Molecular drivers of lobular carcinoma in situ

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Logan, Greg J ^a,b   Dabbs, David J ^a,c   Lucas, Peter C ^a,c   Jankowitz, Rachel C ^a,d   Brown, Daniel D ^a,d   Clark, Beth Z ^a,c   Oesterreich, Steffi ^a,b   McAuliffe, Priscilla F ^a,d  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CARRIER PROTEIN; DIPEPTIDASE; DIPEPTIDASE I; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GUANOSINE TRIPHOSPHATASE; KI 67 ANTIGEN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PROGESTERONE RECEPTOR; PROTEIN P120; PROTEIN P53; PROTEIN TYROSINE KINASE; SLC37A3 PROTEIN; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BREAST CARCINOMA; CANCER CLASSIFICATION; CANCER GROWTH; CANCER PROGNOSIS; CANCER RISK; CARCINOMA IN SITU; DISEASE ASSOCIATION; DISEASE MARKER; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN; LOBULAR CARCINOMA IN SITU; NONHUMAN; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; BREAST NEOPLASMS; CARCINOMA, LOBULAR; CELL TRANSFORMATION; DISEASE COURSE; FEMALE; GENETIC PREDISPOSITION; GENETICS; PATHOLOGY; PROGNOSIS;

ANIMALS; BREAST NEOPLASMS; CARCINOMA IN SITU; CARCINOMA, LOBULAR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; PROGNOSIS; SIGNAL TRANSDUCTION;

EID: 84930620671     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0580-5     Document Type: Article

References (101)

1. Degnim AC, King TA. Surgical management of high-risk breast lesions. Surg Clin North Am. 2013;93:329-40.
2. Li CI, Daling JR, Malone KE. Age-specific incidence rates of in situ breast carcinomas by histologic type, 1980 to 2001. Cancer Epidemiol Biomarkers Prev. 2005;14:1008-11.
3. Page DL, Kidd Jr TE, Dupont WD, Simpson JF, Rogers LW. Lobular neoplasia of the breast: higher risk for subsequent invasive cancer predicted by more extensive disease. Hum Pathol. 1991;22:1232-9.
4. Bodian CA, Perzin KH, Lattes R. Lobular neoplasia. Long term risk of breast cancer and relation to other factors. Cancer. 1996;78:1024-34.
5. To T, Wall C, Baines CJ, Miller AB. Is carcinoma in situ a precursor lesion of invasive breast cancer? Int J Cancer. 2014;135:1646-52.
6. Wellings SR. A hypothesis of the origin of human breast cancer from the terminal ductal lobular unit. Pathol Res Pract. 1980;166:515-35.
7. Wellings SR, Jensen HM, Marcum RG. An atlas of subgross pathology of the human breast with special reference to possible precancerous lesions. J Natl Cancer Inst. 1975;55:231-73.
8. Jensen HM, Rice JR, Wellings SR. Preneoplastic lesions in the human breast. Science. 1976;191:295-7.
9. 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;58:4721-7.
10. Gomes DS, Porto SS, Balabram D, Gobbi H. Inter-observer variability between general pathologists and a specialist in breast pathology in the diagnosis of lobular neoplasia, columnar cell lesions, atypical ductal hyperplasia and ductal carcinoma in situ of the breast. Diagn Pathol. 2014;9:121.
11. Dabbs DJ, Schnitt SJ, Geyer FC, Weigelt B, Baehner FL, Decker T, et al. Lobular neoplasia of the breast revisited with emphasis on the role of E-cadherin immunohistochemistry. Am J Surg Pathol. 2013;37:e1-11.
12. Foote FW, Stewart FW. Lobular carcinoma in situ: a rare form of mammary cancer. Am J Pathol. 1941;17:491-6.
13. McDivitt RW, Hutter RV, Foote Jr FW, Stewart FW. In situ lobular carcinoma. A prospective follow-up study indicating cumulative patient risks. JAMA. 1967;201:82-6.
14. Haagensen CD, Lane N, Lattes R, Bodian C. Lobular neoplasia (so-called lobular carcinoma in situ) of the breast. Cancer. 1978;42:737-69.
15. Rosen PP, Kosloff C, Lieberman PH, Adair F, Braun Jr DW. Lobular carcinoma in situ of the breast. Detailed analysis of 99 patients with average follow-up of 24 years. Am J Surg Pathol. 1978;2:225-51.
