Lobular breast cancer: Pathology, biology, and options for clinical intervention

Archivum Immunologiae et Therapiae Experimentalis

Volumn 62, Issue 1, 2014, Pages 7-21

  Vlug, Eva ^a   Ercan, Cigdem ^a   Van Der Wall, Elsken ^a   Van Diest, Paul J ^a   Derksen, Patrick W B ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Clinical features; Lobular breast cancer; Molecular features; Pathological features

Indexed keywords

ADENOCARCINOMA; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CARCINOMA, LOBULAR; EPITHELIAL CELLS; FEMALE; HUMANS; PRECANCEROUS CONDITIONS;

EID: 84895068647     PISSN: 0004069X     EISSN: 16614917     Source Type: Journal    
DOI: 10.1007/s00005-013-0251-0     Document Type: Review

References (174)

1. Abdel-Fatah TM, Powe DG et al (2007) 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 31:417-426
2. Ademuyiwa FO, Khoury T et al (2012) An 81-year-old patient with distant metastasis of invasive lobular carcinoma occurring 41 years after mastectomy. Clin Breast Cancer 12:293-295
3. Arpino G, Bardou VJ et al (2004) Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 6:R149-R156
4. Ashikari R, Huvos AG et al (1973) Infiltrating lobular carcinoma of the breast. Cancer 31:110-116
5. Aulmann S, Penzel R et al (2008) Clonality of lobular carcinoma in situ (LCIS) and metachronous invasive breast cancer. Breast Cancer Res Treat 107:331-335
6. Bauer VP, Ditkoff BA et al (2003) The management of lobular neoplasia identified on percutaneous core breast biopsy. Breast J 9:4-9
7. Berg WA, Mrose HE et al (2001) Atypical lobular hyperplasia or lobular carcinoma in situ at core-needle breast biopsy. Radiology 218:503-509
8. Berx G, Van Roy F (2001) The E-cadherin/catenin complex: an important gatekeeper in breast cancer tumorigenesis and malignant progression. Breast Cancer Res 3:289-293
9. Berx G, Cleton-Jansen AM et al (1995) E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J 14:6107-6115
10. Berx G, Becker KF et al (1998) Mutations of the human E-cadherin (CDH1) gene. Hum Mutat 12:226-237
11. Beute BJ, Kalisher L et al (1991) Lobular carcinoma in situ of the breast: clinical, pathologic, and mammographic features. AJR Am J Roentgenol 157:257-265
12. Biglia N, Mariani L et al (2007) Increased incidence of lobular breast cancer in women treated with hormone replacement therapy: implications for diagnosis, surgical and medical treatment. Endocr Relat Cancer 14:549-567
13. Blanco-Aparicio C, Renner O et al (2007) PTEN, more than the AKT pathway. Carcinogenesis 28:1379-1386
14. Bodian CA, Perzin KH et al (1996) Lobular neoplasia. Long term risk of breast cancer and relation to other factors. Cancer 78:1024-1034
15. Boetes C, Veltman J et al (2004) The role of MRI in invasive lobular carcinoma. Breast Cancer Res Treat 86:31-37
16. Borgstein PJ, Pijpers R et al (1998) Sentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg 186:275-283
17. Boussadia O, Kutsch S et al (2002) E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev 115:53-62
18. Boyault S, Drouet Y et al (2012) Mutational characterization of individual breast tumors: TP53 and PI3 K pathway genes are frequently and distinctively mutated in different subtypes. Breast Cancer Res Treat 132:29-39
19. Bratthauer GL, Tavassoli FA (2002) Lobular intraepithelial neoplasia: previously unexplored aspects assessed in 775 cases and their clinical implications. Virchows Arch 440:134-138
20. Brem RF, Ioffe M et al (2009) Invasive lobular carcinoma: detection with mammography, sonography, MRI, and breast-specific gamma imaging. Am J Roentgenol 192:379-383
21. Broders AC (1932) Carcinoma in situ contrasted with benign penetrating epithelium. J Am Med Assoc 99:1670-1674
22. Buchanan CL, Flynn LW et al (2008) Is pleomorphic lobular carcinoma really a distinct clinical entity? J Surg Oncol 98:314-317
