/clinchem.2008.121962.PubMedCrossRef Kristensen LS, Hansen LL: PCR-based methods for detecting single-locus DNA methylation biomarkers in cancer diagnostics, prognostics, and response to treatment. Clin Chem. 2009, 55: 1471-1483. 10.1373/clinchem.2008.121962.PubMedCrossRef
33.
go back to reference Evron E, Umbricht CB, Korz D, Raman V, Loeb DM, Niranjan B, Buluwela L, Weitzman SA, Marks J, Sukumar S: Loss of cyclin D2 expression in the majority of breast cancers is associated with promoter hypermethylation. Cancer Res. 2001, 61: 2782-2787.PubMed Evron E, Umbricht CB, Korz D, Raman V, Loeb DM, Niranjan B, Buluwela L, Weitzman SA, Marks J, Sukumar S: Loss of cyclin D2 expression in the majority of breast cancers is associated with promoter hypermethylation. Cancer Res. 2001, 61: 2782-2787.PubMed
34.
go back to reference Kang JH, Kim SJ, Noh DY, Park IA, Choe KJ, Yoo OJ, Kang HS: Methylation in the p53 promoter is a supplementary route to breast carcinogenesis: correlation between CpG methylation in the p53 promoter and the mutation of the p53 gene in the progression from ductal carcinoma in situ to invasive ductal carcinoma. Lab Invest. 2001, 81: 573-579. 10.1038/labinvest.3780266.PubMedCrossRef Kang JH, Kim SJ, Noh DY, Park IA, Choe KJ, Yoo OJ, Kang HS: Methylation in the p53 promoter is a supplementary route to breast carcinogenesis: correlation between CpG methylation in the p53 promoter and the mutation of the p53 gene in the progression from ductal carcinoma in situ to invasive ductal carcinoma. Lab Invest. 2001, 81: 573-579. 10.1038/labinvest.3780266.PubMedCrossRef
35.
go back to reference Umbricht CB, Evron E, Gabrielson E, Ferguson A, Marks J, Sukumar S: Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene. 2001, 20: 3348-3353. 10.1038/sj.onc.1204438.PubMedCrossRef Umbricht CB, Evron E, Gabrielson E, Ferguson A, Marks J, Sukumar S: Hypermethylation of 14-3-3 sigma (stratifin) is an early event in breast cancer. Oncogene. 2001, 20: 3348-3353. 10.1038/sj.onc.1204438.PubMedCrossRef
36.
go back to reference Lehmann U, Langer F, Feist H, Glockner S, Hasemeier B, Kreipe H: Quantitative assessment of promoter hypermethylation during breast cancer development. Am J Pathol. 2002, 160: 605-612. 10.1016/S0002-9440(10)64880-8.PubMedPubMedCentralCrossRef Lehmann U, Langer F, Feist H, Glockner S, Hasemeier B, Kreipe H: Quantitative assessment of promoter hypermethylation during breast cancer development. Am J Pathol. 2002, 160: 605-612. 10.1016/S0002-9440(10)64880-8.PubMedPubMedCentralCrossRef
37.
go back to reference Fackler MJ, McVeigh M, Evron E, Garrett E, Mehrotra J, Polyak K, Sukumar S, Argani P: DNA methylation of RASSF1A, HIN-1, RAR-beta, Cyclin D2 and Twist in in situ and invasive lobular breast carcinoma. Int J Cancer. 2003, 107: 970-975. 10.1002/ijc.11508.PubMedCrossRef Fackler MJ, McVeigh M, Evron E, Garrett E, Mehrotra J, Polyak K, Sukumar S, Argani P: DNA methylation of RASSF1A, HIN-1, RAR-beta, Cyclin D2 and Twist in in situ and invasive lobular breast carcinoma. Int J Cancer. 2003, 107: 970-975. 10.1002/ijc.11508.PubMedCrossRef
38.
go back to reference Honorio S, Agathanggelou A, Schuermann M, Pankow W, Viacava P, Maher ER, Latif F: Detection of RASSF1A aberrant promoter hypermethylation in sputum from chronic smokers and ductal carcinoma in situ from breast cancer patients. Oncogene. 2003, 22: 147-150. 10.1038/sj.onc.1206057.PubMedCrossRef Honorio S, Agathanggelou A, Schuermann M, Pankow W, Viacava P, Maher ER, Latif F: Detection of RASSF1A aberrant promoter hypermethylation in sputum from chronic smokers and ductal carcinoma in situ from breast cancer patients. Oncogene. 2003, 22: 147-150. 10.1038/sj.onc.1206057.PubMedCrossRef
39.
go back to reference Yuan Y, Liu H, Sahin A, Dai JL: Reactivation of SYK expression by inhibition of DNA methylation suppresses breast cancer cell invasiveness. Int J Cancer. 2005, 113: 654-659. 10.1002/ijc.20628.PubMedCrossRef Yuan Y, Liu H, Sahin A, Dai JL: Reactivation of SYK expression by inhibition of DNA methylation suppresses breast cancer cell invasiveness. Int J Cancer. 2005, 113: 654-659. 10.1002/ijc.20628.PubMedCrossRef
40.
go back to reference Douglas DB, Akiyama Y, Carraway H, Belinsky SA, Esteller M, Gabrielson E, Weitzman S, Williams T, Herman JG, Baylin SB: Hypermethylation of a small CpGuanine-rich region correlates with loss of activator protein-2alpha expression during progression of breast cancer. Cancer Res. 2004, 64: 1611-1620. 10.1158/0008-5472.CAN-0318-2.PubMedCrossRef Douglas DB, Akiyama Y, Carraway H, Belinsky SA, Esteller M, Gabrielson E, Weitzman S, Williams T, Herman JG, Baylin SB: Hypermethylation of a small CpGuanine-rich region correlates with loss of activator protein-2alpha expression during progression of breast cancer. Cancer Res. 2004, 64: 1611-1620. 10.1158/0008-5472.CAN-0318-2.PubMedCrossRef
41.