16. Hutter RV, Foote Jr FW. Lobular carcinoma in situ. Long term follow-up. Cancer. 1969;24:1081-5.
17. Page DL, Schuyler PA, Dupont WD, Jensen RA, Plummer Jr WD, Simpson JF. Atypical lobular hyperplasia as a unilateral predictor of breast cancer risk: a retrospective cohort study. Lancet. 2003;361:125-9.
18. Marshall LM, Hunter DJ, Connolly JL, Schnitt SJ, Byrne C, London SJ, et al. Risk of breast cancer associated with atypical hyperplasia of lobular and ductal types. Cancer Epidemiol Biomarkers Prev. 1997;6:297-301.
19. Ottesen GL, Graversen HP, Blichert-Toft M, Christensen IJ, Andersen JA. Carcinoma in situ of the female breast. 10 year follow-up results of a prospective nationwide study. Breast Cancer Res Treat. 2000;62:197-210.
20. Hwang ES, Nyante SJ, Yi Chen Y, Moore D, DeVries S, Korkola JE, et al. Clonality of lobular carcinoma in situ and synchronous invasive lobular carcinoma. Cancer. 2004;100:2562-72.
21. Morandi L, Marucci G, Foschini MP, Cattani MG, Pession A, Riva C, et al. Genetic similarities and differences between lobular in situ neoplasia (LN) and invasive lobular carcinoma of the breast. Virchows Arch. 2006;449:14-23.
22. Andrade VP, Ostrovnaya I, Seshan VE, Morrogh M, Giri D, Olvera N, et al. Clonal relatedness between lobular carcinoma in situ and synchronous malignant lesions. Breast Cancer Res. 2012;14:R103.
23. Aulmann S, Penzel R, Longerich T, Funke B, Schirmacher P, Sinn HP. Clonality of lobular carcinoma in situ (LCIS) and metachronous invasive breast cancer. Breast Cancer Res Treat. 2008;107:331-5.
24. Wallace AS, Xiang D, Hockman L, Arya M, Jeffress J, Wang Z, et al. Synchronous lobular carcinoma in situ and invasive lobular cancer: marker or precursor for invasive lobular carcinoma. Eur J Surg Oncol. 2014;40:1245-9.
25. Visvanathan K, Hurley P, Bantug E, Brown P, Col NF, Cuzick J, et al. Use of pharmacologic interventions for breast cancer risk reduction: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol. 2013;31:2942-62.
26. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst. 1998;90:1371-88.
27. Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, et al. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: the NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 trial. JAMA. 2006;295:2727-41.
28. Oppong BA, King TA. Recommendations for women with lobular carcinoma in situ (LCIS). Oncology (Williston Park). 2011;25:1051-6.
29. Simpson PT, Gale T, Fulford LG, Reis-Filho JS, Lakhani SR. The diagnosis and management of pre-invasive breast disease: pathology of atypical lobular hyperplasia and lobular carcinoma in situ. Breast Cancer Res. 2003;5:258-62.
30. Moumen M, Chiche A, Cagnet S, Petit V, Raymond K, Faraldo MM, et al. The mammary myoepithelial cell. Int J Dev Biol. 2011;55:763-71.
31. King TA, Reis-Filho JS. Lobular Neoplasia. Surg Oncol Clin N Am. 2014;23:487-503.
32. Bagaria SP, Shamonki J, Kinnaird M, Ray PS, Giuliano AE. The florid subtype of lobular carcinoma in situ: marker or precursor for invasive lobular carcinoma? Ann Surg Oncol. 2011;18:1845-51.
33. Shin SJ, Lal A, De Vries S, Suzuki J, Roy R, Hwang ES, et al. Florid lobular carcinoma in situ: molecular profiling and comparison to classic lobular carcinoma in situ and pleomorphic lobular carcinoma in situ. Hum Pathol. 2013;44:1998-2009.
34. Lopez-Garcia MA, Geyer FC, Lacroix-Triki M, Marchió C, Reis-Filho JS. Breast cancer precursors revisited: molecular features and progression pathways. Histopathology. 2010;57:171-92.
35. Middleton LP, Palacios DM, Bryant BR, Krebs P, Otis CN, Merino MJ. Pleomorphic lobular carcinoma: morphology, immunohistochemistry, and molecular analysis. Am J Surg Pathol. 2000;24:1650-6.
36. Chivukula M, Haynik DM, Brufsky A, Carter G, Dabbs DJ. Pleomorphic lobular carcinoma in situ (PLCIS) on breast core needle biopsies: clinical significance and immunoprofile. Am J Surg Pathol. 2008;32:1721-6.