23. Buttitta F, Felicioni L et al (2006) PIK3CA mutation and histological type in breast carcinoma: high frequency of mutations in lobular carcinoma. J Pathol 208:350-355
24. Cancer Genome Atlas Network (2012) Comprehensive molecular portraits of human breast tumours. Nature 490:61-70
25. Cannon-Albright LA, Thomas A et al (1994) Familiality of cancer in Utah. Cancer Res 54:2378-2385
26. Carter D, Smith RR (1977) Carcinoma in situ of the breast. Cancer 40:1189-1193
27. Chen YY, Hwang ES et al (2009) Genetic and phenotypic characteristics of pleomorphic lobular carcinoma in situ of the breast. Am J Surg Pathol 33:1683-1694
28. Christgen M, Noskowicz M et al (2012) IPH-926 lobular breast cancer cells harbor a p53 mutant with temperature-sensitive functional activity and allow for profiling of p53-responsive genes. Lab Invest 92:1635-1647
29. Christgen M, Noskowicz M et al (2013) Oncogenic PIK3CA mutations in lobular breast cancer progression. Genes Chromosom Cancer 52:69-80
30. Chuba PJ, Hamre MR et al (2005) Bilateral risk for subsequent breast cancer after lobular carcinoma-in situ: analysis of surveillance, epidemiology, and end results data. J Clin Oncol 23:5534-5541
31. Clarke M, Collins R et al (2005) Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet 366:2087-2106
32. Cohen MA (2004) Cancer upgrades at excisional biopsy after diagnosis of atypical lobular hyperplasia or lobular carcinoma in situ at core-needle biopsy: some reasons why. Radiology 231:617-621
33. Cristofanilli M, Gonzalez-Angulo A et al (2005) Invasive lobular carcinoma classic type: response to primary chemotherapy and survival outcomes. J Clin Oncol 23:41-48
34. Curtis C, Shah SP et al (2012) The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486:346-352
35. Cutuli B, de Lafontan B et al (2005) Breast-conserving surgery and radiotherapy: a possible treatment for lobular carcinoma in situ? Eur J Cancer 41:380-385
36. Da Silva L, Parry S et al (2008) Aberrant expression of E-cadherin in lobular carcinomas of the breast. Am J Surg Pathol 32:773-783
37. Davis MA, Ireton RC et al (2003) A core function for p120-catenin in cadherin turnover. J Cell Biol 163:525-534
38. De Leeuw WJ, Berx G et al (1997) Simultaneous loss of E-cadherin and catenins in invasive lobular breast cancer and lobular carcinoma in situ. J Pathol 183:404-411
39. Derksen PW, Liu X et al (2006) Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437-449
40. Derksen PW, Braumuller TM et al (2011) Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice. Dis Model Mech 4:347-358
41. Downs-Kelly E, Bell D et al (2011) Clinical implications of margin involvement by pleomorphic lobular carcinoma in situ. Arch Pathol Lab Med 135:737-743
42. Drees F, Pokutta S et al (2005) Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123:903-915
43. Droufakou S, Deshmane V et al (2001) Multiple ways of silencing E-cadherin gene expression in lobular carcinoma of the breast. Int J Cancer 92:404-408
44. Dupont Jensen J, Laenkholm AV et al (2011) PIK3CA mutations may be discordant between primary and corresponding metastatic disease in breast cancer. Clin Cancer Res 17:667-677
45. Elsheikh TM, Silverman JF (2005) Follow-up surgical excision is indicated when breast core needle biopsies show atypical lobular hyperplasia or lobular carcinoma in situ: a correlative study of 33 patients with review of the literature. Am J Surg Pathol 29:534-543
46. Ercan C, van Diest PJ et al (2012a) p53 mutations in classic and pleomorphic invasive lobular carcinoma of the breast. Cell Oncol 35:111-118
47. Ercan C, Vermeulen JF et al (2012b) HIF-1alpha and NOTCH signaling in ductal and lobular carcinomas of the breast. Cell Oncol 35:435-442