go back to reference Futscher BW, O'Meara MM, Kim CJ, Rennels MA, Lu D, Gruman LM, Seftor RE, Hendrix MJ, Domann FE: Aberrant methylation of the maspin promoter is an early event in human breast cancer. Neoplasia. 2004, 6: 380-389. 10.1593/neo.04115.PubMedPubMedCentralCrossRef Futscher BW, O'Meara MM, Kim CJ, Rennels MA, Lu D, Gruman LM, Seftor RE, Hendrix MJ, Domann FE: Aberrant methylation of the maspin promoter is an early event in human breast cancer. Neoplasia. 2004, 6: 380-389. 10.1593/neo.04115.PubMedPubMedCentralCrossRef
42.
go back to reference Lo PK, Mehrotra J, D'Costa A, Fackler MJ, Garrett-Mayer E, Argani P, Sukumar S: Epigenetic suppression of secreted frizzled related protein 1 (SFRP1) expression in human breast cancer. Cancer Biol Ther. 2006, 5: 281-286. 10.4161/cbt.5.3.2384.PubMedCrossRef Lo PK, Mehrotra J, D'Costa A, Fackler MJ, Garrett-Mayer E, Argani P, Sukumar S: Epigenetic suppression of secreted frizzled related protein 1 (SFRP1) expression in human breast cancer. Cancer Biol Ther. 2006, 5: 281-286. 10.4161/cbt.5.3.2384.PubMedCrossRef
43.
go back to reference Liu T, Niu Y, Feng Y, Niu R, Yu Y, Lv A, Yang Y: Methylation of CpG islands of p16(INK4a) and cyclinD1 overexpression associated with progression of intraductal proliferative lesions of the breast. Hum Pathol. 2008, 39: 1637-1646. 10.1016/j.humpath.2008.04.001.PubMedCrossRef Liu T, Niu Y, Feng Y, Niu R, Yu Y, Lv A, Yang Y: Methylation of CpG islands of p16(INK4a) and cyclinD1 overexpression associated with progression of intraductal proliferative lesions of the breast. Hum Pathol. 2008, 39: 1637-1646. 10.1016/j.humpath.2008.04.001.PubMedCrossRef
44.
go back to reference Lee JS, Fackler MJ, Teo WW, Lee JH, Choi C, Park MH, Yoon JH, Zhang Z, Argani P, Sukumar S: Quantitative promoter hypermethylation profiles of ductal carcinoma in situ in North American and Korean women: potential applications for diagnosis. Cancer Biol Ther. 2008, 7: 1398-1406.PubMedCrossRef Lee JS, Fackler MJ, Teo WW, Lee JH, Choi C, Park MH, Yoon JH, Zhang Z, Argani P, Sukumar S: Quantitative promoter hypermethylation profiles of ductal carcinoma in situ in North American and Korean women: potential applications for diagnosis. Cancer Biol Ther. 2008, 7: 1398-1406.PubMedCrossRef
45.
go back to reference Subramaniam MM, Chan JY, Soong R, Ito K, Ito Y, Yeoh KG, Salto-Tellez M, Putti TC: RUNX3 inactivation by frequent promoter hypermethylation and protein mislocalization constitute an early event in breast cancer progression. Breast Cancer Res Treat. 2009, 113: 113-121. 10.1007/s10549-008-9917-4.PubMedCrossRef Subramaniam MM, Chan JY, Soong R, Ito K, Ito Y, Yeoh KG, Salto-Tellez M, Putti TC: RUNX3 inactivation by frequent promoter hypermethylation and protein mislocalization constitute an early event in breast cancer progression. Breast Cancer Res Treat. 2009, 113: 113-121. 10.1007/s10549-008-9917-4.PubMedCrossRef
46.
go back to reference Hoque MO, Prencipe M, Poeta ML, Barbano R, Valori VM, Copetti M, Gallo AP, Brait M, Maiello E, Apicella A, Rossiello R, Zito F, Stefania T, Paradiso A, Carella M, Dallapiccola B, Murgo R, Carosi I, Bisceglia M, Fazio VM, Sidransky D, Parrella P: Changes in CpG islands promoter methylation patterns during ductal breast carcinoma progression. Cancer Epidemiol Biomarkers Prev. 2009, 18: 2694-2700. 10.1158/1055-9965.EPI-08-0821.PubMedPubMedCentralCrossRef Hoque MO, Prencipe M, Poeta ML, Barbano R, Valori VM, Copetti M, Gallo AP, Brait M, Maiello E, Apicella A, Rossiello R, Zito F, Stefania T, Paradiso A, Carella M, Dallapiccola B, Murgo R, Carosi I, Bisceglia M, Fazio VM, Sidransky D, Parrella P: Changes in CpG islands promoter methylation patterns during ductal breast carcinoma progression. Cancer Epidemiol Biomarkers Prev. 2009, 18: 2694-2700. 10.1158/1055-9965.EPI-08-0821.PubMedPubMedCentralCrossRef
47.
go back to reference Muggerud AA, Rønneberg JA, Wärnberg F, Botling J, Busato F, Jovanovic J, Solvang H, Bukholm I, Børresen-Dale AL, Kristensen VN, Sørlie T, Tost J: Frequent aberrant DNA methylation of ABCB1, FOXC1, PPP2R2B and PTEN in ductal carcinoma in situ and early invasive breast cancer. Breast Cancer Res. 2010, 12: R3-10.1186/bcr2466.PubMedPubMedCentralCrossRef Muggerud AA, Rønneberg JA, Wärnberg F, Botling J, Busato F, Jovanovic J, Solvang H, Bukholm I, Børresen-Dale AL, Kristensen VN, Sørlie T, Tost J: Frequent aberrant DNA methylation of ABCB1, FOXC1, PPP2R2B and PTEN in ductal carcinoma in situ and early invasive breast cancer. Breast Cancer Res. 2010, 12: R3-10.1186/bcr2466.PubMedPubMedCentralCrossRef
48.
