Precursors and preinvasive lesions of the breast: The role of molecular prognostic markers in the diagnostic and therapeutic dilemma

World Journal of Surgical Oncology

Volumn 5, Issue , 2007, Pages

  Zagouri, Flora ^a   Sergentanis, Theodoros N ^a   Zografos, George C ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; KI 67 ANTIGEN; MOLECULAR MARKER; PROTEIN 14 3 3; PROTEIN BCL 2; PROTEIN P16INK4A; PROTEIN P53; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN; VASCULOTROPIN; TUMOR MARKER;

ANGIOGENESIS; BREAST CARCINOMA; BREAST DISEASE; BREAST HYPERPLASIA; BREAST TUMOR; CANCER RISK; CARCINOMA IN SITU; DIAGNOSTIC VALUE; DISEASE CLASSIFICATION; GENETIC PREDISPOSITION; HUMAN; INTRADUCTAL CARCINOMA; INVASIVE CARCINOMA; MEDICAL DECISION MAKING; MOLECULAR EVOLUTION; PATHOGENESIS; PATHOPHYSIOLOGY; PROGNOSIS; REVIEW; TREATMENT PLANNING; CANCER DIAGNOSIS; CANCER INVASION; FEMALE; MOLECULAR BIOLOGY; PAGET NIPPLE DISEASE; PATHOLOGY; PRECANCER; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; SURVIVAL;

BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; EARLY DETECTION OF CANCER; FEMALE; HUMANS; MOLECULAR BIOLOGY; NEOPLASM INVASIVENESS; PRECANCEROUS CONDITIONS; PROGNOSIS; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; SURVIVAL ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 34347326186     PISSN: None     EISSN: 14777819     Source Type: Journal    
DOI: 10.1186/1477-7819-5-57     Document Type: Review

References (161)

1. Pinder SE Ellis IO The diagnosis and management of pre-invasive breast disease: Ductal carcinoma in situ (DCIS) and atypical ductal hyperplasia (ADH)-current definitions and classification Breast Cancer Res 2003 5 254-257 314427 12927035 10.1186/bcr623
2. Van de Vijver MJ Peterse H The diagnosis and management of pre-invasive breast disease: Pathological diagnosis - problems with existing classifications Breast Cancer Res 2003 5 269 314433 12927038 10.1186/ bcr629
3. Purushotham AD The diagnosis and management of pre-invasive breast disease: Problems associated with management of pre-invasive lesions Breast Cancer Res 2003 5 309-312 314409 14580248 10.1186/bcr649
4. Reis-Filho JS Lakhani SR The diagnosis and management of pre-invasive breast disease: Genetic alterations in pre-invasive lesions Breast Cancer Res 2003 5 313-319 314410 14580249 10.1186/bcr650
5. Jeffrey SS Pollack JR The diagnosis and management of pre-invasive breast disease: Promise of new technologies in understanding pre-invasive breast lesions Breast Cancer Res 2003 5 320-328 314415 14580250 10.1186/bcr655
6. Betsill WL Jr Rosen PP Lieberman PH Robbins GF Intraductal carcinoma. Long-term follow-up after treatment by biopsy alone JAMA 1978 239 1863-1867 10.1001/jama.239.18.1863 205686
7. Page DL Dupont WD Rogers LW Landenberger M Intraductal carcinoma of the breast: Follow-up after biopsy only Cancer 1982 49 751-758 10.1002/ 1097-0142(19820215)49:4<751::AID-CNCR2820490426>3.0.CO;2-Y 6275978
8. Schnitt SJ The diagnosis and management of pre-invasive breast disease: flat epithelial atypia - classification, pathologic features and clinical significance Breast Cancer Res 2003 5 263-268 314429 12927037 10.1186/bcr625
9. Boecker W Moll R Dervan P Buerger H Poremba C Diallo RI Herbst H Schmidt A Lerch MM Buchwalow IB Usual ductal hyperplasia of the breast is a committed stem (progenitor) cell lesion distinct from atypical ductal hyperplasia and ductal carcinoma in situ J Pathol 2002 198 458-467 10.1002/path.1241 12434415
10. Dupont WD Parl FF Hartmann WH Brinton LA Winfield AC Worrell JA Schuyler PA Plummer WD Breast cancer risk associated with proliferative breast disease and atypical hyperplasia Cancer 1993 71 1258-1265 10.1002/ 1097-0142(19930215)71:4<1258::AID-CNCR2820710415>3.0.CO;2-I 8435803
11. Oyama T Maluf H Koerner F Atypical cystic lobules: An early stage in the formation of low-grade ductal carcinoma in situ Virchows Arch 1999 435 413-421 10.1007/s004280050419 10526005
12. Locke I Mitchell G Eeles R Ductal approaches to assessment and management of women at high risk for developing breast cancer Breast Cancer Res 2004 6 75-81 400658 14979910 10.1186/bcr759
13. Sloane JP Ellman R Anderson TJ Brown CL Coyne J Dallimore NS Davies JD Eakins D Ellis IO Elston CW Consistency of histopathological reporting of breast lesions detected by screening: Findings of the U.K. National External Quality Assessment (EQA) Scheme. U. K. National Coordinating Group for Breast. Screening Pathology Eur J Cancer 1994 30A 1414-1419 10.1016/0959-8049(94)00261-3 7833094