48. Eusebi V, Magalhaes F et al (1992) Pleomorphic lobular carcinoma of the breast: an aggressive tumor showing apocrine differentiation. Hum Pathol 23:655-662
49. Ewing J (1919) Neoplastic diseases: a textbook on tumors. WB Saunders Co., Philadelphia
50. Fackler MJ, McVeigh M et al (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
51. Fadare O, Wang SA et al (2008) The expression of cytokeratin 5/6 in invasive lobular carcinoma of the breast: evidence of a basal-like subset? Hum Pathol 39:331-336
52. Fechner RE (1975) Histologic variants of infiltrating lobular carcinoma of the breast. Hum Pathol 6:373-378
53. Fisher B, Costantino JP et al (1998) Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 90:1371-1388
54. Fisher ER, Land SR et al (2004) Pathologic findings from the National Surgical Adjuvant Breast and Bowel Project: twelve-year observations concerning lobular carcinoma in situ. Cancer 100:238-244
55. Foote FW, Stewart FW (1941) Lobular carcinoma in situ: a rare form of mammary cancer. Am J Pathol 17:491-496
56. Frolik D, Caduff R et al (2001) Pleomorphic lobular carcinoma of the breast: its cell kinetics, expression of oncogenes and tumour suppressor genes compared with invasive ductal carcinomas and classical infiltrating lobular carcinomas. Histopathology 39:503-513
57. Frykberg ER (1999) Lobular carcinoma in situ of the breast. Breast J 5:296-303
58. Fujita Y, Krause G et al (2002) Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 4:222-231
59. Gayther SA, Gorringe KL et al (1998) Identification of germ-line E-cadherin mutations in gastric cancer families of European origin. Cancer Res 58:4086-4089
60. Georgian-Smith D, Lawton TJ (2001) Calcifications of lobular carcinoma in situ of the breast: radiologic-pathologic correlation. Am J Roentgenol 176:1255-1259
61. Geyer FC, Lacroix-Triki M et al (2011) Beta-Catenin pathway activation in breast cancer is associated with triple-negative phenotype but not with CTNNB1 mutation. Mod Pathol 24:209-231
62. Goldwyn RM (1977) Subcutaneous mastectomy. N Engl J Med 297:503-505
63. Guilford P, Hopkins J et al (1998) E-cadherin germline mutations in familial gastric cancer. Nature 392:402-405
64. Haagensen CD, Lane N et al (1978) Lobular neoplasia (so-called lobular carcinoma in situ) of the breast. Cancer 42:737-769
65. Hajdu SI, Tang P (2009) Lobular carcinoma in situ. Ann Clin Lab Sci 39:413-415
66. Halsted WS (1898) I. A clinical and histological study of certain adenocarcinomata of the breast: and a brief consideration of the supraclavicular operation and of the results of operations for cancer of the breast from 1889 to 1898 at the Johns Hopkins Hospital. Ann Surg 28:557-576
67. Han SP, Yap AS (2012) The cytoskeleton and classical cadherin adhesions. Subcell Biochem 60:111-135
68. Hartsock A, Nelson WJ (2012) Competitive regulation of E-cadherin juxtamembrane domain degradation by p120-catenin binding and Hakai-mediated ubiquitination. PLoS ONE 7:e37476
69. Harvey DG, Fechner RE (1978) Atypical lobular and papillary lesions of the breast: a follow-up study of 30 cases. South Med J 71:361-364
70. Hayes MJ, Thomas D et al (2008) Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin Cancer Res 14:4038-4044
71. Hazan RB, Norton L (1998) The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J Biol Chem 273:9078-9084
72. Hazan RB, Kang L et al (1997) Vinculin is associated with the E-cadherin adhesion complex. J Biol Chem 272:32448-32453
73. Hernandez-Aya LF, Gonzalez-Angulo AM (2011) Targeting the phosphatidylinositol 3-kinase signaling pathway in breast cancer. Oncologist 16:404-414
74. Hoefnagel LD, van de Vijver MJ et al (2010) Receptor conversion in distant breast cancer metastases. Breast Cancer Res 12:R75
75. Hollestelle A, Elstrodt F et al (2010) Four human breast cancer cell lines with biallelic inactivating alpha-catenin gene mutations. Breast Cancer Res Treat 122:125-133