go back to reference Moelans CB, Verschuur-Maes AH, van Diest PJ: Frequent promoter hypermethylation of BRCA2, CDH13, MSH6, PAX5, PAX6 and WT1 in ductal carcinoma in situ and invasive breast cancer. J Pathol. 2011, 225: 222-231. 10.1002/path.2930.PubMedCrossRef Moelans CB, Verschuur-Maes AH, van Diest PJ: Frequent promoter hypermethylation of BRCA2, CDH13, MSH6, PAX5, PAX6 and WT1 in ductal carcinoma in situ and invasive breast cancer. J Pathol. 2011, 225: 222-231. 10.1002/path.2930.PubMedCrossRef
49.
go back to reference Park SY, Kwon HJ, Lee HE, Ryu HS, Kim SW, Kim JH, Kim IA, Jung N, Cho NY, Kang GH: Promoter CpG island hypermethylation during breast cancer progression. Virchows Arch. 2011, 458: 73-84. 10.1007/s00428-010-1013-6.PubMedCrossRef Park SY, Kwon HJ, Lee HE, Ryu HS, Kim SW, Kim JH, Kim IA, Jung N, Cho NY, Kang GH: Promoter CpG island hypermethylation during breast cancer progression. Virchows Arch. 2011, 458: 73-84. 10.1007/s00428-010-1013-6.PubMedCrossRef
50.
go back to reference Iakovlev VV, Arneson NC, Wong V, Wang C, Leung S, Iakovleva G, Warren K, Pintilie M, Done SJ: Genomic differences between pure ductal carcinoma in situ of the breast and that associated with invasive disease: a calibrated aCGH study. Clin Cancer Res. 2008, 14: 4446-4454. 10.1158/1078-0432.CCR-07-4960.PubMedCrossRef Iakovlev VV, Arneson NC, Wong V, Wang C, Leung S, Iakovleva G, Warren K, Pintilie M, Done SJ: Genomic differences between pure ductal carcinoma in situ of the breast and that associated with invasive disease: a calibrated aCGH study. Clin Cancer Res. 2008, 14: 4446-4454. 10.1158/1078-0432.CCR-07-4960.PubMedCrossRef
51.
go back to reference Farabegoli F, Champeme MH, Bieche I, Santini D, Ceccarelli C, Derenzini M, Lidereau R: Genetic pathways in the evolution of breast ductal carcinoma in situ. J Pathol. 2002, 196: 280-286. 10.1002/path.1048.PubMedCrossRef Farabegoli F, Champeme MH, Bieche I, Santini D, Ceccarelli C, Derenzini M, Lidereau R: Genetic pathways in the evolution of breast ductal carcinoma in situ. J Pathol. 2002, 196: 280-286. 10.1002/path.1048.PubMedCrossRef
52.
go back to reference Krop IE, Sgroi D, Porter DA, Lunetta KL, LeVangie R, Seth P, Kaelin CM, Rhei E, Bosenberg M, Schnitt S, Marks JR, Pagon Z, Belina D, Razumovic J, Polyak K: HIN-1, a putative cytokine highly expressed in normal but not cancerous mammary epithelial cells. Proc Natl Acad Sci USA. 2001, 98: 9796-9801. 10.1073/pnas.171138398.PubMedPubMedCentralCrossRef Krop IE, Sgroi D, Porter DA, Lunetta KL, LeVangie R, Seth P, Kaelin CM, Rhei E, Bosenberg M, Schnitt S, Marks JR, Pagon Z, Belina D, Razumovic J, Polyak K: HIN-1, a putative cytokine highly expressed in normal but not cancerous mammary epithelial cells. Proc Natl Acad Sci USA. 2001, 98: 9796-9801. 10.1073/pnas.171138398.PubMedPubMedCentralCrossRef
53.
go back to reference Verschuur-Maes AH, de Bruin PC, van Diest PJ: Epigenetic progression of columnar cell lesions of the breast to invasive breast cancer. Breast Cancer Res Treat. 2012, 136: 705-715. 10.1007/s10549-012-2301-4.PubMedCrossRef Verschuur-Maes AH, de Bruin PC, van Diest PJ: Epigenetic progression of columnar cell lesions of the breast to invasive breast cancer. Breast Cancer Res Treat. 2012, 136: 705-715. 10.1007/s10549-012-2301-4.PubMedCrossRef
54.
go back to reference Faryna M, Konermann C, Aulmann S, Bermejo JL, Brugger M, Diederichs S, Rom J, Weichenhan D, Claus R, Rehli M, Schirmacher P, Sinn HP, Plass C, Gerhauser C: Genome-wide methylation screen in low-grade breast cancer identifies novel epigenetically altered genes as potential biomarkers for tumor diagnosis. FASEB J. 2012, 26: 4937-4950. 10.1096/fj.12-209502.PubMedCrossRef Faryna M, Konermann C, Aulmann S, Bermejo JL, Brugger M, Diederichs S, Rom J, Weichenhan D, Claus R, Rehli M, Schirmacher P, Sinn HP, Plass C, Gerhauser C: Genome-wide methylation screen in low-grade breast cancer identifies novel epigenetically altered genes as potential biomarkers for tumor diagnosis. FASEB J. 2012, 26: 4937-4950. 10.1096/fj.12-209502.PubMedCrossRef
55.
go back to reference Tommasi S, Karm DL, Wu X, Yen Y, Pfeifer GP: Methylation of homeobox genes is a frequent and early epigenetic event in breast cancer. Breast Cancer Res. 2009, 11: R14-10.1186/bcr2233.PubMedPubMedCentralCrossRef Tommasi S, Karm DL, Wu X, Yen Y, Pfeifer GP: Methylation of homeobox genes is a frequent and early epigenetic event in breast cancer. Breast Cancer Res. 2009, 11: R14-10.1186/bcr2233.PubMedPubMedCentralCrossRef
56.
go back to reference Lee JS: GSTP1 promoter hypermethylation is an early event in breast carcinogenesis. Virchows Arch. 2007, 450: 637-642. 10.1007/s00428-007-0421-8.PubMedCrossRef Lee JS: GSTP1 promoter hypermethylation is an early event in breast carcinogenesis. Virchows Arch. 2007, 450: 637-642. 10.1007/s00428-007-0421-8.PubMedCrossRef
57.