14. European Commission European Guidelines for Quality Assurance in Mammography Screening Luxembourg: Office for Official Publications of the European Communities 2 1996
15. Zografos GC Panou M Panou N Common risk factors of breast and ovarian cancer: Recent view Int J Gynecol Cancer 2004 14 721-740 10.1111/ j.1048-891X.2004.14503.x 15361179
16. Lagios MD Heterogeneity of duct carcinoma in situ (DCIS): Relationship of grade and subtype analysis to local recurrence and risk of invasive transformation Cancer Lett 1995 90 97-102 10.1016/0304-3835(94)03683-A 7720048
17. Ketcham AS Moffat FL Vexed surgeons, perplexed patients, and breast cancers which may not be cancer Cancer 1990 65 387-393 10.1002/ 1097-0142(19900201)65:3<387::AID-CNCR2820650302>3.0.CO;2-Y 2404554
18. Lishman SC Lakhani SR Atypical lobular hyperplasia and lobular carcinoma in situ: Surgical and molecular pathology Histopathology 1999 35 195-200 10.1046/j.1365-2559.1999.00815.x 10469210
19. Lu YJ Osin P Lakhani SR Di Palma S Gusterson BA Shipley JM Comparative genomic hybridization analysis of lobular carcinoma in situ and atypical lobular hyperplasia and potential roles for gains and losses of genetic material in breast neoplasia Cancer Res 1998 58 4721-4727 9788628
20. Page DL Schuyler PA Dupont WD Jensen RA Plummer WD Jr Simpson JF Atypical lobular hyperplasia as a unilateral predictor of breast cancer risk: A retrospective cohort study Lancet 2003 361 125-129 10.1016/ S0140-6736(03)12230-1 12531579
21. Buerger H Otterbach F Simon R Poremba C Diallo R Decker T Riethdorf L Brinkschmidt C Dockhorn-Dworniczak B Boecker W Comparative genomic hybridization of ductal carcinoma in situ of the breast-evidence of multiple genetic pathways J Pathol 1999 187 396-402 10.1002/ (SICI)1096-9896(199903)187:4<396::AID-PATH286>3.0.CO;2-L 10398097
22. Dupont WD Page DL Risk factors for breast cancer in women with proliferative breast disease N Engl J Med 1985 312 146-151 3965932
23. Allred DC Mohsin SK Fuqua SA Histological and biological evolution of human premalignant breast disease Endocr Relat Cancer 2001 8 47-61 10.1677/erc.0.0080047 11350726
24. Moinfar F Man YG Bratthauer GL Ratschek M Tavassoli FA Genetic abnormalities in mammary ductal intraepithelial neoplasia-flat type ("clinging ductal carcinoma in situ"): A simulator of normal mammary epithelium Cancer 2000 88 2072-2081 10.1002/ (SICI)1097-0142(20000501)88:9<2072::AID-CNCR13>3.0.CO;2-H 10813719
25. O'Connell P Pekkel V Fuqua SA Osborne CK Clark GM Allred DC Analysis of loss of heterozygosity in 399 premalignant breast lesions at 15 genetic loci J Natl Cancer Inst 1998 90 697-703 10.1093/jnci/90.9.697 9586667
26. Noguchi S Motomura K Inaji H Imaoka S Koyama H Clonal analysis of predominantly intraductal carcinoma and precancerous lesions of the breast by means of polymerase chain reaction Cancer Res 1994 54 1849-1853 7907946
27. Amari M Suzuki A Moriya T Yoshinaga K Amano G Sasano H Ohuchi N Satomi S Horii A LOH analyses of premalignant and malignant lesions of human breast: Frequent LOH in 8p, 16q, and 17q in atypical ductal hyperplasia Oncol Rep 1999 6 1277-1280 10523696
28. Gong G DeVries S Chew KL Cha I Ljung BM Waldman FM Genetic changes in paired atypical and usual ductal hyperplasia of the breast by comparative genomic hybridization Clin Cancer Res 2001 7 2410-2414 11489820
29. Moll R Franke WW Schiller DL Geiger B Krepler R The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells Cell 1982 31 11-24 10.1016/0092-8674(82)90400-7 6186379
30. Achtstaetter T Hatzfeld M Quinlan RA Parmelee DC Franke WW Separation of cytokeratin polypeptides by gel electrophoretic and chromatographic techniques and their identification by immunoblotting Methods Enzymol 1986 134 355-371 2434826
31. Moinfar F Man YG Lininger RA Bodian C Tavassoli FA Use of keratin 35betaE12 as an adjunct in the diagnosis of mammary intraepithelial neoplasia-ductal type - benign and malignant intraductal proliferations Am J Surg Pathol 1999 23 1048-1058 10.1097/00000478-199909000-00007 10478664
32. Aldaz CM Chen T Sahin A Cunningham J Bondy M Comparative allelotype of in situ and invasive human breast cancer: High frequency of microsatellite instability in lobular breast carcinomas Cancer Res 1995 55 3976-3981 7664266
33. Tsuda H Fukutomi T Hirohashi S Pattern of gene alterations in intraductal breast neoplasms associated with histological type and grade Clin Cancer Res 1995 1 261-267 9815981
34. Cleton-Jansen AM Moerland HW Callen DF Doggett NA Devilee P Cornelisse CJ Mapping of the breast basic conserved gene (D16S444E) to human chromosome band 16q24.3 Cytogenet Cell Genet 1995 68 49-51 7956357
