Epigenetic progression of columnar cell lesions of the breast to invasive breast cancer

Breast Cancer Research and Treatment

Volumn 136, Issue 3, 2012, Pages 705-715

  Verschuur Maes, Anoek H J ^a   De Bruin, Peter C ^b   Van Diest, Paul J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ST ANTONIUS HOSPITAL   (Netherlands)

Author keywords

Breast; Columnar cell lesions; Flat epithelial atypia; Methylation; MS MLPA

Indexed keywords

CYCLIN D2; SECRETED FRIZZLED RELATED PROTEIN 5; CADHERIN; CCND2 PROTEIN, HUMAN; CYTOKINE; H CADHERIN; H-CADHERIN; ID4 PROTEIN, HUMAN; INHIBITOR OF DIFFERENTIATION PROTEIN; RASSF1 PROTEIN, HUMAN; SCGB3A1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CADHERIN 13 GENE; CANCER GENETICS; CANCER GRADING; CANCER GROWTH; CELL DAMAGE; CLINICAL ARTICLE; COLUMNAR CELL LESION; CYCLIN D2 GENE; EPIGENETICS; FEMALE; GENE FREQUENCY; HUMAN; HUMAN TISSUE; INHIBITOR OF DNA BINDING 4 GENE; INTRADUCTAL CARCINOMA; METHYLATION; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; PRIORITY JOURNAL; PROMOTER REGION; RAS ASSOCIATED DOMAIN FAMILY 1 GENE; SECRETED FRIZZLED RELATED PROTEIN 5 GENE; SECRETOGLOBULIN FAMILY 3A GENE; TUMOR INVASION; TUMOR SUPPRESSOR GENE; BREAST TUMOR; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; MAMMARY GLAND; MIDDLE AGED; MULTIPLEX POLYMERASE CHAIN REACTION; PATHOLOGY; PRECANCER; REFERENCE VALUE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BREAST NEOPLASMS; CADHERINS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CYCLIN D2; CYTOKINES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; MAMMARY GLANDS, HUMAN; MIDDLE AGED; MULTIPLEX POLYMERASE CHAIN REACTION; PRECANCEROUS CONDITIONS; PROMOTER REGIONS, GENETIC; REFERENCE VALUES; TUMOR SUPPRESSOR PROTEINS;

EID: 84878769859     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-012-2301-4     Document Type: Article

References (54)