37. Wick MR, Lillemoe TJ, Copland GT, Swanson PE, Manivel JC, Kiang DT. Gross cystic disease fluid protein-15 as a marker for breast cancer: immunohistochemical analysis of 690 human neoplasms and comparison with alpha-lactalbumin. Hum Pathol. 1989;20:281-7.
38. Bratthauer GL, Tavassoli FA. Lobular intraepithelial neoplasia: previously unexplored aspects assessed in 775 cases and their clinical implications. Virchows Arch. 2002;440:134-8.
39. Galimberti V, Monti S, Mastropasqua MG. DCIS and LCIS are confusing and outdated terms. They should be abandoned in favor of ductal intraepithelial neoplasia (DIN) and lobular intraepithelial neoplasia (LIN). Breast. 2013;22:431-5.
40. Downs-Kelly E, Bell D, Perkins GH, Sneige N, Middleton LP. Clinical implications of margin involvement by pleomorphic lobular carcinoma in situ. Arch Pathol Lab Med. 2011;135:737-43.
41. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF, et al. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics. 2006;7:96.
42. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001;98:10869-74.
43. Green AR, Young P, Krivinskas S, Rakha EA, Claire Paish E, Powe DG, et al. The expression of ERalpha, ERbeta and PR in lobular carcinoma in situ of the breast determined using laser microdissection and real-time PCR. Histopathology. 2009;54:419-27.
44. Mohsin SK, O'Connell P, Allred DC, Libby AL. Biomarker profile and genetic abnormalities in lobular carcinoma in situ. Breast Cancer Res Treat. 2005;90:249-56.
45. Querzoli P, Albonico G, Ferretti S, Rinaldi R, Beccati D, Corcione S, et al. Modulation of biomarkers in minimal breast carcinoma: a model for human breast carcinoma progression. Cancer. 1998;83:89-97.
46. Rudas M, Neumayer R, Gnant MF, Mittelböck 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.
47. Arpino G, Bardou VJ, Clark GM, Elledge RM. Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res. 2004;6:R149-56.
48. Bharat A, Gao F, Margenthaler JA. Tumor characteristics and patient outcomes are similar between invasive lobular and mixed invasive ductal/lobular breast cancers but differ from pure invasive ductal breast cancers. Am J Surg. 2009;198:516-9.
49. Chen YY, Hwang ES, Roy R, DeVries S, Anderson J, Wa C, et al. Genetic and phenotypic characteristics of pleomorphic lobular carcinoma in situ of the breast. Am J Surg Pathol. 2009;33:1683-94.
50. Cui X, Schiff R, Arpino G, Osborne CK, Lee AV. Biology of progesterone receptor loss in breast cancer and its implications for endocrine therapy. J Clin Oncol. 2005;23:7721-35.
51. Hopp TA, Weiss HL, Hilsenbeck SG, Cui Y, Allred DC, Horwitz KB, et al. Breast cancer patients with progesterone receptor PR-A-rich tumors have poorer disease-free survival rates. Clin Cancer Res. 2004;10:2751-60.
52. Wong H, Lau S, Cheung P, Wong TT, Parker A, Yau T, et al. Lobular breast cancers lack the inverse relationship between ER/PR status and cell growth rate characteristic of ductal cancers in two independent patient cohorts: implications for tumor biology and adjuvant therapy. BMC Cancer. 2014;14:826.
53. Murphy LC, Leygue E. The role of estrogen receptor-beta in breast cancer. Semin Reprod Med. 2012;30:5-13.
54. Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ, et al. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 1997;277:1508-10.
55. Huang B, Omoto Y, Iwase H, Yamashita H, Toyama T, Coombes RC, et al. Differential expression of estrogen receptor alpha, beta1, and beta2 in lobular and ductal breast cancer. Proc Natl Acad Sci U S A. 2014;111:1933-8.
56. Nonni A, Zagouri F, Sergentanis TN, Lazaris AC, Patsouris ES, Zografos GC. Immunohistochemical expression of estrogen receptors alpha and beta in lobular neoplasia. Virchows Arch. 2007;451:893-7.
57. Figueroa-Magalhães MC. Jelovac D1, Connolly RM1, Wolff AC. Treatment of HER2-positive breast cancer. Breast. 2014;23:128-36.
58. Urruticoechea A, Smith IE, Dowsett M. Proliferation marker Ki-67 in early breast cancer. J Clin Oncol. 2005;23:7212-20.
59. Vincent-Salomon A, Hajage D, Rouquette A, Cédenot A, Gruel N, Alran S, et al. High Ki67 expression is a risk marker of invasive relapse for classical lobular carcinoma in situ patients. Breast. 2012;21:380-3.