go back to reference Stirzaker C, Song JZ, Davidson B, Clark SJ: Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res. 2004, 64: 3871-3877. 10.1158/0008-5472.CAN-03-3690.PubMedCrossRef Stirzaker C, Song JZ, Davidson B, Clark SJ: Transcriptional gene silencing promotes DNA hypermethylation through a sequential change in chromatin modifications in cancer cells. Cancer Res. 2004, 64: 3871-3877. 10.1158/0008-5472.CAN-03-3690.PubMedCrossRef
58.
go back to reference Xu X, Gammon MD, Zhang Y, Cho YH, Wetmur JG, Bradshaw PT, Garbowski G, Hibshoosh H, Teitelbaum SL, Neugut AI, Santella RM, Chen J: Gene promoter methylation is associated with increased mortality among women with breast cancer. Breast Cancer Res Treat. 2010, 121: 685-692. 10.1007/s10549-009-0628-2.PubMedCrossRef Xu X, Gammon MD, Zhang Y, Cho YH, Wetmur JG, Bradshaw PT, Garbowski G, Hibshoosh H, Teitelbaum SL, Neugut AI, Santella RM, Chen J: Gene promoter methylation is associated with increased mortality among women with breast cancer. Breast Cancer Res Treat. 2010, 121: 685-692. 10.1007/s10549-009-0628-2.PubMedCrossRef
59.
go back to reference Jiang Y, Cui L, Chen WD, Shen SH, Ding LD: The prognostic role of RASSF1A promoter methylation in breast cancer: a meta-analysis of published data. PLoS One. 2012, 7: e36780-10.1371/journal.pone.0036780.PubMedPubMedCentralCrossRef Jiang Y, Cui L, Chen WD, Shen SH, Ding LD: The prognostic role of RASSF1A promoter methylation in breast cancer: a meta-analysis of published data. PLoS One. 2012, 7: e36780-10.1371/journal.pone.0036780.PubMedPubMedCentralCrossRef
60.
go back to reference Dejeux E, Rønneberg JA, Solvang H, Bukholm I, Geisler S, Aas T, Gut IG, Børresen-Dale AL, Lønning PE, Kristensen VN, Tost J: DNA methylation profiling in doxorubicin treated primary locally advanced breast tumours identifies novel genes associated with survival and treatment response. Mol Cancer. 2010, 9: 68-10.1186/1476-4598-9-68.PubMedPubMedCentralCrossRef Dejeux E, Rønneberg JA, Solvang H, Bukholm I, Geisler S, Aas T, Gut IG, Børresen-Dale AL, Lønning PE, Kristensen VN, Tost J: DNA methylation profiling in doxorubicin treated primary locally advanced breast tumours identifies novel genes associated with survival and treatment response. Mol Cancer. 2010, 9: 68-10.1186/1476-4598-9-68.PubMedPubMedCentralCrossRef
61.
go back to reference Cho YH, Shen J, Gammon MD, Zhang YJ, Wang Q, Gonzalez K, Xu X, Bradshaw PT, Teitelbaum SL, Garbowski G, Hibshoosh H, Neugut AI, Chen J, Santella RM: Prognostic significance of gene-specific promoter hypermethylation in breast cancer patients. Breast Cancer Res Treat. 2012, 131: 197-205. 10.1007/s10549-011-1712-y.PubMedCrossRef Cho YH, Shen J, Gammon MD, Zhang YJ, Wang Q, Gonzalez K, Xu X, Bradshaw PT, Teitelbaum SL, Garbowski G, Hibshoosh H, Neugut AI, Chen J, Santella RM: Prognostic significance of gene-specific promoter hypermethylation in breast cancer patients. Breast Cancer Res Treat. 2012, 131: 197-205. 10.1007/s10549-011-1712-y.PubMedCrossRef
62.
go back to reference Hill VK, Ricketts C, Bieche I, Vacher S, Gentle D, Lewis C, Maher ER, Latif F: Genome-wide DNA methylation profiling of CpG islands in breast cancer identifies novel genes associated with tumorigenicity. Cancer Res. 2011, 71: 2988-2999. 10.1158/0008-5472.CAN-10-4026.PubMedCrossRef Hill VK, Ricketts C, Bieche I, Vacher S, Gentle D, Lewis C, Maher ER, Latif F: Genome-wide DNA methylation profiling of CpG islands in breast cancer identifies novel genes associated with tumorigenicity. Cancer Res. 2011, 71: 2988-2999. 10.1158/0008-5472.CAN-10-4026.PubMedCrossRef
63.
go back to reference Maier S, Nimmrich I, Koenig T, Eppenberger-Castori S, Bohlmann I, Paradiso A, Spyratos F, Thomssen C, Mueller V, Nährig J, Schittulli F, Kates R, Lesche R, Schwope I, Kluth A, Marx A, Martens JW, Foekens JA, Schmitt M, Harbeck N, European Organisation for Research and Treatment of Cancer (EORTC) PathoBiology group: DNA-methylation of the homeodomain transcription factor PITX2 reliably predicts risk of distant disease recurrence in tamoxifen-treated, node-negative breast cancer patients--Technical and clinical validation in a multi-centre setting in collaboration with the European Organisation for Research and Treatment of Cancer (EORTC) PathoBiology group. Eur J Cancer. 2007, 43: 1679-1686. 10.1016/j.ejca.2007.04.025.PubMedCrossRef Maier S, Nimmrich I, Koenig T, Eppenberger-Castori S, Bohlmann I, Paradiso A, Spyratos F, Thomssen C, Mueller V, Nährig J, Schittulli F, Kates R, Lesche R, Schwope I, Kluth A, Marx A, Martens JW, Foekens JA, Schmitt M, Harbeck N, European Organisation for Research and Treatment of Cancer (EORTC) PathoBiology group: DNA-methylation of the homeodomain transcription factor PITX2 reliably predicts risk of distant disease recurrence in tamoxifen-treated, node-negative breast cancer patients--Technical and clinical validation in a multi-centre setting in collaboration with the European Organisation for Research and Treatment of Cancer (EORTC) PathoBiology group. Eur J Cancer. 2007, 43: 1679-1686. 10.1016/j.ejca.2007.04.025.PubMedCrossRef
64.