35. Rosai J Borderline epithelial lesions of the breast Am J Surg Pathol 1991 15 209-221 1847606
36. Tavassoli FA Ductal carcinoma in situ: Introduction of the concept of ductal intraepithelial neoplasia Mod Pathol 1998 11 140-154 9504685
37. Page DL Dupont WD Rogers LW Landenberger M Intraductal carcinoma of the breast: Follow-up after biopsy only Cancer 1982 49 751-758 10.1002/ 1097-0142(19820215)49:4<751::AID-CNCR2820490426>3.0.CO;2-Y 6275978
38. 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 11857490
39. Leong AS Sormunen RT Vinyuvat S Hamdani RW Suthipintawong C Biologic markers in ductal carcinoma in situ and concurrent infiltrating carcinoma. A comparison of eight contemporary grading systems Am J Clin Pathol 2001 115 709-718 10.1309/WBU9-22QN-C3NA-2Q12 11345835
40. Lakhani SR Collins N Stratton MR Sloane JP Atypical ductal hyperplasia of the breast: Clonal proliferation with loss of heterozygosity on chromosomes 16q and 17p J Clin Pathol 1995 48 611-615 502709 7560165
41. Lakhani SR Slack DN Hamoudi RA Collins N Stratton MR Sloane JP Detection of allelic imbalance indicates that a proportion of mammary hyperplasia of usual type are clonal, neoplastic proliferations Lab Invest 1996 74 129-135 8569175
42. Buerger H Otterbach F Simon R Schafer KL Poremba C Diallo R Brinkschmidt C Dockhorn-Dworniczak B Boecker W Different genetic pathways in the evolution of invasive breast cancer are associated with distinct morphological subtypes J Pathol 1999 189 521-526 10.1002/ (SICI)1096-9896(199912)189:4<521::AID-PATH472>3.0.CO;2-B 10629552
43. Nissan A Jager D Roystacher M Prus D Peretz T Eisenberg I Freund HR Scanlan M Ritter G Old LJ Mitrani-Rosenbaum S Multimarker RT-PCR assay for the detection of minimal residual disease in sentinel lymph nodes of breast cancer patients Br J Cancer 2006 94 681-685 16495929
44. Silverstein MJ Craig PH Lagios MD Waisman JK Lewinsky BS Colburn WJ Poller DN Developing a prognostic index for ductal carcinoma in situ of the breast. Are we there yet? Cancer 1996 78 1138-1140 10.1002/ (SICI)1097-0142(19960901)78:5<1138::AID-CNCR27>3.0.CO;2-2 8780555
45. Henderson BE Ross R Bernstein L Estrogens as a cause of human cancer: the Richard and Hinda Rosenthal Foundation award lecture Cancer Res 1998 48 246-253
46. Pike MC Spicer DV Dahmoush L Press MF Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk Epidemiol Rev 1993 15 17-35 8405201
47. Ali S Coombes RC Estrogen receptor alpha in human breast cancer: occurrence and significance J Mammary Gland Biol Neoplasia 2000 5 271-281 10.1023/A:1009594727358 14973389
48. Petersen OW Hoyer PE van Deurs B Frequency and distribution of estrogen receptor-positive cells in normal, nonlactating human breast tissue Cancer Res 1987 47 5748-5751 3664479
49. Clarke RB Howell A Potten CS Anderson E Dissociation between steroid receptor expression and cell proliferation in the human breast Cancer Res 1997 57 4987-4991 9371488
50. Shoker BS Jarvis C Clarke RB Anderson E Hewlett J Davies MP Sibson DR Sloane JP Estrogen receptor-positive proliferating cells in the normal and precancerous breast Am J Pathol 1999 155 1811-1815 10595909
51. Khan SA Rogers MA Khurana KK Meguid MM Numann PJ Estrogen receptor expression in benign breast epithelium and breast cancer risk J Natl Cancer Inst 1998 90 37-42 10.1093/jnci/90.1.37 9428781
52. Iqbal M Davies MP Shoker BS Jarvis C Sibson DR Sloane JP Subgroups of non-atypical hyperplasia of breast defined by proliferation of oestrogen receptor-positive cells J Pathol 2001 193 333-338 10.1002/ 1096-9896(2000)9999:9999<::AID-PATH801>3.0.CO;2-# 11241412
53. Gobbi H Dupont WD Parl FF Schuyler PA Plummer WD Olson SJ Page DL Breast cancer risk associated with estrogen receptor expression in epithelial hyperplasia lacking atypia and adjacent lobular units Int J Cancer 2005 113 857-859 10.1002/ijc.20632 15499614
54. Shoker BS Jarvis C Clarke RB Anderson E Munro C Davies MP Sibson DR Sloane JP Abnormal regulation of the oestrogen receptor in benign breast lesions J Clin Pathol 2000 53 778-783 10.1136/jcp.53.10.778 11064673
55. McLaren BK Gobbi H Schuyler PA Olson SJ Parl FF Dupont WD Page DL Immunohistochemical expression of estrogen receptor in enlarged lobular units with columnar alteration in benign breast biopsies: A nested case-control study Am J Surg Pathol 2005 29 105-108 10.1097/ 01.pas.0000146013.76881.d9 15613861
56. Bose S Lesser ML Norton L Rosen PP Immunophenotype of intraductal carcinoma Arch Pathol Lab Med 1996 120 81-85 8554451
57. Karayiannakis AJ Bastounis EA Chatzigianni EB Makri GG Alexiou D Karamanakos P Immunohistochemical detection of oestrogen receptors in ductal carcinoma in situ of the breast Eur J Surg Oncol 1996 22 578-582 10.1016/S0748-7983(96)92242-8 9005143
58. Roger P Sahla ME Makela S Gustafsson JA Baldet P Rochefort H Decreased expression of estrogen receptor beta protein in proliferative preinvasive mammary tumors Cancer Res 2001 61 2537-2541 11289127
59. Shaaban AM O'Neill PA Davies MP Sibson R West CR Smith PH Foster CS Declining estrogen receptor-beta expression defines malignant progression of human breast neoplasia Am J Surg Pathol 2003 27 1502-1512 10.1097/00000478-200302000-00021 14657709
60. Shaaban AM Jarvis C Moore F West C Dodson A Foster CS Prognostic significance of estrogen receptor Beta in epithelial hyperplasia of usual type with known outcome Am J Surg Pathol 2005 29 1593-1599 10.1097/ 01.pas.0000184807.38037.75 16327431
61. O'Neill PA Shaaban AM West CR Dodson A Jarvis C Moore P Davies MP Sibson DR Foster CS Increased risk of malignant progression in benign proliferating breast lesions defined by expression of heat shock protein 27 Br J Cancer 2004 90 182-188 10.1038/sj.bjc.6601449 14710227
62. Hudelist G Czerwenka K Kubista E Marton E Pischinger K Singer CF Expression of sex steroid receptors and their co-factors in normal and malignant breast tissue: AIB1 is a carcinoma-specific co-activator Breast Cancer Res Treat 2003 78 193-204 10.1023/A:1022930710850 12725419
63. Lee S Mohsin SK Mao S Hilsenbeck SG Medina D Allred DC Hormones, receptors, and growth in hyperplastic enlarged lobular units: Early potential precursors of breast cancer Breast Cancer Res 2006 8 R6 1413990 16417654 10.1186/bcr1367
64. Ariga N Suzuki T Moriya T Kimura M Inoue T Ohuchi N Sasano H Progesterone receptor A and B isoforms in the human breast and its disorders Jpn J Cancer Res 2001 92 302-308 11267940
65. Barnes NL Boland GP Davenport A Knox WF Bundred NJ Relationship between hormone receptor status and tumour size, grade and comedo necrosis in ductal carcinoma in situ Br J Surg 2005 92 429-434 10.1002/bjs.4878 15736216
66. Ringberg A Anagnostaki L Anderson H Idvall I Ferno M South Sweden Breast Cancer Group Cell biological factors in ductal carcinoma in situ (DCIS) of the breast-relationship to ipsilateral local recurrence and histopathological characteristics Eur J Cancer 2001 37 1514-1522 10.1016/ S0959-8049(01)00165-4 11506959
67. Claus EB Chu P Howe CL Davison TL Stern DF Carter D DiGiovanna MP Pathobiologic findings in DCIS of the breast: Morphologic features, angiogenesis, HER-2/neu and hormone receptors Exp Mol Pathol 2001 70 303-316 10.1006/exmp.2001.2366 11418009
68. Rody A Diallo R Poremba C Speich R Wuelfing P Kissler S Solbach C Kiesel L Jackisch C Estrogen receptor alpha and beta, progesterone receptor, pS2 and HER-2/neu expression delineate different subgroups in ductal carcinoma in situ of the breast Oncol Rep 2004 12 695-699 15375487
69. Lebrecht A Buchmann J Hefler L Lampe D Koelbl H Histological category and expression of hormone receptors in ductal carcinoma in situ of the breast Anticancer Res 2002 22 1909-1911 12168892
70. Kepple J Henry-Tillman RS Klimberg VS Layeeque R Siegel E Westbrook K Korourian S The receptor expression pattern in ductal carcinoma in situ predicts recurrence Am J Surg 2006 192 68-71 10.1016/ j.amjsurg.2006.04.002 16769278
71. Cornfield DB Palazzo JP Schwartz GF Goonewardene SA Kovatich AJ Chervoneva I Hyslop T Schwarting R The prognostic significance of multiple morphologic features and biologic markers in ductal carcinoma in situ of the breast: A study of a large cohort of patients treated with surgery alone Cancer 2004 100 2317-2327 10.1002/cncr.20260 15160334
72. 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 12628841
73. Nofech-Mozes S Spayne J Rakovitch E Hanna W Prognostic and predictive molecular markers in DCIS: A review Adv Anat Pathol 2005 12 256-264 10.1097/01.pap.0000184177.65919.5e 16210921
74. Fadare O Dadmanesh F Alvarado-Cabrero I Snyder R Stephen Mitchell J Tot T Wang SA Ghofrani M Eusebi V Martel M Tavassoli FA Lobular intraepithelial neoplasia [lobular carcinoma in situ] with comedo-type necrosis: A clinicopathologic study of 18 cases Am J Surg Pathol 2006 30 1445-1453 10.1097/01.pas.0000213290.58283.82 17063087
75. Fisher ER Costantino J Fisher B Palekar AS Paik SM Suarez CM Wolmark N Pathologic findings from the National Surgical Adjuvant Breast Project (NSABP) Protocol B-17. Five-year observations concerning lobular carcinoma in situ Cancer 1996 78 1403-1416 10.1002/ (SICI)1097-0142(19961001)78:7<1403::AID-CNCR6>3.0.CO;2-L 8839545