76. Hong S, Troyanovsky RB et al (2010) Spontaneous assembly and active disassembly balance adherens junction homeostasis. Proc Natl Acad Sci USA 107:3528-3533
77. Huang CH, Mandelker D et al (2008) Insights into the oncogenic effects of PIK3CA mutations from the structure of p110alpha/p85alpha. Cell Cycle 7:1151-1156
78. Hussain M, Cunnick GH (2011) Management of lobular carcinoma in situ and atypical lobular hyperplasia of the breast-a review. Eur J Surg Oncol 37:279-289
79. Hutter RV, Snyder RE et al (1969) Clinical and pathologic correlation with mammographic findings in lobular carcinoma in situ. Cancer 23:826-839
80. Hwang ES, Nyante SJ et al (2004) Clonality of lobular carcinoma in situ and synchronous invasive lobular carcinoma. Cancer 100:2562-2572
81. Iorfida M, Maiorano E et al (2012) Invasive lobular breast cancer: subtypes and outcome. Breast Cancer Res Treat 133:713-723
82. Jonsson BA, Bergh A et al (2002) Germline mutations in E-cadherin do not explain association of hereditary prostate cancer, gastric cancer and breast cancer. Int J Cancer 98:838-843
83. Kalinsky K, Heguy A et al (2011) PIK3CA mutations rarely demonstrate genotypic intratumoral heterogeneity and are selected for in breast cancer progression. Breast Cancer Res Treat 129:635-643
84. Kaurah P, MacMillan A et al (2007) Founder and recurrent CDH1 mutations in families with hereditary diffuse gastric cancer. JAMA 297:2360-2372
85. Kizaka-Kondoh S, Inoue M et al (2003) Tumor hypoxia: a target for selective cancer therapy. Cancer Sci 94:1021-1028
86. Krecke KN, Gisvold JJ (1993) Invasive lobular carcinoma of the breast: mammographic findings and extent of disease at diagnosis in 184 patients. Am J Roentgenol 161:957-960
87. Kurose K, Gilley K et al (2002) Frequent somatic mutations in PTEN and TP53 are mutually exclusive in the stroma of breast carcinomas. Nat Genet 32:355-357
88. Le TL, Yap AS et al (1999) Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J Cell Biol 146:219-232
89. Leary RJ, Kinde I et al (2010) Development of personalized tumor biomarkers using massively parallel sequencing. Sci Transl Med 2:20ra14
90. Li CI, Daling JR (2007) Changes in breast cancer incidence rates in the United States by histologic subtype and race/ethnicity, 1995 to 2004. Cancer Epidemiol Biomarkers Prev 16:2773-2780
91. Li CI, Anderson BO et al (2002a) Changing incidence of lobular carcinoma in situ of the breast. Breast Cancer Res Treat 75:259-268
92. Li CI, Daling JR et al (2005) Age-specific incidence rates of in situ breast carcinomas by histologic type, 1980 to 2001. Cancer Epidemiol Biomarkers Prev 14:1008-1011
93. Li CI, Malone KE et al (2006) Risk of invasive breast carcinoma among women diagnosed with ductal carcinoma in situ and lobular carcinoma in situ, 1988-2001. Cancer 106:2104-2112
94. Li G, Robinson GW et al (2002b) Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. Development 129:4159-4170
95. Liberman L (2000) Clinical management issues in percutaneous core breast biopsy. Radiol Clin North Am 38:791-807
96. Liberman L, Sama M et al (1999) Lobular carcinoma in situ at percutaneous breast biopsy: surgical biopsy findings. Am J Roentgenol 173:291-299
97. Ligon LA, Karki S et al (2001) Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol 3:913-917
98. Londero V, Zuiani C et al (2008) Lobular neoplasia: core needle breast biopsy underestimation of malignancy in relation to radiologic and pathologic features. Breast 17:623-630
99. Maehama T, Dixon JE (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 273:13375-13378
100. Mahtani RL, Vogel CL (2008) Pleomorphic lobular carcinoma of the breast: four long-term responders to trastuzumab-coincidence or hint? J Clin Oncol 26:5823-5824