go back to reference Swift-Scanlan T, Vang R, Blackford A, Fackler MJ, Sukumar S: Methylated genes in breast cancer: associations with clinical and histopathological features in a familial breast cancer cohort. Cancer Biol Ther. 2011, 11: 853-865. 10.4161/cbt.11.10.15177.PubMedPubMedCentralCrossRef Swift-Scanlan T, Vang R, Blackford A, Fackler MJ, Sukumar S: Methylated genes in breast cancer: associations with clinical and histopathological features in a familial breast cancer cohort. Cancer Biol Ther. 2011, 11: 853-865. 10.4161/cbt.11.10.15177.PubMedPubMedCentralCrossRef
65.
go back to reference Lo Nigro C, Monteverde M, Lee S, Lattanzio L, Vivenza D, Comino A, Syed N, McHugh A, Wang H, Proby C, Garrone O, Merlano M, Hatzimichael E, Briasoulis E, Gojis O, Palmieri C, Jordan L, Quinlan P, Thompson A, Crook T: NT5E CpG island methylation is a favourable breast cancer biomarker. Br J Cancer. 2012, 107: 75-83. 10.1038/bjc.2012.212.PubMedPubMedCentralCrossRef Lo Nigro C, Monteverde M, Lee S, Lattanzio L, Vivenza D, Comino A, Syed N, McHugh A, Wang H, Proby C, Garrone O, Merlano M, Hatzimichael E, Briasoulis E, Gojis O, Palmieri C, Jordan L, Quinlan P, Thompson A, Crook T: NT5E CpG island methylation is a favourable breast cancer biomarker. Br J Cancer. 2012, 107: 75-83. 10.1038/bjc.2012.212.PubMedPubMedCentralCrossRef
66.
go back to reference Palmieri C, Monteverde M, Lattanzio L, Gojis O, Rudraraju B, Fortunato M, Syed N, Thompson A, Garrone O, Merlano M, Lo Nigro C, Crook T: Site-specific CpG methylation in the CCAAT/enhancer binding protein delta (CEBPdelta) CpG island in breast cancer is associated with metastatic relapse. Br J Cancer. 2012, 107: 732-738. 10.1038/bjc.2012.308.PubMedPubMedCentralCrossRef Palmieri C, Monteverde M, Lattanzio L, Gojis O, Rudraraju B, Fortunato M, Syed N, Thompson A, Garrone O, Merlano M, Lo Nigro C, Crook T: Site-specific CpG methylation in the CCAAT/enhancer binding protein delta (CEBPdelta) CpG island in breast cancer is associated with metastatic relapse. Br J Cancer. 2012, 107: 732-738. 10.1038/bjc.2012.308.PubMedPubMedCentralCrossRef
67.
go back to reference Widschwendter M, Siegmund KD, Muller HM, Fiegl H, Marth C, Muller-Holzner E, Jones PA, Laird PW: Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen. Cancer Res. 2004, 64: 3807-3813. 10.1158/0008-5472.CAN-03-3852.PubMedCrossRef Widschwendter M, Siegmund KD, Muller HM, Fiegl H, Marth C, Muller-Holzner E, Jones PA, Laird PW: Association of breast cancer DNA methylation profiles with hormone receptor status and response to tamoxifen. Cancer Res. 2004, 64: 3807-3813. 10.1158/0008-5472.CAN-03-3852.PubMedCrossRef
68.
go back to reference Martens JW, Nimmrich I, Koenig T, Look MP, Harbeck N, Model F, Kluth A, Bolt-de Vries J, Sieuwerts AM, Portengen H, Meijer-Van Gelder ME, Piepenbrock C, Olek A, Höfler H, Kiechle M, Klijn JG, Schmitt M, Maier S, Foekens JA: Association of DNA methylation of phosphoserine aminotransferase with response to endocrine therapy in patients with recurrent breast cancer. Cancer Res. 2005, 65: 4101-4117. 10.1158/0008-5472.CAN-05-0064.PubMedCrossRef Martens JW, Nimmrich I, Koenig T, Look MP, Harbeck N, Model F, Kluth A, Bolt-de Vries J, Sieuwerts AM, Portengen H, Meijer-Van Gelder ME, Piepenbrock C, Olek A, Höfler H, Kiechle M, Klijn JG, Schmitt M, Maier S, Foekens JA: Association of DNA methylation of phosphoserine aminotransferase with response to endocrine therapy in patients with recurrent breast cancer. Cancer Res. 2005, 65: 4101-4117. 10.1158/0008-5472.CAN-05-0064.PubMedCrossRef
69.
go back to reference Hurd PJ, Nelson CJ: Advantages of next-generation sequencing versus the microarray in epigenetic research. Brief Funct Genomic Proteomic. 2009, 8: 174-183. 10.1093/bfgp/elp013.PubMedCrossRef Hurd PJ, Nelson CJ: Advantages of next-generation sequencing versus the microarray in epigenetic research. Brief Funct Genomic Proteomic. 2009, 8: 174-183. 10.1093/bfgp/elp013.PubMedCrossRef
70.
go back to reference Laird PW: Principles and challenges of genomewide DNA methylation analysis. Nat Rev Genet. 2010, 11: 191-203.PubMedCrossRef Laird PW: Principles and challenges of genomewide DNA methylation analysis. Nat Rev Genet. 2010, 11: 191-203.PubMedCrossRef
71.
go back to reference Zhao Q, Zhang Y: Epigenome sequencing comes of age in development, differentiation and disease mechanism research. Epigenomics. 2011, 3: 207-220. 10.2217/epi.10.78.PubMedCrossRef Zhao Q, Zhang Y: Epigenome sequencing comes of age in development, differentiation and disease mechanism research. Epigenomics. 2011, 3: 207-220. 10.2217/epi.10.78.PubMedCrossRef
72.