76. Mote PA Bartow S Tran N Clarke CL Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis Breast Cancer Res Treat 2002 72 163-172 10.1023/ A:1014820500738 12038707
77. McGowan EM Clarke CL Effect of overexpression of progesterone receptor A on endogenous progestin-sensitive endpoints in breast cancer cells Mol Endocrinol 1999 13 1657-1671 10.1210/me.13.10.1657 10517668
78. Graham JD Yager ML Hill HD Byth K O'Neill GM Clarke CL Altered progesterone receptor isoform expression remodels progestin responsiveness of breast cancer cells Mol Endocrinol 2005 19 2713-2735 10.1210/me.2005-0126 15976005
79. Mote PA Leary JA Avery KA Sandelin K Chenevix-Trench G Kirk JA Clarke CL kConFab Investigators Germ-line mutations in BRCA1 or BRCA2 in the normal breast are associated with altered expression of estrogen-responsive proteins and the predominance of progesterone receptor A Genes Chromosomes Cancer 2004 39 236-248 10.1002/gcc.10321 14732925
80. De Potter CR Van Daele S Van de Vijver MJ Pauwels C Maertens G De Boever J Vandekerckhove D Roels H The expression of the neu oncogene product in breast lesions and in normal fetal and adult human tissues Histopathology 1989 15 351-362 10.1111/j.1365-2559.1989.tb01587.x 2572531
81. Olayioye MA Update on HER-2 as a target for cancer therapy: intracellular signaling pathways of ErbB2/HER-2 and family members Breast Cancer Res 2001 3 385-389 138705 11737890 10.1186/bcr327
82. Ross JS Fletcher JA HER-2/neu (c-erb-B2) gene and protein in breast cancer Am J Clin Pathol 1999 112 S53-67 10396301
83. Gusterson BA Machin LG Gullick WJ Gibbs NM Powles TJ Elliott C Ashley S Monaghan P Harrison S C-erbB-2 expression in benign and malignant breast disease Br J Cancer 1988 58 453-457 2849975
84. Edorh A Leroux A N'sossani B Parache RM Rihn B Detection by immunohistochemistry of c-erbB2 oncoprotein in breast carcinomas and benign mammary lesions Cell Mol Biol (Noisy-le-grand) 1999 45 831-840 10541479
85. Aubele M Werner M Hofler H Genetic alterations in presumptive precursor lesions of breast carcinomas Anal Cell Pathol 2002 24 69-76 12446956
86. Heffelfinger SC Yassin R Miller MA Lower EE Cyclin D1, retinoblastoma, p53, and Her2/neu protein expression in preinvasive breast pathologies: correlation with vascularity Pathobiology 2000 68 129-136 10.1159/ 000055913 11174070
87. Xu R Perle MA Inghirami G Chan W Delgado Y Feiner H Amplification of Her-2/neu gene in Her-2/neu-overexpressing and -nonexpressing breast carcinomas and their synchronous benign, premalignant, and metastatic lesions detected by FISH in archival material Mod Pathol 2002 15 116-124 10.1038/modpathol.3880503 11850540
88. Stark A Hulka BS Joens S Novotny D Thor AD Wold LE Schell MJ Melton LJ 3rd Liu ET Conway K HER-2/neu amplification in benign breast disease and the risk of subsequent breast cancer J Clin Oncol 2000 18 267-274 10637239
89. Rohan TE Hartwick W Miller AB Kandel RA Immunohistochemical detection of c-erbB-2 and p53 in benign breast disease and breast cancer risk J Natl Cancer Inst 1998 90 1262-1269 10.1093/jnci/90.17.1262 9731732
90. Mohsin SK O'Connell P Allred DC Libby AL Biomarker profile and genetic abnormalities in lobular carcinoma in situ Breast Cancer Res Treat 2005 90 249-256 10.1007/s10549-004-4493-8 15830138
91. Sneige N Wang J Baker BA Krishnamurthy S Middleton LP Clinical, histopathologic, and biologic features of pleomorphic lobular (ductal-lobular) carcinoma in situ of the breast: A report of 24 cases Mod Pathol 2002 15 1044-1050 10.1097/01.MP.0000030450.20581.E3 12379750
92. Tsuda H Hirohashi S Multiple developmental pathways of highly aggressive breast cancers disclosed by comparison of histological grades and c-erbB-2 expression patterns in both the non-invasive and invasive portions Pathol Int 1998 48 518-525 9701014
93. Albonico G Querzoli P Ferretti S Magri E Nenci I Biophenotypes of breast carcinoma in situ defined by image analysis of biological parameters Pathol Res Pract 1996 192 117-123 8692711
94. Tsuda H Iwaya K Fukutomi T Hirohashi S p53 mutations and c-erbB-2 amplification in intraductal and invasive breast carcinomas of high histologic grade Jpn J Cancer Res 1993 84 394-401 8099903
95. Allred DC Clark GM Molina R Tandon AK Schnitt SJ Gilchrist KW Osborne CK Tormey DC McGuire WL Overexpression of HER-2/neu and its relationship with other prognostic factors change during the progression of in situ to invasive breast cancer Hum Pathol 1992 23 974-979 10.1016/ 0046-8177(92)90257-4 1355464