60. Gasco M, Shami S, Crook T. The p53 pathway in breast cancer. Breast Cancer Res. 2002;4:70-6.
61. Andrade VP, Morrogh M, Qin LX, Olvera N, Giri D, Muhsen S, et al. Gene expression profiling of lobular carcinoma in situ reveals candidate precursor genes for invasion. Mol Oncol. 2015;9:772-82.
62. Tazaki E, Shishido-Hara Y, Mizutani N, Nomura S, Isaka H, Ito H, et al. Histopathologcial and clonal study of combined lobular and ductal carcinoma of the breast. Pathol Int. 2013;63:297-304.
63. Abdel-Fatah TM, Powe DG, Hodi Z, Lee AH, Reis-Filho JS, Ellis IO. High frequency of coexistence of columnar cell lesions, lobular neoplasia, and low grade ductal carcinoma in situ with invasive tubular carcinoma and invasive lobular carcinoma. Am J Surg Pathol. 2007;31:417-26.
64. Abdel-Fatah TM, Powe DG, Hodi Z, Reis-Filho JS, Lee AH, Ellis IO. Morphologic and molecular evolutionary pathways of low nuclear grade invasive breast cancers and their putative precursor lesions: further evidence to support the concept of low nuclear grade breast neoplasia family. Am J Surg Pathol. 2008;32:513-23.
65. Hungermann D, Schmidt H, Natrajan R, Tidow N, Poos K, Reis-Filho JS, et al. Influence of whole arm loss of chromosome 16q on gene expression patterns in oestrogen receptor-positive, invasive breast cancer. J Pathol. 2011;224:517-28.
66. Stacher E, Boldt V, Leibl S, Halbwedl I, Popper HH, Ullmann R, et al. Chromosomal aberrations as detected by array comparative genomic hybridization in early low-grade intraepithelial neoplasias of the breast. Histopathology. 2011;59:549-55.
67. King TA, Sakr RA, Muhsen S, Andrade VP, Giri D, Van Zee KJ, et al. Is there a low-grade precursor pathway in breast cancer? Ann Surg Oncol. 2012;19:1115-21.
68. Green AR, Krivinskas S, Young P, Rakha EA, Paish EC, Powe DG, et al. Loss of expression of chromosome 16q genes DPEP1 and CTCF in lobular carcinoma in situ of the breast. Breast Cancer Res Treat. 2009;113:59-66.
69. Foschini MP, Righi A, Cucchi MC, Ragazzini T, Merelli S, Santeramo B, et al. The impact of large sections and 3D technique on the study of lobular in situ and invasive carcinoma of the breast. Virchows Arch. 2006;448:256-61.
70. Claus EB, Risch N, Thompson WD, Carter D. Relationship between breast histopathology and family history of breast cancer. Cancer. 1993;71:147-53.
71. Petridis C, Shinomiya I, Kohut K, Gorman P, Caneppele M, Shah V, et al. Germline CDH1 mutations in bilateral lobular carcinoma in situ. Br J Cancer. 2014;110:1053-7.
72. Kluijt I, Siemerink EJ, Ausems MG, van Os TA, de Jong D, Simões-Correia J, et al. CDH1-related hereditary diffuse gastric cancer syndrome: clinical variations and implications for counseling. Int J Cancer. 2012;131:367-76.
73. Sawyer E, Roylance R, Petridis C, Brook MN, Nowinski S, Papouli E, et al. Genetic predisposition to in situ and invasive lobular carcinoma of the breast. PLoS Genet. 2014;10, e1004285.
74. Michailidou K, Hall P, Gonzalez-Neira A, Ghoussaini M, Dennis J, Milne RL, et al. Large-scale genotyping identifies 41 new loci associated with breast cancer risk. Nat Genet. 2013;45:353-61.
75. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med. 2013;19:1438-49.
76. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014;15:178-96.
77. Morrogh M, Andrade VP, Giri D, Sakr RA, Paik W, Qin LX, et al. Cadherin-catenin complex dissociation in lobular neoplasia of the breast. Breast Cancer Res Treat. 2012;132:641-52.
78. Cao D, Polyak K, Halushka MK, Nassar H, Kouprina N, Iacobuzio-Donahue C, et al. Serial analysis of gene expression of lobular carcinoma in situ identifies down regulation of claudin 4 and overexpression of matrix metalloproteinase 9. Breast Cancer Res. 2008;10:R91.
79. Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, et al. The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene. 2007;26:6979-88.