1. Allred DC, Mohsin SK, Fuqua SA (2001) Histological and biological evolution of human premalignant breast disease. Endocr Relat Cancer 8:47-61
2. Lee S, Medina D, Tsimelzon A, Mohsin SK, Mao S, Wu Y, Allred DC (2007) Alterations of gene expression in the development of early hyperplastic precursors of breast cancer. Am J Pathol 171:252-262
3. Simpson PT, Gale T, Reis-Filho JS, Jones C, Parry S, Sloane JP, Hanby A, Pinder SE, Lee AH, Humphreys S, Ellis IO, Lakhani SR (2005) Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am J Surg Pathol 29:734-746
4. Sinn HP (2009) Breast cancer precursors: lessons learned from molecular genetics. J Mol Med 87:113-115
5. Schnitt SJ, Vincent-Salomon A (2003) Columnar cell lesions of the breast. Adv Anat Pathol 10:113-124
6. Tavassoli FA, Devilee P (2003) WHO classification tumours of the breast and female genital organs. IARC, Lyon
7. Feeley L, Quinn CM (2008) Columnar cell lesions of the breast. Histopathology 52:11-19
8. Verschuur-Maes AHJ, Van Deurzen CHM, Monninkhof EM, van Diest PJ (2011) Columnar cell lesions on breast needle biopsies: is surgical excision necessary? A systematic review. Ann Surg 255:259-265
9. Aulmann S, Elsawaf Z, Penzel R, Schirmacher P, Sinn HP (2009) Invasive tubular carcinoma of the breast frequently is clonally related to flat epithelial atypia and low-grade ductal carcinoma in situ. Am J Surg Pathol 33:1646-1653
10. Dabbs DJ, Carter G, Fudge M, Peng Y, Swalsky P, Finkelstein S (2006) Molecular alterations in columnar cell lesions of the breast. Mod Pathol 19:344-349
11. Moinfar F, Man YG, Bratthauer GL, Ratschek M, Tavassoli FA (2000) Genetic abnormalities in mammary ductal intraepithelial neoplasia-flat type ("clinging ductal carcinoma in situ"): a simulator of normal mammary epithelium. Cancer 88:2072-2081
12. Buyru N, Altinisik J, Ozdemir F, Demokan S, Dalay N (2009) Methylation profiles in breast cancer. Cancer Invest 27:307-312
13. Esteller M, Silva JM, Dominguez G, Bonilla F, Matias-Guiu X, Lerma E, Bussaglia E, Prat J, Harkes IC, Repasky EA, Gabrielson E, Schutte M, Baylin SB, Herman JG (2000) Promoter hypermethylation and BRCA1 inactivation in sporadic breast and ovarian tumors. J Natl Cancer Inst 92:564-569
14. Jones PA, Baylin SB (2007) The epigenomics of cancer. Cell 128:683-692
15. Jovanovic J, Ronneberg JA, Tost J, Kristensen V (2010) The epigenetics of breast cancer. Mol Oncol 4:242-254
16. Marzese DM, Gago FE, Vargas-Roig LM, Roque M (2010) Simultaneous analysis of the methylation profile of 26 cancer related regions in invasive breast carcinomas by MS-MLPA and drMS-MLPA. Mol Cell Probes 24:271-280
17. Widschwendter M, Jones PA (2002) DNA methylation and breast carcinogenesis. Oncogene 21:5462-5482
18. 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 (2009) Changes in CpG islands promoter methylation patterns during ductal breast carcinoma progression. Cancer Epidemiol Biomarkers Prev 18:2694-2700
19. Liu T, Niu Y, Feng Y, Niu R, Yu Y, Lv A, Yang Y (2008) Methylation of CpG islands of p16(INK4a) and cyclinD1 overexpression associated with progression of intraductal proliferative lesions of the breast. Hum Pathol 39:1637-1646
20. Park SY, Kwon HJ, Lee HE, Ryu HS, Kim SW, Kim JH, Kim IA, Jung N, Cho NY, Kang GH (2011) Promoter CpG island hypermethylation during breast cancer progression. Virchows Arch 458:73-84
21. van Diest PJ (2002) No consent should be needed for using leftover body material for scientific purposes. BMJ 325:648-651
22. Bol GM, Suijkerbuijk KP, Bart J, Vooijs M, van der Wall E, van Diest PJ (2010) Methylation profiles of hereditary and sporadic ovarian cancer. Histopathology 57:363-370
23. Seeber LM, Zweemer RP, Marchionni L, Massuger LF, Smit VT, van Baal WM, Verheijen RH, van Diest PJ (2010) Methylation profiles of endometrioid and serous endometrial cancers. Endocr Relat Cancer 17:663-673
24. Suijkerbuijk KP, Pan X, Van der Wall E, van Diest PJ, Vooijs M (2010) Comparison of different promoter methylation assays in breast cancer. Anal Cell Pathol (Amst) 33:133-141
25. van Diest PJ, Suijkerbuijk KP, Koop EA, de Weger RA, Van der Wall E (2010) Low levels of BNIP3 promoter hypermethylation in invasive breast cancer. Anal Cell Pathol (Amst) 33:175-176
26. Gylling A, Abdel-Rahman WM, Juhola M, Nuorva K, Hautala E, Jarvinen HJ, Mecklin JP, Aarnio M, Peltomaki P (2007) Is gastric cancer part of the tumour spectrum of hereditary non-polyposis colorectal cancer? A molecular genetic study. Gut 56:926-933
27. Joensuu EI, Abdel-Rahman WM, Ollikainen M, Ruosaari S, Knuutila S, Peltomaki P (2008) Epigenetic signatures of familial cancer are characteristic of tumor type and family category. Cancer Res 68:4597-4605
28. Suijkerbuijk KP, Fackler MJ, Sukumar S, van Gils CH, van Laar T, Van der Wall E, Vooijs M, van Diest PJ (2008) Methylation is less abundant in BRCA1-associated compared with sporadic breast cancer. Ann Oncol 19:1870-1874
29. Liu T, Niu Y, Feng Y, Niu R, Yu Y, Lv A, Yang Y (2008) Methylation of CpG islands of p16(INK4a) and cyclinD1 overexpression associated with progression of intraductal proliferative lesions of the breast. Hum Pathol 39:1637-1646
30. O'Connell P, Pekkel V, Fuqua SA, Osborne CK, Clark GM, Allred DC (1998) Analysis of loss of heterozygosity in 399 premalignant breast lesions at 15 genetic loci. J Natl Cancer Inst 90:697-703
31. Simpson PT, Gale T, Reis-Filho JS, Jones C, Parry S, Sloane JP, Hanby A, Pinder SE, Lee AH, Humphreys S, Ellis IO, Lakhani SR (2005) Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am J Surg Pathol 29:734-746
32. Qi L, Bart J, Tan LP, Platteel I, Sluis T, Huitema S, Harms G, Fu L, Hollema H, Berg A (2009) Expression of miR-21 and its targets (PTEN, PDCD4, TM1) in flat epithelial atypia of the breast in relation to ductal carcinoma in situ and invasive carcinoma. BMC Cancer 9:163
33. Ellsworth RE, Ellsworth DL, Weyandt JD, Fantacone-Campbell JL, Deyarmin B, Hooke JA, Shriver CD (2010) Chromosomal alterations in pure nonneoplastic breast lesions: implications for breast cancer progression. Ann Surg Oncol 17:1688-1694
34. Subramaniam MM, Chan JY, Omar MF, Ito K, Ito Y, Yeoh KG, Salto-Tellez M, Putti TC (2010) Lack of RUNX3 inactivation in columnar cell lesions of breast. Histopathology 57:555-563
35. Fackler MJ, McVeigh M, Evron E, Garrett E, Mehrotra J, Polyak K, Sukumar S, Argani P (2003) DNA methylation of RASSF1A, HIN-1, RAR-beta, Cyclin D2 and Twist in in situ and invasive lobular breast carcinoma. Int J Cancer 107:970-975
36. Moelans CB, de Weger RA, Monsuur HN, Maes AH, van Diest PJ (2010) Molecular differences between ductal carcinoma in situ and adjacent invasive breast carcinoma: a multiplex ligation-dependent probe amplification study. Anal Cell Pathol (Amst) 33:165-173
37. Muggerud AA, Ronneberg JA, Warnberg F, Botling J, Busato F, Jovanovic J, Solvang H, Bukholm I, Borresen-Dale AL, Kristensen VN, Sorlie T, Tost J (2010) Frequent aberrant DNA methylation of ABCB1, FOXC1, PPP2R2B and PTEN in ductal carcinoma in situ and early invasive breast cancer. Breast Cancer Res 12:R3
38. Bertolo C, Guerrero D, Vicente F, Cordoba A, Esteller M, Ropero S, Guillen-Grima F, Martinez-Penuela JM, Lera JM (2008) Differences and molecular immunohistochemical parameters in the subtypes of infiltrating ductal breast cancer. Am J Clin Pathol 130:414-424
39. Burbee DG, Forgacs E, Zochbauer-Muller S, Shivakumar L, Fong K, Gao B, Randle D, Kondo M, Virmani A, Bader S, Sekido Y, Latif F, Milchgrub S, Toyooka S, Gazdar AF, Lerman MI, Zabarovsky E, White M, Minna JD (2001) Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression. J Natl Cancer Inst 93:691-699
40. Chen CM, Chen HL, Hsiau TH, Hsiau AH, Shi H, Brock GJ, Wei SH, Caldwell CW, Yan PS, Huang TH (2003) Methylation target array for rapid analysis of CpG island hypermethylation in multiple tissue genomes. Am J Pathol 163:37-45
41. Feng W, Orlandi R, Zhao N, Carcangiu ML, Tagliabue E, Xu J, Bast RC Jr, Yu Y (2010) Tumor suppressor genes are frequently methylated in lymph node metastases of breast cancers. BMC Cancer 10:378
42. Honorio S, Agathanggelou A, Schuermann M, Pankow W, Viacava P, Maher ER, Latif F (2003) Detection of RASSF1A aberrant promoter hypermethylation in sputum from chronic smokers and ductal carcinoma in situ from breast cancer patients. Oncogene 22:147-150
43. Lee JS, Fackler MJ, Teo WW, Lee JH, Choi C, Park MH, Yoon JH, Zhang Z, Argani P, Sukumar S (2008) Quantitative promoter hypermethylation profiles of ductal carcinoma in situ in North American and Korean women: potential applications for diagnosis. Cancer Biol Ther 7:1398-1406
44. Pasquali L, Bedeir A, Ringquist S, Styche A, Bhargava R, Trucco G (2007) Quantification of CpG island methylation in progressive breast lesions from normal to invasive carcinoma. Cancer Lett 257:136-144
45. Shinozaki M, Hoon DS, Giuliano AE, Hansen NM, Wang HJ, Turner R, Taback B (2005) Distinct hypermethylation profile of primary breast cancer is associated with sentinel lymph node metastasis. Clin Cancer Res 11:2156-2162
46. Noetzel E, Veeck J, Niederacher D, Galm O, Horn F, Hartmann A, Knuchel R, Dahl E (2008) Promoter methylation-associated loss of ID4 expression is a marker of tumour recurrence in human breast cancer. BMC Cancer 8:154
47. Umetani N, Mori T, Koyanagi K, Shinozaki M, Kim J, Giuliano AE, Hoon DS (2005) Aberrant hypermethylation of ID4 gene promoter region increases risk of lymph node metastasis in T1 breast cancer. Oncogene 24:4721-4727
48. Evron E, Umbricht CB, Korz D, Raman V, Loeb DM, Niranjan B, Buluwela L, Weitzman SA, Marks J, Sukumar S (2001) Loss of cyclin D2 expression in the majority of breast cancers is associated with promoter hypermethylation. Cancer Res 61:2782-2787
49. Li S, Rong M, Iacopetta B (2006) DNA hypermethylation in breast cancer and its association with clinicopathological features. Cancer Lett 237:272-280
50. Parrella P, Poeta ML, Gallo AP, Prencipe M, Scintu M, Apicella A, Rossiello R, Liguoro G, Seripa D, Gravina C, Rabitti C, Rinaldi M, Nicol T, Tommasi S, Paradiso A, Schittulli F, Altomare V, Fazio VM (2004) Nonrandom distribution of aberrant promoter methylation of cancer-related genes in sporadic breast tumors. Clin Cancer Res 10:5349-5354
51. Shigematsu H, Suzuki M, Takahashi T, Miyajima K, Toyooka S, Shivapurkar N, Tomlinson GE, Mastrangelo D, Pass HI, Brambilla E, Sathyanarayana UG, Czerniak B, Fujisawa T, Shimizu N, Gazdar AF (2005) Aberrant methylation of HIN-1 (high in normal-1) is a frequent event in many human malignancies. Int J Cancer 113:600-604
52. Toyooka KO, Toyooka S, Virmani AK, Sathyanarayana UG, Euhus DM, Gilcrease M, Minna JD, Gazdar AF (2001) Loss of expression and aberrant methylation of the CDH13 (H-cadherin) gene in breast and lung carcinomas. Cancer Res 61:4556-4560
53. Suzuki H, Toyota M, Carraway H, Gabrielson E, Ohmura T, Fujikane T, Nishikawa N, Sogabe Y, Nojima M, Sonoda T, Mori M, Hirata K, Imai K, Shinomura Y, Baylin SB, Tokino T (2008) Frequent epigenetic inactivation of Wnt antagonist genes in breast cancer. Br J Cancer 98:1147-1156
54. Veeck J, Geisler C, Noetzel E, Alkaya S, Hartmann A, Knuchel R, Dahl E (2008) Epigenetic inactivation of the secreted frizzled-related protein-5 (SFRP5) gene in human breast cancer is associated with unfavorable prognosis. Carcinogenesis 29:991-998