go back to reference Ku CS, Naidoo N, Wu M, Soong R: Studying the epigenome using next generation sequencing. J Med Genet. 2011, 48: 721-730. 10.1136/jmedgenet-2011-100242.PubMedCrossRef Ku CS, Naidoo N, Wu M, Soong R: Studying the epigenome using next generation sequencing. J Med Genet. 2011, 48: 721-730. 10.1136/jmedgenet-2011-100242.PubMedCrossRef
73.
go back to reference Hirst M, Marra MA: Next generation sequencing based approaches to epigenomics. Brief Funct Genomics. 2010, 9: 455-465. 10.1093/bfgp/elq035.PubMedCrossRef Hirst M, Marra MA: Next generation sequencing based approaches to epigenomics. Brief Funct Genomics. 2010, 9: 455-465. 10.1093/bfgp/elq035.PubMedCrossRef
74.
go back to reference Carvalho RH, Haberle V, Hou J, van Gent T, Thongjuea S, van Ijcken W, Kockx C, Brouwer R, Rijkers E, Sieuwerts A, Foekens J, van Vroonhoven M, Aerts J, Grosveld F, Lenhard B, Philipsen S: Genome-wide DNA methylation profiling of non-small cell lung carcinomas. Epigenetics Chromatin. 2012, 5: 9-10.1186/1756-8935-5-9.PubMedPubMedCentralCrossRef Carvalho RH, Haberle V, Hou J, van Gent T, Thongjuea S, van Ijcken W, Kockx C, Brouwer R, Rijkers E, Sieuwerts A, Foekens J, van Vroonhoven M, Aerts J, Grosveld F, Lenhard B, Philipsen S: Genome-wide DNA methylation profiling of non-small cell lung carcinomas. Epigenetics Chromatin. 2012, 5: 9-10.1186/1756-8935-5-9.PubMedPubMedCentralCrossRef
75.
go back to reference Gu H, Bock C, Mikkelsen TS, Jager N, Smith ZD, Tomazou E, Gnirke A, Lander ES, Meissner A: Genome-scale DNA methylation mapping of clinical samples at single-nucleotide resolution. Nat Methods. 2010, 7: 133-136. 10.1038/nmeth.1414.PubMedPubMedCentralCrossRef Gu H, Bock C, Mikkelsen TS, Jager N, Smith ZD, Tomazou E, Gnirke A, Lander ES, Meissner A: Genome-scale DNA methylation mapping of clinical samples at single-nucleotide resolution. Nat Methods. 2010, 7: 133-136. 10.1038/nmeth.1414.PubMedPubMedCentralCrossRef
76.
go back to reference Kim JH, Dhanasekaran SM, Prensner JR, Cao X, Robinson D, Kalyana-Sundaram S, Huang C, Shankar S, Jing X, Iyer M, Hu M, Sam L, Grasso C, Maher CA, Palanisamy N, Mehra R, Kominsky HD, Siddiqui J, Yu J, Qin ZS, Chinnaiyan AM: Deep sequencing reveals distinct patterns of DNA methylation in prostate cancer. Genome Res. 2011, 21: 1028-1041. 10.1101/gr.119347.110.PubMedPubMedCentralCrossRef Kim JH, Dhanasekaran SM, Prensner JR, Cao X, Robinson D, Kalyana-Sundaram S, Huang C, Shankar S, Jing X, Iyer M, Hu M, Sam L, Grasso C, Maher CA, Palanisamy N, Mehra R, Kominsky HD, Siddiqui J, Yu J, Qin ZS, Chinnaiyan AM: Deep sequencing reveals distinct patterns of DNA methylation in prostate cancer. Genome Res. 2011, 21: 1028-1041. 10.1101/gr.119347.110.PubMedPubMedCentralCrossRef
77.
go back to reference Weng YI, Huang TH, Yan PS: Methylated DNA immunoprecipitation and microarray-based analysis: detection of DNA methylation in breast cancer cell lines. Methods Mol Biol. 2009, 590: 165-176. 10.1007/978-1-60327-378-7_10.PubMedPubMedCentralCrossRef Weng YI, Huang TH, Yan PS: Methylated DNA immunoprecipitation and microarray-based analysis: detection of DNA methylation in breast cancer cell lines. Methods Mol Biol. 2009, 590: 165-176. 10.1007/978-1-60327-378-7_10.PubMedPubMedCentralCrossRef
78.
go back to reference Ruike Y, Imanaka Y, Sato F, Shimizu K, Tsujimoto G: Genome-wide analysis of aberrant methylation in human breast cancer cells using methyl-DNA immunoprecipitation combined with high-throughput sequencing. BMC Genomics. 2010, 11: 137-10.1186/1471-2164-11-137.PubMedPubMedCentralCrossRef Ruike Y, Imanaka Y, Sato F, Shimizu K, Tsujimoto G: Genome-wide analysis of aberrant methylation in human breast cancer cells using methyl-DNA immunoprecipitation combined with high-throughput sequencing. BMC Genomics. 2010, 11: 137-10.1186/1471-2164-11-137.PubMedPubMedCentralCrossRef
79.
go back to reference Morita S, Takahashi RU, Yamashita R, Toyoda A, Horii T, Kimura M, Fujiyama A, Nakai K, Tajima S, Matoba R, Ochiya T, Hatada I: Genome-wide analysis of DNA methylation and expression of microRNAs in breast cancer cells. Int J Mol Sci. 2012, 13: 8259-8272. 10.3390/ijms13078259.PubMedPubMedCentralCrossRef Morita S, Takahashi RU, Yamashita R, Toyoda A, Horii T, Kimura M, Fujiyama A, Nakai K, Tajima S, Matoba R, Ochiya T, Hatada I: Genome-wide analysis of DNA methylation and expression of microRNAs in breast cancer cells. Int J Mol Sci. 2012, 13: 8259-8272. 10.3390/ijms13078259.PubMedPubMedCentralCrossRef
80.
go back to reference Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL: A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA. 1992, 89: 1827-1831. 10.1073/pnas.89.5.1827.PubMedPubMedCentralCrossRef Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL: A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA. 1992, 89: 1827-1831. 10.1073/pnas.89.5.1827.PubMedPubMedCentralCrossRef
81.