96. Toledo F Wahl GM Regulating the p53 pathway: In vitro hypotheses, in vivo veritas Nat Rev Cancer 2006 6 909-923 10.1038/nrc2012 17128209
97. Green DR Chipuk JE p53 and metabolism: Inside the TIGAR Cell 2006 126 30-32 10.1016/j.cell.2006.06.032 16839873
98. Vogelstein B Lane D Levine AJ Surfing the p53 network Nature 2000 408 307-310 10.1038/35042675 11099028
99. Gasco M Shami S Crook T The p53 pathway in breast cancer Breast Cancer Res 2002 4 70-76 138723 11879567 10.1186/bcr426
100. Younes M Lebovitz RM Bommer KE Cagle PT Morton D Khan S Laucirica R p53 accumulation in benign breast biopsy specimens Hum Pathol 1995 26 155-158 10.1016/0046-8177(95)90031-4 7860045
101. Done SJ Arneson NC Ozcelik H Redston M Andrulis IL p53 mutations in mammary ductal carcinoma in situ but not in epithelial hyperplasias Cancer Res 1998 58 785-789 9485035
102. Chitemerere M Andersen TI Holm R Karlsen F Borresen AL Nesland JM TP53 alterations in atypical ductal hyperplasia and ductal carcinoma in situ of the breast Breast Cancer Res Treat 1996 41 103-109 10.1007/BF01807155 8944328
103. Kang JH Kim SJ Noh DY Choe KJ Lee ES Kang HS The timing and characterization of p53 mutations in progression from atypical ductal hyperplasia to invasive lesions in the breast cancer J Mol Med 2001 79 648-655 10.1007/s001090100269 11715068
104. Keohavong P Gao WM Mady HH Kanbour-Shakir A Melhem MF Analysis of p53 mutations in cells taken from paraffin-embedded tissue sections of ductal carcinoma in situ and atypical ductal hyperplasia of the breast Cancer Lett 2004 212 121-130 10.1016/j.canlet.2004.03.010 15246568
105. Siziopikou KP Prioleau JE Harris JR Schnitt SJ bcl-2 expression in the spectrum of preinvasive breast lesions Cancer 1996 77 499-506 10.1002/ (SICI)1097-0142(19960201)77:3<499::AID-CNCR11>3.0.CO;2-# 8630957
106. Sapino A Frigerio A Peterse JL Arisio R Coluccia C Bussolati G Mammographically detected in situ lobular carcinomas of the breast Virchows Arch 2000 436 421-430 10.1007/s004280050469 10881735
107. Lebeau A Unholzer A Amann G Kronawitter M Bauerfeind I Sendelhofert A Iff A Lohrs U EGFR, HER-2/neu, cyclin D1, p21 and p53 in correlation to cell proliferation and steroid hormone receptor status in ductal carcinoma in situ of the breast Breast Cancer Res Treat 2003 79 187-198 10.1023/A:1023958324448 12825853
108. Tan PH Chuah KL Chiang G Wong CY Dong F Bay BH Correlation of p53 and cerbB2 expression and hormonal receptor status with clinicopathologic parameters in ductal carcinoma in situ of the breast Oncol Rep 2002 9 1081-1086 12168077
109. Megha T Ferrari F Benvenuto A Bellan C Lalinga AV Lazzi S Bartolommei S Cevenini G Leoncini L Tosi P p53 mutation in breast cancer. Correlation with cell kinetics and cell of origin J Clin Pathol 2002 55 461-466 12037031
110. Bartley AN Ross DW Validation of p53 immunohistochemistry as a prognostic factor in breast cancer in clinical practice Arch Pathol Lab Med 2002 126 456-458 11900572
111. Poller DN Roberts EC Bell JA Elston CW Blamey RW Ellis IO p53 protein expression in mammary ductal carcinoma in situ: Relationship to immunohistochemical expression of estrogen receptor and c-erbB-2 protein Hum Pathol 1993 24 463-468 10.1016/0046-8177(93)90157-C 8098318
112. O'Malley FP Vnencak-Jones CL Dupont WD Parl F Manning S Page DL p53 mutations are confined to the comedo type ductal carcinoma in situ of the breast. Immunohistochemical and sequencing data Lab Invest 1994 71 67-72 8041120
113. Rudas M Neumayer R Gnant MF Mittelbock M Jakesz R Reiner A p53 protein expression, cell proliferation and steroid hormone receptors in ductal and lobular in situ carcinomas of the breast Eur J Cancer 1997 33-39 44 10.1016/S0959-8049(96)00368-1 9071897
114. Mylonas I Makovitzky J Jeschke U Briese V Friese K Gerber B Expression of Her2/neu, steroid receptors (ER and PR), Ki67 and p53 in invasive mammary ductal carcinoma associated with ductal carcinoma In Situ (DCIS) Versus invasive breast cancer alone Anticancer Res 2005 25 1719-1723 16033090
115. Gerdes J Lemke H Baisch H Wacker HH Schwab U Stein H Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67 J Immunol 1984 133 1710-1715 6206131
116. Midulla C Pisani T De Iorio P Cenci M Divizia E Nofroni I Vecchione A Cytological analysis and immunocytochemical expression of Ki67 and Bcl-2 in breast proliferative lesions Anticancer Res 2002 22 1341-1345 12168948
117. Viacava P Naccarato AG Bevilacqua G Different proliferative patterns characterize different preinvasive breast lesions J Pathol 1999 188 245-251 10.1002/ (SICI)1096-9896(199907)188:3<245::AID-PATH353>3.0.CO;2-6 10419590
118. Shaaban AM Sloane JP West CR Foster CS Breast cancer risk in usual ductal hyperplasia is defined by estrogen receptor-alpha and Ki-67 expression Am J Pathol 2002 160 597-604 11839580
119. Papantoniou V Tsiouris S Koutsikos J Sotiropoulou M Mainta E Lazaris D Valsamaki P Melissinou M Zerva C Antsaklis A Scintimammographic detection of usual ductal breast hyperplasia with increased proliferation rate at risk for malignancy Nucl Med Commun 2006 27 911-917 10.1097/01.mnm.0000243367.73141.85 17021432
120. van Delft MF Huang DC How the Bcl-2 family of proteins interact to regulate apoptosis Cell Res 2006 16 203-213 10.1038/sj.cr.7310028 16474435
121. Reed JC Bcl-2 and the regulation of programmed cell death J Cell Biol 1994 124 1-6 10.1083/jcb.124.1.1 8294493
122. Hockenbery DM bcl-2 in cancer, development and apoptosis J Cell Sci Suppl 1994 18 51-55 7883792
123. Kim R Unknotting the roles of Bcl-2 and Bcl-xL in cell death Biochem Biophys Res Commun 2005 333 336-343 10.1016/j.bbrc.2005.04.161 15922292
124. Bai M Agnantis NJ Kamina S Demou A Zagorianakou P Katsaraki A Kanavaros P In vivo cell kinetics in breast carcinogenesis Breast Cancer Res 2001 3 276-283 34112 11434879 10.1186/bcr306
125. Kapucuoglu N Losi L Eusebi V Immunohistochemical localization of Bcl-2 and Bax proteins in in situ and invasive duct breast carcinomas Virchows Arch 1997 430 17-22 10.1007/BF01008011 9037310
126. Krogerus LA Leivonen M Haasto AL Expression patterns of biologic markers in small breast cancers and preneoplastic breast lesions Breast 2000 9 281-285 10.1054/brst.2000.0141 14732179
127. Meteoglu I Dikicioglu E Erkus M Culhaci N Kacar F Ozkara E Uyar M Breast carcinogenesis. Transition from hyperplasia to invasive lesions Saudi Med J 2005 26 1889-1896 16380768
128. Mustonen M Raunio H Paakko P Soini Y The extent of apoptosis is inversely associated with bcl-2 expression in premalignant and malignant breast lesions Histopathology 1997 31 347-354 10.1046/ j.1365-2559.1997.2710877.x 9363451
129. Sledge GW Jr VEGF-targeting therapy for breast cancer J Mammary Gland Biol Neoplasia 2005 10 319-323 10.1007/s10911-006-9005-5 16924373
130. Kataoka N Cai Q Wen W Shu XO Jin F Gao YT Zheng W Population-based case-control study of VEGF gene polymorphisms and breast cancer risk among Chinese women Cancer Epidemiol Biomarkers Prev 2006 15 1148-1152 10.1158/1055-9965.EPI-05-0871 16775174
131. Jacobs EJ Feigelson HS Bain EB Brady KA Rodriguez C Stevens VL Patel AV Thun MJ Calle EE Polymorphisms in the vascular endothelial growth factor gene and breast cancer in the Cancer Prevention Study II cohort Breast Cancer Res 2006 8 R22 1557725 16613616 10.1186/bcr1400
132. Viacava P Naccarato AG Bocci G Fanelli G Aretini P Lonobile A Evangelista G Montruccoli G Bevilacqua G Angiogenesis and VEGF expression in pre-invasive lesions of the human breast J Pathol 2004 204 140-146 10.1002/path.1626 15376259
133. Hieken TJ Farolan M D'Alessandro S Velasco JM Predicting the biologic behavior of ductal carcinoma in situ: An analysis of molecular markers Surgery 2001 130 593-600 discussion 600-1 10.1067/msy.2001.116921 11602889
134. Vogl G Dietze O Hauser-Kronberger C Angiogenic potential of ductal carcinoma in situ (DCIS) of human breast Histopathology 2005 47 617-624 10.1111/j.1365-2559.2005.02299.x 16324200
135. Berx G Cleton-Jansen AM Nollet F de Leeuw WJ van de Vijver M Cornelisse C van Roy F E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers EMBO J 1995 14 6107-6115 394735 8557030
136. Bratthauer GL Moinfar F Stamatakos MD Mezzetti TP Shekitka KM Man YG Tavassoli FA Combined E-cadherin and high molecular weight cytokeratin immunoprofile differentiates lobular, ductal, and hybrid mammary intraepithelial neoplasias Hum Pathol 2002 33 620-627 10.1053/ hupa.2002.124789 12152161
137. Lerwill MF Current practical applications of diagnostic immunohistochemistry in breast pathology Am J Surg Pathol 2004 28 1076-1091 10.1097/01.pas.0000126780.10029.f0 15252316
138. Putti TC Pinder SE Elston CW Lee AH Ellis IO Breast pathology practice: most common problems in a consultation service Histopathology 2005 47 445-457 10.1111/j.1365-2559.2005.02246.x 16241992
139. Vos CB Cleton-Jansen AM Berx G de Leeuw WJ ter Haar NT van Roy F Cornelisse CJ Peterse JL van de Vijver MJ E-cadherin inactivation in lobular carcinoma in situ of the breast: An early event in tumorigenesis Br J Cancer 1997 76 1131-1133 9365159
140. Mastracci TL Tjan S Bane AL O'Malley FP Andrulis IL E-cadherin alterations in atypical lobular hyperplasia and lobular carcinoma in situ of the breast Mod Pathol 2005 18 741-751 10.1038/modpathol.3800362 15696125
141. Nass SJ Herman JG Gabrielson E Iversen PW Parl FF Davidson NE Graff JR Aberrant methylation of the estrogen receptor and E-cadherin 5′ CpG islands increases with malignant progression in human breast cancer Cancer Res 2000 60 4346-4348 10969774
142. Gupta SK Douglas-Jones AG Jasani B Morgan JM Pignatelli M Mansel RE E-cadherin (E-cad) expression in duct carcinoma in situ (DCIS) of the breast Virchows Arch 1997 430 23-28 10.1007/BF01008012 9037311
143. Rieger-Christ KM Pezza JA Dugan JM Braasch JW Hughes KS Summerhayes IC Disparate E-cadherin mutations in LCIS and associated invasive breast carcinomas Mol Pathol 2001 54 91-97 1187009 11322170 10.1136/mp.54.2.91
144. Wakefield LM Piek E Bottinger EP TGF-beta signaling in mammary gland development and tumorigenesis J Mammary Gland Biol Neoplasia 2001 6 67-82 10.1023/A:1009568532177 11467453
145. Lebrecht A Grimm C Euller G Ludwig E Ulbrich E Lantzsch T Hefler L Koelbl H Transforming growth factor beta 1 serum levels in patients with preinvasive and invasive lesions of the breast Int J Biol Markers 2004 19 236-239 15503826
146. Walker RA Dearing SJ Transforming growth factor beta 1 in ductal carcinoma in situ and invasive carcinomas of the breast Eur J Cancer 1992 28 641-644 10.1016/S0959-8049(05)80116-9 1317202
147. Gobbi H Dupont WD Simpson JF Plummer WD Jr Schuyler PA Olson SJ Arteaga CL Page DL Transforming growth factor-beta and breast cancer risk in women with mammary epithelial hyperplasia J Natl Cancer Inst 1999 91 2096-2101 10.1093/jnci/91.24.2096 10601380
148. Rocco JW Sidransky D p16(MTS-1/CDKN2/INK4a) in cancer progression Exp Cell Res 2001 264 42-55 10.1006/excr.2000.5149 11237522
149. Lehmann U Langer F Feist H Glockner S Hasemeier B Kreipe H (Krassenstein R Sauter E Dulaimi E Battagli C Ehya H Klein-Szanto A Cairns P Detection of breast cancer in nipple aspirate fluid by CpG island hypermethylation Clin Cancer Res 2004 10 28-32 10.1158/1078-0432.CCR-0410-3 14734448
150. Van Zee KJ Calvano JE Bisogna M Hypomethylation and increased gene expression of p16INK4a in primary and metastatic breast carcinoma as compared to normal breast tissue Oncogene 1998 16 2723-2727 10.1038/ sj.onc.1201794 9652738
151. Di Vinci A Perdelli L Banelli B Salvi S Casciano I Gelvi I Allemanni G Margallo E Gatteschi B Romani M p16(INK4a) promoter methylation and protein expression in breast fibroadenoma and carcinoma Int J Cancer 2005 114 414-21 10.1002/ijc.20771 15578730
152. Debniak T Gorski B Huzarski T Byrski T Cybulski C Mackiewicz A Gozdecka-Grodecka S Gronwald J Kowalska E Haus O Grzybowska E Stawicka M Swiec M Urbanski K Niepsuj S Wasko B Gozdz S Wandzel P Szczylik C Surdyka D Rozmiarek A Zambrano O Posmyk M Narod SA Lubinski J A common variant of CDKN2A (p16) predisposes to breast cancer J Med Genet 2005 42 763-765 10.1136/jmg.2005.031476 15879498
153. Colozza M Azambuja E Cardoso F Sotiriou C Larsimont D Piccart MJ Proliferative markers as prognostic and predictive tools in early breast cancer: Where are we now? Ann Oncol 2005 16 1723-1739 10.1093/annonc/ mdi352 15980158
154. Alkarain A Jordan R Slingerland J p27 deregulation in breast cancer: prognostic significance and implications for therapy J Mammary Gland Biol Neoplasia 2004 9 67-80 10.1023/B:JOMG.0000023589.00994.5e 15082919
155. Musgrove EA Davison EA Ormandy CJ Role of the CDK inhibitor p27 (Kip1) in mammary development and carcinogenesis: Insights from knockout mice J Mammary Gland Biol Neoplasia 2004 9 55-66 10.1023/ B:JOMG.0000023588.55733.84 15082918
156. Oh YL Choi JS Song SY Ko YH Han BK Nam SJ Yang JH Expression of p21Waf1, p27Kip1 and cyclin D1 proteins in breast ductal carcinoma in situ: Relation with clinicopathologic characteristics and with p53 expression and estrogen receptor status Pathol Int 2001 51 94-99 10.1046/ j.1440-1827.2001.01173.x 11169147
157. Dotto GP p21(WAF1/Cip1): More than a break to the cell cycle? Biochim Biophys Acta 2000 1471 M43-56 10967424
158. 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 12628841
159. 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 11423985
160. Simooka H Oyama T Sano T Horiguchi J Nakajima T Immunohistochemical analysis of 14-3-3 sigma and related proteins in hyperplastic and neoplastic breast lesions, with particular reference to early carcinogenesis Pathol Int 2004 54 595-602 10.1111/ j.1440-1827.2004.01668.x 15260850
161. Gerger A Langsenlehner U Renner W Weitzer W Eder T Yazdani-Biuki B Hofmann G Samonigg H Krippl P A multigenic approach to predict breast cancer risk Breast Cancer Res Treat 2006