80. Aigner K, Descovich L, Mikula M, Sultan A, Dampier B, Bonné S, et al. The transcription factor ZEB1 (deltaEF1) represses Plakophilin 3 during human cancer progression. FEBS Lett. 2007;581:1617-24.
81. Fackler MJ, McVeigh M, Evron E, Garrett E, Mehrotra J, Polyak K, et al. DNA methylation of RASSF1A, HIN-1, RAR-beta, Cyclin D2 and Twist in in situ and invasive lobular breast carcinoma. Int J Cancer. 2003;107:970-5.
82. Anastasiadis PZ, Reynolds AB. Regulation of Rho GTPases by p120-catenin. Curr Opin Cell Biol. 2001;13:604-10.
83. Shibata T, Kokubu A, Sekine S, Kanai Y, Hirohashi S. Cytoplasmic p120ctn regulates the invasive phenotypes of E-cadherin-deficient breast cancer. Am J Pathol. 2004;164:2269-78.
84. Zou D, Yoon HS, Anjomshoaa A, Perez D, Fukuzawa R, Guilford P, et al. Increased levels of active c-Src distinguish invasive from in situ lobular lesions. Breast Cancer Res. 2009;11:R45.
85. Viacava P, Naccarato AG, Collecchi P, Ménard S, Castronovo V, Bevilacqua G. The spectrum of 67-kD laminin receptor expression in breast carcinoma progression. J Pathol. 1997;182:36-44.
86. Ang DC, Warrick AL, Shilling A, Beadling C, Corless CL, Troxell ML. Frequent phosphatidylinositol-3-kinase mutations in proliferative breast lesions. Mod Pathol. 2014;27:740-50.
87. Karakas B, Bachman KE, Park BH. Mutation of the PIK3CA oncogene in human cancers. Br J Cancer. 2006;94:455-9.
88. Irby RB, Yeatman TJ. Role of Src expression and activation in human cancer. Oncogene. 2000;19:5636-42.
89. Bratthauer GL, Strauss BL, Tavassoli FA. STAT 5a expression in various lesions of the breast. Virchows Arch. 2006;448:165-71.
90. Macias H, Hinck L. Mammary gland development. Wiley Interdiscip Rev Dev Biol. 2012;1:533-57.
91. Haricharan S, Dong J, Hein S, Reddy JP, Du Z, Toneff M, et al. Mechanism and preclinical prevention of increased breast cancer risk caused by pregnancy. Elife. 2013;2, e00996.
92. Tran-Thanh D, Arneson NC, Pintilie M, Deliallisi A, Warren KS, Bane A, et al. Amplification of the prolactin receptor gene in mammary lobular neoplasia. Breast Cancer Res Treat. 2011;128:31-40.
93. Bratthauer GL, Strauss BL, Barner R. Reversed expression of the JAK/STAT pathway related proteins prolactin receptor and STAT5a in normal and abnormal breast epithelial cells. Breast Cancer (Auckl). 2008;1:7-14.
94. Perrone G, Zagami M, Altomare V, Battista C, Morini S, Rabitti C. COX-2 localization within plasma membrane caveolae-like structures in human lobular intraepithelial neoplasia of the breast. Virchows Arch. 2007;451:1039-45.
95. Perrone G, Zagami M, Santini D, Vincenzi B, Gullotta G, Morini S, et al. COX-2 expression in lobular in situ neoplasia of the breast: correlation with histopathological grading system according to the Tavassoli classification. Histopathology. 2007;51:33-9.
96. Rizzo MT. Cyclooxygenase-2 in oncogenesis. Clin Chim Acta. 2011;412:671-87.
97. Vos CB, Cleton-Jansen AM, Berx G, de Leeuw WJ, ter Haar NT, van Roy F, et al. E-cadherin inactivation in lobular carcinoma in situ of the breast: an early event in tumorigenesis. Br J Cancer. 1997;76:1131-3.
98. Palacios J, Sarrió D, García-Macias MC, Bryant B, Sobel ME, Merino MJ. Frequent E-cadherin gene inactivation by loss of heterozygosity in pleomorphic lobular carcinoma of the breast. Mod Pathol. 2003;16:674-8.
99. Sarrió D, Moreno-Bueno G, Hardisson D, Sánchez-Estévez C, Guo M, Herman JG, et al. Epigenetic and genetic alterations of APC and CDH1 genes in lobular breast cancer: relationships with abnormal E-cadherin and catenin expression and microsatellite instability. Int J Cancer. 2003;106:208-15.
100. 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;18:741-51.
101. 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;54:91-7.