go back to reference Clark SJ, Harrison J, Paul CL, Frommer M: High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 1994, 22: 2990-2997. 10.1093/nar/22.15.2990.PubMedPubMedCentralCrossRef Clark SJ, Harrison J, Paul CL, Frommer M: High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 1994, 22: 2990-2997. 10.1093/nar/22.15.2990.PubMedPubMedCentralCrossRef
82.
go back to reference Colella S, Shen L, Baggerly KA, Issa JP, Krahe R: Sensitive and quantitative universal Pyrosequencing methylation analysis of CpG sites. Biotechniques. 2003, 35: 146-150.PubMed Colella S, Shen L, Baggerly KA, Issa JP, Krahe R: Sensitive and quantitative universal Pyrosequencing methylation analysis of CpG sites. Biotechniques. 2003, 35: 146-150.PubMed
83.
go back to reference Tost J, Dunker J, Gut IG: Analysis and quantification of multiple methylation variable positions in CpG islands by Pyrosequencing. Biotechniques. 2003, 35: 152-156.PubMed Tost J, Dunker J, Gut IG: Analysis and quantification of multiple methylation variable positions in CpG islands by Pyrosequencing. Biotechniques. 2003, 35: 152-156.PubMed
84.
go back to reference Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, Cantor CR, Field JK, van den Boom D: Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci USA. 2005, 102: 15785-15790. 10.1073/pnas.0507816102.PubMedPubMedCentralCrossRef Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, Cantor CR, Field JK, van den Boom D: Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci USA. 2005, 102: 15785-15790. 10.1073/pnas.0507816102.PubMedPubMedCentralCrossRef
85.
go back to reference Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ: Genomic profiling of CpG methylation and allelic specificity using quantitative highthroughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res. 2007, 35: e119-10.1093/nar/gkm662.PubMedPubMedCentralCrossRef Coolen MW, Statham AL, Gardiner-Garden M, Clark SJ: Genomic profiling of CpG methylation and allelic specificity using quantitative highthroughput mass spectrometry: critical evaluation and improvements. Nucleic Acids Res. 2007, 35: e119-10.1093/nar/gkm662.PubMedPubMedCentralCrossRef
86.
go back to reference Herman JG, Myohanen S, Nelkin BD, Baylin SB: Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA. 1996, 93: 9821-9826. 10.1073/pnas.93.18.9821.PubMedPubMedCentralCrossRef Herman JG, Myohanen S, Nelkin BD, Baylin SB: Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA. 1996, 93: 9821-9826. 10.1073/pnas.93.18.9821.PubMedPubMedCentralCrossRef
87.
go back to reference Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, Danenberg PV, Laird PW: MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 2000, 28: E32-10.1093/nar/28.8.e32.PubMedPubMedCentralCrossRef Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D, Danenberg PV, Laird PW: MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res. 2000, 28: E32-10.1093/nar/28.8.e32.PubMedPubMedCentralCrossRef
88.
go back to reference Kristensen LS, Mikeska T, Krypuy M, Dobrovic A: Sensitive Melting Analysis after Real Time- Methylation Specific PCR (SMART-MSP): high-throughput and probe-free quantitative DNA methylation detection. Nucleic Acids Res. 2008, 36: e42-10.1093/nar/gkn113.PubMedPubMedCentralCrossRef Kristensen LS, Mikeska T, Krypuy M, Dobrovic A: Sensitive Melting Analysis after Real Time- Methylation Specific PCR (SMART-MSP): high-throughput and probe-free quantitative DNA methylation detection. Nucleic Acids Res. 2008, 36: e42-10.1093/nar/gkn113.PubMedPubMedCentralCrossRef
89.
go back to reference Wojdacz TK, Dobrovic A: Methylation-sensitive high resolution melting (MS-HRM): a new approach for sensitive and high-throughput assessment of methylation. Nucleic Acids Res. 2007, 35: e41-10.1093/nar/gkm013.PubMedPubMedCentralCrossRef Wojdacz TK, Dobrovic A: Methylation-sensitive high resolution melting (MS-HRM): a new approach for sensitive and high-throughput assessment of methylation. Nucleic Acids Res. 2007, 35: e41-10.1093/nar/gkm013.PubMedPubMedCentralCrossRef
90.
go back to reference Bianco T, Hussey D, Dobrovic A: Methylation-sensitive, single-strand conformation analysis (MS-SSCA): a rapid method to screen for and analyze methylation. Hum Mutat. 1999, 14: 289-293. 10.1002/(SICI)1098-1004(199910)14:4<289::AID-HUMU3>3.0.CO;2-A.PubMedCrossRef Bianco T, Hussey D, Dobrovic A: Methylation-sensitive, single-strand conformation analysis (MS-SSCA): a rapid method to screen for and analyze methylation. Hum Mutat. 1999, 14: 289-293. 10.1002/(SICI)1098-1004(199910)14:4<289::AID-HUMU3>3.0.CO;2-A.PubMedCrossRef
91.
go back to reference Gonzalgo ML, Jones PA: Rapid quantitation of methylation differences at specific sites using methylation-sensitive single nucleotide primer extension (Ms-SNuPE). Nucleic Acids Res. 1997, 25: 2529-2531. 10.1093/nar/25.12.2529.PubMedPubMedCentralCrossRef Gonzalgo ML, Jones PA: Rapid quantitation of methylation differences at specific sites using methylation-sensitive single nucleotide primer extension (Ms-SNuPE). Nucleic Acids Res. 1997, 25: 2529-2531. 10.1093/nar/25.12.2529.PubMedPubMedCentralCrossRef
92.
go back to reference Gonzalgo ML, Jones PA: Quantitative methylation analysis using methylation-sensitive single-nucleotide primer extension (Ms-SNuPE). Methods. 2002, 27: 128-133. 10.1016/S1046-2023(02)00064-6.PubMedCrossRef Gonzalgo ML, Jones PA: Quantitative methylation analysis using methylation-sensitive single-nucleotide primer extension (Ms-SNuPE). Methods. 2002, 27: 128-133. 10.1016/S1046-2023(02)00064-6.PubMedCrossRef
93.