101. Maiden SL, Hardin J (2011) The secret life of alpha-catenin: moonlighting in morphogenesis. J Cell Biol 195:543-552
102. Masciari S, Larsson N et al (2007) Germline E-cadherin mutations in familial lobular breast cancer. J Med Genet 44:726-731
103. Mastracci TL, Shadeo A et al (2006) Genomic alterations in lobular neoplasia: a microarray comparative genomic hybridization signature for early neoplastic proliferation in the breast. Genes Chromosomes Cancer 45:1007-1017
104. Mate TP, Carter D et al (1986) A clinical and histopathologic analysis of the results of conservation surgery and radiation therapy in stage I and II breast carcinoma. Cancer 58:1995-2002
105. McAuliffe PF, Meric-Bernstam F et al (2010) Deciphering the role of PI3 K/Akt/mTOR pathway in breast cancer biology and pathogenesis. Clin Breast Cancer 10(Suppl 3):S59-S65
106. McBride DJ, Orpana AK et al (2010) Use of cancer-specific genomic rearrangements to quantify disease burden in plasma from patients with solid tumors. Genes Chromosomes Cancer 49:1062-1069
107. Meng W, Mushika Y et al (2008) Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135:948-959
108. Mercapide J, Zhang SY et al (2002) CCND1- and ERBB2-gene deregulation and PTEN mutation analyses in invasive lobular carcinoma of the breast. Mol Carcinog 35:6-12
109. Middleton LP, Palacios DM et al (2000) Pleomorphic lobular carcinoma: morphology, immunohistochemistry, and molecular analysis. Am J Surg Pathol 24:1650-1656
110. Miyashita Y, Ozawa M (2007) A dileucine motif in its cytoplasmic domain directs beta-catenin-uncoupled E-cadherin to the lysosome. J Cell Sci 120(Pt 24):4395-4406
111. Monhollen L, Morrison C et al (2012) Pleomorphic lobular carcinoma: a distinctive clinical and molecular breast cancer type. Histopathology 61:365-377
112. Morandi L, Marucci G et al (2006) Genetic similarities and differences between lobular in situ neoplasia (LN) and invasive lobular carcinoma of the breast. Virchows Arch 449:14-23
113. Nagata Y, Lan KH et al (2004) PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 6:117-127
114. NCCN (2010) Clinical Practice Guidelines in Oncology, Breast Cancer Version 1.2013. NCCN, The National Comprehensive Cancer Network
115. Nemoto T, Castillo N et al (1998) Lobular carcinoma in situ with microinvasion. J Surg Oncol 67:41-46
116. Nik-Zainal S, Van Loo P et al (2012) The life history of 21 breast cancers. Cell 149:994-1007
117. Nishizaki T, Chew K et al (1997) Genetic alterations in lobular breast cancer by comparative genomic hybridization. Int J Cancer 74:513-517
118. Oliveira C, Bordin MC et al (2002) Screening E-cadherin in gastric cancer families reveals germline mutations only in hereditary diffuse gastric cancer kindred. Hum Mutat 19:510-517
119. Olivier M, Langerod A et al (2006) The clinical value of somatic TP53 gene mutations in 1,794 patients with breast cancer. Clin Cancer Res 12:1157-1167
120. Orsetti B, Nugoli M et al (2006) Genetic profiling of chromosome 1 in breast cancer: mapping of regions of gains and losses and identification of candidate genes on 1q. Br J Cancer 95:1439-1447
121. Orvieto E, Maiorano E et al (2008) Clinicopathologic characteristics of invasive lobular carcinoma of the breast: results of an analysis of 530 cases from a single institution. Cancer 113:1511-1520
122. Ottesen GL, Graversen HP et al (1993) Lobular carcinoma in situ of the female breast. Short-term results of a prospective nationwide study. The Danish Breast Cancer Cooperative Group. Am J Surg Pathol 17:14-21
123. Page DL, Jensen RA et al (2000) Historical and epidemiologic background of human premalignant breast disease. J Mammary Gland Biol Neoplasia 5:341-349
124. Palacios J, Benito N et al (1995) Anomalous expression of P-cadherin in breast carcinoma. Correlation with E-cadherin expression and pathological features. Am J Pathol 146:605-612
125. Palacios J, Sarrio D et al (2003) Frequent E-cadherin gene inactivation by loss of heterozygosity in pleomorphic lobular carcinoma of the breast. Mod Pathol 16:674-678
126. Perou CM, Sorlie T et al (2000) Molecular portraits of human breast tumours. Nature 406:747-752
127. Pestalozzi BC, Zahrieh D et al (2008) Distinct clinical and prognostic features of infiltrating lobular carcinoma of the breast: combined results of 15 International Breast Cancer Study Group clinical trials. J Clin Oncol 26:3006-3014
128. Pharoah PD, Guilford P et al (2001) Incidence of gastric cancer and breast cancer in CDH1 (E-cadherin) mutation carriers from hereditary diffuse gastric cancer families. Gastroenterology 121:1348-1353
129. Pope TL Jr, Fechner RE et al (1988) Lobular carcinoma in situ of the breast: mammographic features. Radiology 168:63-66
130. Powers RW, O'Brien PH et al (1980) Lobular carcinoma in situ. J Surg Oncol 13:269-273
131. Rakha EA, El-Sayed ME et al (2008) Invasive lobular carcinoma of the breast: response to hormonal therapy and outcomes. Eur J Cancer 44:73-83
132. Rakha EA, Patel A et al (2010) Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast. Am J Surg Pathol 34:1472-1479
133. Ratheesh A, Gomez GA et al (2012) Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 14:818-828
134. Reis-Filho JS, Simpson PT et al (2005) Pleomorphic lobular carcinoma of the breast: role of comprehensive molecular pathology in characterization of an entity. J Pathol 207:1-13
135. Renshaw AA, Cartagena N et al (2002) Lobular neoplasia in breast core needle biopsy specimens is not associated with an increased risk of ductal carcinoma in situ or invasive carcinoma. Am J Clin Pathol 117:797-799
136. Richard F, Pacyna-Gengelbach M et al (2000) Patterns of chromosomal imbalances in invasive breast cancer. Int J Cancer 89:305-310
137. Rosen PP, Lesser ML et al (1982) Epidemiology of breast carcinoma III: relationship of family history to tumor type. Cancer 50:171-179
138. Rosenfeld I, Tartter PI et al (2001) The significance of malignancies incidental to microcalcifications in breast spot localization biopsy specimens. Am J Surg 182:1-5
139. Rosenthal SI, Depowski PL et al (2002) Comparison of HER-2/neu oncogene amplification detected by fluorescence in situ hybridization in lobular and ductal breast cancer. Appl Immunohistochem Mol Morphol 10:40-46
140. Ross DS, Hoda SA (2011) Microinvasive (T1mic) lobular carcinoma of the breast: clinicopathologic profile of 16 cases. Am J Surg Pathol 35:750-756
141. Sapino A, Frigerio A et al (2000) Mammographically detected in situ lobular carcinomas of the breast. Virchows Arch 436:421-430
142. Sarrio D, Moreno-Bueno G et al (2003) 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 106:208-215
143. Sarrio D, Perez-Mies B et al (2004) Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions. Oncogene 23:3272-3283
144. Sastre-Garau X, Jouve M et al (1996) Infiltrating lobular carcinoma of the breast. Clinicopathologic analysis of 975 cases with reference to data on conservative therapy and metastatic patterns. Cancer 77:113-120
145. Schackmann RC, van Amersfoort M et al (2011) Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest 121:3176-3188
146. Selinko VL, Middleton LP et al (2004) Role of sonography in diagnosing and staging invasive lobular carcinoma. J Clin Ultrasound 32:323-332
147. Shah SP, Morin RD et al (2009) Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461:809-813
148. Shao MM, Chan SK et al (2012) Keratin expression in breast cancers. Virchows Arch 461:313-322
149. Shin SJ, Rosen PP (2002) Excisional biopsy should be performed if lobular carcinoma in situ is seen on needle core biopsy. Arch Pathol Lab Med 126:697-701
150. Simpson PT, Reis-Filho JS et al (2008) Molecular profiling pleomorphic lobular carcinomas of the breast: evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol 215:231-244
151. Sneige N, Wang J et al (2002) Clinical, histopathologic, and biologic features of pleomorphic lobular (ductal-lobular) carcinoma in situ of the breast: a report of 24 cases. Mod Pathol 15:1044-1050
152. Sonnenfeld MR, Frenna TH et al (1991) Lobular carcinoma in situ: mammographic-pathologic correlation of results of needle-directed biopsy. Radiology 181:363-367
153. Sorlie T, Perou CM et al (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98:10869-10874
154. Soussi T (2007) p53 alterations in human cancer: more questions than answers. Oncogene 26:2145-2156
155. Sun H, Lesche R et al (1999) PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci USA 96:6199-6204
156. Tirkkonen M, Tanner M et al (1998) Molecular cytogenetics of primary breast cancer by CGH. Genes Chromosomes Cancer 21:177-184
157. Toikkanen S, Pylkkanen L et al (1997) Invasive lobular carcinoma of the breast has better short- and long-term survival than invasive ductal carcinoma. Br J Cancer 76:1234-1240
158. Troyanovsky RB, Klingelhofer J et al (2011) Alpha-Catenin contributes to the strength of E-cadherin-p120 interactions. Mol Biol Cell 22:4247-4255
159. Tubiana-Hulin M, Stevens D et al (2006) Response to neoadjuvant chemotherapy in lobular and ductal breast carcinomas: a retrospective study on 860 patients from one institution. Ann Oncol 17:1228-1233
160. Urban JA (1967) Bilaterality of cancer of the breast. Biopsy of the opposite breast. Cancer 20:1867-1870
161. Utermark T, Rao T et al (2012) The p110alpha and p110beta isoforms of PI3 K play divergent roles in mammary gland development and tumorigenesis. Genes Dev 26:1573-1586
162. van Esser S, Stapper G et al (2009) Ultrasound-guided laser-induced thermal therapy for small palpable invasive breast carcinomas: a feasibility study. Ann Surg Oncol 16:2259-2263
163. Verschuur-Maes AH, van Deurzen CH et al (2012) Columnar cell lesions on breast needle biopsies: is surgical excision necessary? A systematic review. Ann Surg 255:259-265
164. Vogel VG, Costantino JP et al (2006) 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 295:2727-2741
165. Vogel VG, Costantino JP et al (2010) Update of the National Surgical Adjuvant Breast and Bowel Project Study of Tamoxifen and Raloxifene (STAR) P-2 Trial: preventing breast cancer. Cancer Prev Res 3:696-706
166. Vos CB, Cleton-Jansen AM et al (1997) E-cadherin inactivation in lobular carcinoma in situ of the breast: an early event in tumorigenesis. Br J Cancer 76:1131-1133
167. Weidner N, Semple JP (1992) Pleomorphic variant of invasive lobular carcinoma of the breast. Hum Pathol 23:1167-1171
168. Weigelt B, Geyer FC et al (2010) The molecular underpinning of lobular histological growth pattern: a genome-wide transcriptomic analysis of invasive lobular carcinomas and grade- and molecular subtype-matched invasive ductal carcinomas of no special type. J Pathol 220:45-57
169. Wheeler JE, Enterline HT et al (1974) Lobular carcinoma in situ of the breast. Long-term followup. Cancer 34:554-563
170. WHO (2010) World Health Statistics 2010. World Health Organization, Geneva
171. Wood LD, Parsons DW et al (2007) The genomic landscapes of human breast and colorectal cancers. Science 318:1108-1113
172. Xie ZM, Li LS et al (2011) Germline mutations of the E-cadherin gene in families with inherited invasive lobular breast carcinoma but no diffuse gastric cancer. Cancer 117:3112-3117
173. Yamada S, Pokutta S et al (2005) Deconstructing the cadherin-catenin- actin complex. Cell 123:889-901
174. Yanagisawa M, Kaverina IN et al (2004) A novel interaction between kinesin and p120 modulates p120 localization and function. J Biol Chem 279:9512-9521