94.
go back to reference Nygren AO, Ameziane N, Duarte HM, Vijzelaar RN, Waisfisz Q, Hess CJ, Schouten JP, Errami A: Methylation-specific MLPA (MS-MLPA): simultaneous detection of CpG methylation and copy number changes of up to 40 sequences. Nucleic Acids Res. 2005, 33: e128-10.1093/nar/gni127.PubMedPubMedCentralCrossRef Nygren AO, Ameziane N, Duarte HM, Vijzelaar RN, Waisfisz Q, Hess CJ, Schouten JP, Errami A: Methylation-specific MLPA (MS-MLPA): simultaneous detection of CpG methylation and copy number changes of up to 40 sequences. Nucleic Acids Res. 2005, 33: e128-10.1093/nar/gni127.PubMedPubMedCentralCrossRef
95.
go back to reference Candiloro IL, Mikeska T, Hokland P, Dobrovic A: Rapid analysis of heterogeneously methylated DNA using digital methylation-sensitive high resolution melting: application to the CDKN2B (p15) gene. Epigenetics Chromatin. 2008, 1: 7-10.1186/1756-8935-1-7.PubMedPubMedCentralCrossRef Candiloro IL, Mikeska T, Hokland P, Dobrovic A: Rapid analysis of heterogeneously methylated DNA using digital methylation-sensitive high resolution melting: application to the CDKN2B (p15) gene. Epigenetics Chromatin. 2008, 1: 7-10.1186/1756-8935-1-7.PubMedPubMedCentralCrossRef
96.
go back to reference Candiloro IL, Dobrovic A: Detection of MGMT promoter methylation in normal individuals is strongly associated with the T allele of the rs16906252 MGMT promoter single nucleotide polymorphism. Cancer Prev Res (Phila). 2009, 2: 862-867. 10.1158/1940-6207.CAPR-09-0056.CrossRef Candiloro IL, Dobrovic A: Detection of MGMT promoter methylation in normal individuals is strongly associated with the T allele of the rs16906252 MGMT promoter single nucleotide polymorphism. Cancer Prev Res (Phila). 2009, 2: 862-867. 10.1158/1940-6207.CAPR-09-0056.CrossRef
97.
go back to reference Li M, Chen WD, Papadopoulos N, Goodman SN, Bjerregaard NC, Laurberg S, Levin B, Juhl H, Arber N, Moinova H, Durkee K, Schmidt K, He Y, Diehl F, Velculescu VE, Zhou S, Diaz LA, Kinzler KW, Markowitz SD, Vogelstein B: Sensitive digital quantification of DNA methylation in clinical samples. Nat Biotechnol. 2009, 27: 858-863. 10.1038/nbt.1559.PubMedPubMedCentralCrossRef Li M, Chen WD, Papadopoulos N, Goodman SN, Bjerregaard NC, Laurberg S, Levin B, Juhl H, Arber N, Moinova H, Durkee K, Schmidt K, He Y, Diehl F, Velculescu VE, Zhou S, Diaz LA, Kinzler KW, Markowitz SD, Vogelstein B: Sensitive digital quantification of DNA methylation in clinical samples. Nat Biotechnol. 2009, 27: 858-863. 10.1038/nbt.1559.PubMedPubMedCentralCrossRef
98.
go back to reference Graff JR, Gabrielson E, Fujii H, Baylin SB, Herman JG: Methylation patterns of the E-cadherin 5' CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J Biol Chem. 2000, 275: 2727-2732. 10.1074/jbc.275.4.2727.PubMedCrossRef Graff JR, Gabrielson E, Fujii H, Baylin SB, Herman JG: Methylation patterns of the E-cadherin 5' CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J Biol Chem. 2000, 275: 2727-2732. 10.1074/jbc.275.4.2727.PubMedCrossRef
99.
go back to reference Pu RT, Laitala LE, Alli PM, Fackler MJ, Sukumar S, Clark DP: Methylation profiling of benign and malignant breast lesions and its application to cytopathology. Mod Pathol. 2003, 16: 1095-1101. 10.1097/01.MP.0000095782.79895.E2.PubMedCrossRef Pu RT, Laitala LE, Alli PM, Fackler MJ, Sukumar S, Clark DP: Methylation profiling of benign and malignant breast lesions and its application to cytopathology. Mod Pathol. 2003, 16: 1095-1101. 10.1097/01.MP.0000095782.79895.E2.PubMedCrossRef
100.
go back to reference Pasquali L, Bedeir A, Ringquist S, Styche A, Bhargava R, Trucco G: Quantification of CpG island methylation in progressive breast lesions from normal to invasive carcinoma. Cancer Lett. 2007, 257: 136-144. 10.1016/j.canlet.2007.07.010.PubMedCrossRef Pasquali L, Bedeir A, Ringquist S, Styche A, Bhargava R, Trucco G: Quantification of CpG island methylation in progressive breast lesions from normal to invasive carcinoma. Cancer Lett. 2007, 257: 136-144. 10.1016/j.canlet.2007.07.010.PubMedCrossRef
101.
go back to reference Alvarez C, Tapia T, Cornejo V, Fernandez W, Munoz A, Camus M, Alvarez M, Devoto L, Carvallo P: Silencing of tumor suppressor genes RASSF1A, SLIT2, and WIF1 by promoter hypermethylation in hereditary breast cancer. Mol Carcinog. 2013, 52: 475-487. 10.1002/mc.21881.PubMedCrossRef Alvarez C, Tapia T, Cornejo V, Fernandez W, Munoz A, Camus M, Alvarez M, Devoto L, Carvallo P: Silencing of tumor suppressor genes RASSF1A, SLIT2, and WIF1 by promoter hypermethylation in hereditary breast cancer. Mol Carcinog. 2013, 52: 475-487. 10.1002/mc.21881.PubMedCrossRef
Metadata
Title
DNA methylation in ductal carcinoma in situof the breast
Authors
Jia-Min B Pang
Alexander Dobrovic
Stephen B Fox
Publication date
01-06-2013
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 3/2013
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/bcr3420

Other articles of this Issue 3/2013

Breast Cancer Research 3/2013 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine