Skip to main content
Top
Published in: Breast Cancer Research 1/2015

Open Access 01-12-2015 | Review

Lobular breast cancer: molecular basis, mouse and cellular models

Authors: Matthias Christgen, Patrick WB Derksen

Published in: Breast Cancer Research | Issue 1/2015

Login to get access

Abstract

Infiltrating lobular breast cancer (ILC) is the most common special breast cancer subtype. With mutational or epigenetic inactivation of the cell adhesion molecule E-cadherin (CDH1) being confined almost exclusively to ILC, this tumor entity stands out from all other types of breast cancers. The molecular basis of ILC is linked to loss of E-cadherin, as evidenced by human CDH1 germline mutations and conditional knockout mouse models. A better understanding of ILC beyond the level of descriptive studies depends on physiologically relevant and functional tools. This review provides a detailed overview on ILC models, including well-characterized cell lines, xenograft tumors and genetically engineered mouse models. We consider advantages and limitations of these models and evaluate their representativeness for human ILC. The still incompletely defined mechanisms by which loss of E-cadherin drives malignant transformation are discussed based on recent findings in these models. Moreover, candidate genes and signaling pathways potentially involved in ILC development and progression as well as anticancer drug and endocrine resistance are highlighted.
Literature
2.
go back to reference Willis RA. Epithelial tumours of the breast. In: Willis RA, editor. Pathology of tumours. London: Butterworth Co. Ltd; 1948. p. 208–57. Willis RA. Epithelial tumours of the breast. In: Willis RA, editor. Pathology of tumours. London: Butterworth Co. Ltd; 1948. p. 208–57.
3.
go back to reference Hyafil F, Babinet C, Jacob F. Cell–cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell. 1981;26:447–54.CrossRefPubMed Hyafil F, Babinet C, Jacob F. Cell–cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell. 1981;26:447–54.CrossRefPubMed
5.
go back to reference Moll R, Mitze M, Frixen UH, Birchmeier W. Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am J Pathol. 1993;143:1731–42.PubMedPubMedCentral Moll R, Mitze M, Frixen UH, Birchmeier W. Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am J Pathol. 1993;143:1731–42.PubMedPubMedCentral
6.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
7.
go back to reference Berx G, Cleton-Jansen AM, Nollet F, de Leeuw WJ, van de Vijver M, Cornelisse C, et al. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. Embo J. 1995;14:6107–15.PubMedPubMedCentral Berx G, Cleton-Jansen AM, Nollet F, de Leeuw WJ, van de Vijver M, Cornelisse C, et al. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. Embo J. 1995;14:6107–15.PubMedPubMedCentral
8.
go back to reference Droufakou S, Deshmane V, Roylance R, Hanby A, Tomlinson I, Hart IR. Multiple ways of silencing E-cadherin gene expression in lobular carcinoma of the breast. Int J Cancer. 2001;92:404–8.CrossRefPubMed Droufakou S, Deshmane V, Roylance R, Hanby A, Tomlinson I, Hart IR. Multiple ways of silencing E-cadherin gene expression in lobular carcinoma of the breast. Int J Cancer. 2001;92:404–8.CrossRefPubMed
10.
go back to reference Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, et al. E-cadherin germline mutations in familial gastric cancer. Nature. 1998;392:402–5.CrossRefPubMed Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, et al. E-cadherin germline mutations in familial gastric cancer. Nature. 1998;392:402–5.CrossRefPubMed
11.
go back to reference Benusiglio PR, Malka D, Rouleau E, De Pauw A, Buecher B, Nogues C, et al. CDH1 germline mutations and the hereditary diffuse gastric and lobular breast cancer syndrome: a multicentre study. J Med Genet. 2013;50:486–9.CrossRefPubMed Benusiglio PR, Malka D, Rouleau E, De Pauw A, Buecher B, Nogues C, et al. CDH1 germline mutations and the hereditary diffuse gastric and lobular breast cancer syndrome: a multicentre study. J Med Genet. 2013;50:486–9.CrossRefPubMed
12.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference Sarrio D, Perez-Mies B, Hardisson D, Moreno-Bueno G, Suarez A, Cano A, et al. Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions. Oncogene. 2004;23:3272–83.CrossRefPubMed Sarrio D, Perez-Mies B, Hardisson D, Moreno-Bueno G, Suarez A, Cano A, et al. Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions. Oncogene. 2004;23:3272–83.CrossRefPubMed
14.
go back to reference Schackmann RC, van Amersfoort M, Haarhuis JH, Vlug EJ, Halim VA, Roodhart JM, et al. Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest. 2011;121:3176–88.CrossRefPubMedPubMedCentral Schackmann RC, van Amersfoort M, Haarhuis JH, Vlug EJ, Halim VA, Roodhart JM, et al. Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest. 2011;121:3176–88.CrossRefPubMedPubMedCentral
15.
go back to reference Bertucci F, Orsetti B, Negre V, Finetti P, Rouge C, Ahomadegbe JC, et al. Lobular and ductal carcinomas of the breast have distinct genomic and expression profiles. Oncogene. 2008;27:5359–72.CrossRefPubMedPubMedCentral Bertucci F, Orsetti B, Negre V, Finetti P, Rouge C, Ahomadegbe JC, et al. Lobular and ductal carcinomas of the breast have distinct genomic and expression profiles. Oncogene. 2008;27:5359–72.CrossRefPubMedPubMedCentral
16.
go back to reference Rakha EA, El-Sayed ME, Powe DG, Green AR, Habashy H, Grainge MJ, et al. Invasive lobular carcinoma of the breast: response to hormonal therapy and outcomes. Eur J Cancer. 2008;44:73–83.CrossRefPubMed Rakha EA, El-Sayed ME, Powe DG, Green AR, Habashy H, Grainge MJ, et al. Invasive lobular carcinoma of the breast: response to hormonal therapy and outcomes. Eur J Cancer. 2008;44:73–83.CrossRefPubMed
17.
go back to reference Ross JS, Wang K, Sheehan CE, Boguniewicz AB, Otto G, Downing SR, et al. Relapsed classic E-cadherin (CDH1)-mutated invasive lobular breast cancer shows a high frequency of HER2 (ERBB2) gene mutations. Clin Cancer Res. 2013;19:2668–76.CrossRefPubMed Ross JS, Wang K, Sheehan CE, Boguniewicz AB, Otto G, Downing SR, et al. Relapsed classic E-cadherin (CDH1)-mutated invasive lobular breast cancer shows a high frequency of HER2 (ERBB2) gene mutations. Clin Cancer Res. 2013;19:2668–76.CrossRefPubMed
18.
go back to reference Christgen M, Noskowicz M, Schipper E, Christgen H, Heil C, Krech T, et al. Oncogenic PIK3CA mutations in lobular breast cancer progression. Genes Chromosomes Cancer. 2013;52:69–80.CrossRefPubMed Christgen M, Noskowicz M, Schipper E, Christgen H, Heil C, Krech T, et al. Oncogenic PIK3CA mutations in lobular breast cancer progression. Genes Chromosomes Cancer. 2013;52:69–80.CrossRefPubMed
19.
go back to reference Simpson PT, Reis-Filho JS, Lambros MB, Jones C, Steele D, Mackay A, et al. Molecular profiling pleomorphic lobular carcinomas of the breast: evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol. 2008;215:231–44.CrossRefPubMed Simpson PT, Reis-Filho JS, Lambros MB, Jones C, Steele D, Mackay A, et al. Molecular profiling pleomorphic lobular carcinomas of the breast: evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol. 2008;215:231–44.CrossRefPubMed
20.
go back to reference Ercan C, van Diest PJ, van der Ende B, Hinrichs J, Bult P, Buerger H, et al. p53 mutations in classic and pleomorphic invasive lobular carcinoma of the breast. Cell Oncol (Dordr). 2012;35:111–8.CrossRef Ercan C, van Diest PJ, van der Ende B, Hinrichs J, Bult P, Buerger H, et al. p53 mutations in classic and pleomorphic invasive lobular carcinoma of the breast. Cell Oncol (Dordr). 2012;35:111–8.CrossRef
21.
go back to reference Korkola JE, DeVries S, Fridlyand J, Hwang ES, Estep AL, Chen YY, et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 2003;63:7167–75.PubMed Korkola JE, DeVries S, Fridlyand J, Hwang ES, Estep AL, Chen YY, et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 2003;63:7167–75.PubMed
22.
go back to reference Weigelt B, Geyer FC, Natrajan R, Lopez-Garcia MA, Ahmad AS, Savage K, et al. 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. 2010;220:45–57.CrossRefPubMed Weigelt B, Geyer FC, Natrajan R, Lopez-Garcia MA, Ahmad AS, Savage K, et al. 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. 2010;220:45–57.CrossRefPubMed
24.
go back to reference Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 2006;10:515–27.CrossRefPubMedPubMedCentral Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 2006;10:515–27.CrossRefPubMedPubMedCentral
25.
go back to reference Cailleau R, Young R, Olive M, Reeves Jr WJ. Breast tumor cell lines from pleural effusions. J Natl Cancer Inst. 1974;53:661–74.PubMed Cailleau R, Young R, Olive M, Reeves Jr WJ. Breast tumor cell lines from pleural effusions. J Natl Cancer Inst. 1974;53:661–74.PubMed
26.
go back to reference Engel LW, Young NA. Human breast carcinoma cells in continuous culture: a review. Cancer Res. 1978;38:4327–39.PubMed Engel LW, Young NA. Human breast carcinoma cells in continuous culture: a review. Cancer Res. 1978;38:4327–39.PubMed
27.
go back to reference Rye PD, Norum L, Olsen DR, Garman-Vik S, Kaul S, Fodstad O. Brain metastasis model in athymic nude mice using a novel MUC1-secreting human breast-cancer cell line, MA11. Int J Cancer. 1996;68:682–7.CrossRefPubMed Rye PD, Norum L, Olsen DR, Garman-Vik S, Kaul S, Fodstad O. Brain metastasis model in athymic nude mice using a novel MUC1-secreting human breast-cancer cell line, MA11. Int J Cancer. 1996;68:682–7.CrossRefPubMed
28.
go back to reference Ethier SP, Mahacek ML, Gullick WJ, Frank TS, Weber BL. Differential isolation of normal luminal mammary epithelial cells and breast cancer cells from primary and metastatic sites using selective media. Cancer Res. 1993;53:627–35.PubMed Ethier SP, Mahacek ML, Gullick WJ, Frank TS, Weber BL. Differential isolation of normal luminal mammary epithelial cells and breast cancer cells from primary and metastatic sites using selective media. Cancer Res. 1993;53:627–35.PubMed
29.
go back to reference Gazdar AF, Kurvari V, Virmani A, Gollahon L, Sakaguchi M, Westerfield M, et al. Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer. Int J Cancer. 1998;78:766–74.CrossRefPubMed Gazdar AF, Kurvari V, Virmani A, Gollahon L, Sakaguchi M, Westerfield M, et al. Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer. Int J Cancer. 1998;78:766–74.CrossRefPubMed
30.
go back to reference Christgen M, Bruchhardt H, Hadamitzky C, Rudolph C, Steinemann D, Gadzicki D, et al. Comprehensive genetic and functional characterization of IPH-926: a novel CDH1-null tumour cell line from human lobular breast cancer. J Pathol. 2009;217:620–32.CrossRefPubMed Christgen M, Bruchhardt H, Hadamitzky C, Rudolph C, Steinemann D, Gadzicki D, et al. Comprehensive genetic and functional characterization of IPH-926: a novel CDH1-null tumour cell line from human lobular breast cancer. J Pathol. 2009;217:620–32.CrossRefPubMed
31.
go back to reference Jambal P, Badtke MM, Harrell JC, Borges VF, Post MD, Sollender GE, et al. Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features. Breast Cancer Res Treat. 2012;137:431–48.CrossRefPubMedPubMedCentral Jambal P, Badtke MM, Harrell JC, Borges VF, Post MD, Sollender GE, et al. Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features. Breast Cancer Res Treat. 2012;137:431–48.CrossRefPubMedPubMedCentral
32.
go back to reference Hollestelle A, Peeters JK, Smid M, Timmermans M, Verhoog LC, Westenend PJ, et al. Loss of E-cadherin is not a necessity for epithelial to mesenchymal transition in human breast cancer. Breast Cancer Res Treat. 2013;138:47–57.CrossRefPubMed Hollestelle A, Peeters JK, Smid M, Timmermans M, Verhoog LC, Westenend PJ, et al. Loss of E-cadherin is not a necessity for epithelial to mesenchymal transition in human breast cancer. Breast Cancer Res Treat. 2013;138:47–57.CrossRefPubMed
33.
go back to reference Karch I, Schipper E, Christgen H, Kreipe H, Lehmann U, Christgen M. Is upregulation of BCL2 a determinant of tumor development driven by inactivation of CDH1/E-cadherin? PLoS One. 2013;8:e73062.CrossRefPubMedPubMedCentral Karch I, Schipper E, Christgen H, Kreipe H, Lehmann U, Christgen M. Is upregulation of BCL2 a determinant of tumor development driven by inactivation of CDH1/E-cadherin? PLoS One. 2013;8:e73062.CrossRefPubMedPubMedCentral
34.
go back to reference Reis-Filho JS, Simpson PT, Turner NC, Lambros MB, Jones C, Mackay A, et al. FGFR1 emerges as a potential therapeutic target for lobular breast carcinomas. Clin Cancer Res. 2006;12:6652–62.CrossRefPubMed Reis-Filho JS, Simpson PT, Turner NC, Lambros MB, Jones C, Mackay A, et al. FGFR1 emerges as a potential therapeutic target for lobular breast carcinomas. Clin Cancer Res. 2006;12:6652–62.CrossRefPubMed
35.
go back to reference Hollestelle A, Nagel JH, Smid M, Lam S, Elstrodt F, Wasielewski M, et al. Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res Treat. 2010;121:53–64.CrossRefPubMed Hollestelle A, Nagel JH, Smid M, Lam S, Elstrodt F, Wasielewski M, et al. Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res Treat. 2010;121:53–64.CrossRefPubMed
36.
go back to reference Sikora MJ, Cooper KL, Bahreini A, Luthra S, Wang G, Chandran UR, et al. Invasive lobular carcinoma cell lines are characterized by unique estrogen-mediated gene expression patterns and altered tamoxifen response. Cancer Res. 2014;74:1463–74.CrossRefPubMedPubMedCentral Sikora MJ, Cooper KL, Bahreini A, Luthra S, Wang G, Chandran UR, et al. Invasive lobular carcinoma cell lines are characterized by unique estrogen-mediated gene expression patterns and altered tamoxifen response. Cancer Res. 2014;74:1463–74.CrossRefPubMedPubMedCentral
37.
go back to reference Riggins RB, Lan JP, Klimach U, Zwart A, Cavalli LR, Haddad BR, et al. ERRgamma mediates tamoxifen resistance in novel models of invasive lobular breast cancer. Cancer Res. 2008;68:8908–17.CrossRefPubMedPubMedCentral Riggins RB, Lan JP, Klimach U, Zwart A, Cavalli LR, Haddad BR, et al. ERRgamma mediates tamoxifen resistance in novel models of invasive lobular breast cancer. Cancer Res. 2008;68:8908–17.CrossRefPubMedPubMedCentral
38.
go back to reference Turner N, Pearson A, Sharpe R, Lambros M, Geyer F, Lopez-Garcia MA, et al. FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res. 2010;70:2085–94.CrossRefPubMedPubMedCentral Turner N, Pearson A, Sharpe R, Lambros M, Geyer F, Lopez-Garcia MA, et al. FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res. 2010;70:2085–94.CrossRefPubMedPubMedCentral
39.
go back to reference Sircoulomb F, Nicolas N, Ferrari A, Finetti P, Bekhouche I, Rousselet E, et al. ZNF703 gene amplification at 8p12 specifies luminal B breast cancer. EMBO Mol Med. 2011;3:153–66.CrossRefPubMedPubMedCentral Sircoulomb F, Nicolas N, Ferrari A, Finetti P, Bekhouche I, Rousselet E, et al. ZNF703 gene amplification at 8p12 specifies luminal B breast cancer. EMBO Mol Med. 2011;3:153–66.CrossRefPubMedPubMedCentral
40.
go back to reference Zhang X, Mu X, Huang O, Xie Z, Jiang M, Geng M, et al. Luminal breast cancer cell lines overexpressing ZNF703 are resistant to tamoxifen through activation of Akt/mTOR signaling. PLoS One. 2013;8:e72053.CrossRefPubMedPubMedCentral Zhang X, Mu X, Huang O, Xie Z, Jiang M, Geng M, et al. Luminal breast cancer cell lines overexpressing ZNF703 are resistant to tamoxifen through activation of Akt/mTOR signaling. PLoS One. 2013;8:e72053.CrossRefPubMedPubMedCentral
41.
go back to reference Christgen M, Noskowicz M, Heil C, Schipper E, Christgen H, Geffers R, et al. 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. 2012;92:1635–47.CrossRefPubMed Christgen M, Noskowicz M, Heil C, Schipper E, Christgen H, Geffers R, et al. 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. 2012;92:1635–47.CrossRefPubMed
42.
go back to reference Christgen M, Geffers R, Kreipe H, Lehmann U. IPH-926 lobular breast cancer cells are triple-negative but their microarray profile uncovers a luminal subtype. Cancer Sci. 2013;104:1726–30.CrossRefPubMed Christgen M, Geffers R, Kreipe H, Lehmann U. IPH-926 lobular breast cancer cells are triple-negative but their microarray profile uncovers a luminal subtype. Cancer Sci. 2013;104:1726–30.CrossRefPubMed
43.
go back to reference Krech T, Scheuerer E, Geffers R, Kreipe H, Lehmann U, Christgen M. ABCB1/MDR1 contributes to the anticancer drug-resistant phenotype of IPH-926 human lobular breast cancer cells. Cancer Lett. 2012;315:153–60.CrossRefPubMed Krech T, Scheuerer E, Geffers R, Kreipe H, Lehmann U, Christgen M. ABCB1/MDR1 contributes to the anticancer drug-resistant phenotype of IPH-926 human lobular breast cancer cells. Cancer Lett. 2012;315:153–60.CrossRefPubMed
44.
go back to reference Meijer D, van Agthoven T, Bosma PT, Nooter K, Dorssers LC. Functional screen for genes responsible for tamoxifen resistance in human breast cancer cells. Mol Cancer Res. 2006;4:379–86.CrossRefPubMed Meijer D, van Agthoven T, Bosma PT, Nooter K, Dorssers LC. Functional screen for genes responsible for tamoxifen resistance in human breast cancer cells. Mol Cancer Res. 2006;4:379–86.CrossRefPubMed
45.
go back to reference Keimling M, Wiesmuller L. DNA double-strand break repair activities in mammary epithelial cells – influence of endogenous p53 variants. Carcinogenesis. 2009;30:1260–8.CrossRefPubMed Keimling M, Wiesmuller L. DNA double-strand break repair activities in mammary epithelial cells – influence of endogenous p53 variants. Carcinogenesis. 2009;30:1260–8.CrossRefPubMed
46.
go back to reference Hollestelle A, Elstrodt F, Timmermans M, Sieuwerts AM, Klijn JG, Foekens JA, et al. Four human breast cancer cell lines with biallelic inactivating alpha-catenin gene mutations. Breast Cancer Res Treat. 2010;122:125–33.CrossRefPubMed Hollestelle A, Elstrodt F, Timmermans M, Sieuwerts AM, Klijn JG, Foekens JA, et al. Four human breast cancer cell lines with biallelic inactivating alpha-catenin gene mutations. Breast Cancer Res Treat. 2010;122:125–33.CrossRefPubMed
47.
go back to reference DeRose YS, Wang G, Lin YC, Bernard PS, Buys SS, Ebbert MT, et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med. 2011;17:1514–20.CrossRefPubMedPubMedCentral DeRose YS, Wang G, Lin YC, Bernard PS, Buys SS, Ebbert MT, et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med. 2011;17:1514–20.CrossRefPubMedPubMedCentral
48.
go back to reference Marangoni E, Vincent-Salomon A, Auger N, Degeorges A, Assayag F, de Cremoux P, et al. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin Cancer Res. 2007;13:3989–98.CrossRefPubMed Marangoni E, Vincent-Salomon A, Auger N, Degeorges A, Assayag F, de Cremoux P, et al. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin Cancer Res. 2007;13:3989–98.CrossRefPubMed
49.
go back to reference Cottu P, Marangoni E, Assayag F, de Cremoux P, Vincent-Salomon A, Guyader C, et al. Modeling of response to endocrine therapy in a panel of human luminal breast cancer xenografts. Breast Cancer Res Treat. 2012;133:595–606.CrossRefPubMed Cottu P, Marangoni E, Assayag F, de Cremoux P, Vincent-Salomon A, Guyader C, et al. Modeling of response to endocrine therapy in a panel of human luminal breast cancer xenografts. Breast Cancer Res Treat. 2012;133:595–606.CrossRefPubMed
50.
go back to reference Goldschmidt M, Pena L, Rasotto R, Zappulli V. Classification and grading of canine mammary tumors. Vet Pathol. 2011;48:117–31.CrossRefPubMed Goldschmidt M, Pena L, Rasotto R, Zappulli V. Classification and grading of canine mammary tumors. Vet Pathol. 2011;48:117–31.CrossRefPubMed
51.
go back to reference Cardiff RD, Wellings SR. The comparative pathology of human and mouse mammary glands. J Mammary Gland Biol Neoplasia. 1999;4:105–22.CrossRefPubMed Cardiff RD, Wellings SR. The comparative pathology of human and mouse mammary glands. J Mammary Gland Biol Neoplasia. 1999;4:105–22.CrossRefPubMed
52.
go back to reference Ressel L, Millanta F, Poli A. Canine invasive lobular carcinoma of the mammary gland: morphological and immunohistochemical characterizations of three cases. J Comp Pathol. 2011;144:303–7.CrossRefPubMed Ressel L, Millanta F, Poli A. Canine invasive lobular carcinoma of the mammary gland: morphological and immunohistochemical characterizations of three cases. J Comp Pathol. 2011;144:303–7.CrossRefPubMed
53.
go back to reference Wood CE, Usborne AL, Starost MF, Tarara RP, Hill LR, Wilkinson LM, et al. Hyperplastic and neoplastic lesions of the mammary gland in macaques. Vet Pathol. 2006;43:471–83.CrossRefPubMed Wood CE, Usborne AL, Starost MF, Tarara RP, Hill LR, Wilkinson LM, et al. Hyperplastic and neoplastic lesions of the mammary gland in macaques. Vet Pathol. 2006;43:471–83.CrossRefPubMed
54.
go back to reference Jonkers J, Derksen PW. Modeling metastatic breast cancer in mice. J Mammary Gland Biol Neoplasia. 2007;12:191–203.CrossRefPubMed Jonkers J, Derksen PW. Modeling metastatic breast cancer in mice. J Mammary Gland Biol Neoplasia. 2007;12:191–203.CrossRefPubMed
55.
go back to reference Riethmacher D, Brinkmann V, Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci U S A. 1995;92:855–9.CrossRefPubMedPubMedCentral Riethmacher D, Brinkmann V, Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci U S A. 1995;92:855–9.CrossRefPubMedPubMedCentral
56.
go back to reference Redmer T, Diecke S, Grigoryan T, Quiroga-Negreira A, Birchmeier W, Besser D. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep. 2011;12:720–6.CrossRefPubMedPubMedCentral Redmer T, Diecke S, Grigoryan T, Quiroga-Negreira A, Birchmeier W, Besser D. E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming. EMBO Rep. 2011;12:720–6.CrossRefPubMedPubMedCentral
57.
go back to reference Humar B, Blair V, Charlton A, More H, Martin I, Guilford P. E-cadherin deficiency initiates gastric signet-ring cell carcinoma in mice and man. Cancer Res. 2009;69:2050–6.CrossRefPubMed Humar B, Blair V, Charlton A, More H, Martin I, Guilford P. E-cadherin deficiency initiates gastric signet-ring cell carcinoma in mice and man. Cancer Res. 2009;69:2050–6.CrossRefPubMed
58.
go back to reference Gu H, Zou YR, Rajewsky K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell. 1993;73:1155–64.CrossRefPubMed Gu H, Zou YR, Rajewsky K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell. 1993;73:1155–64.CrossRefPubMed
59.
go back to reference Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R. E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev. 2002;115:53–62.CrossRefPubMed Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R. E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev. 2002;115:53–62.CrossRefPubMed
60.
go back to reference Tinkle CL, Lechler T, Pasolli HA, Fuchs E. Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci U S A. 2004;101:552–7.CrossRefPubMedPubMedCentral Tinkle CL, Lechler T, Pasolli HA, Fuchs E. Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci U S A. 2004;101:552–7.CrossRefPubMedPubMedCentral
61.
go back to reference Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell. 2006;10:437–49.CrossRefPubMed Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell. 2006;10:437–49.CrossRefPubMed
62.
go back to reference Kotb AM, Hierholzer A, Kemler R. Replacement of E-cadherin by N-cadherin in the mammary gland leads to fibrocystic changes and tumor formation. Breast Cancer Res. 2011;13:R104.CrossRefPubMedPubMedCentral Kotb AM, Hierholzer A, Kemler R. Replacement of E-cadherin by N-cadherin in the mammary gland leads to fibrocystic changes and tumor formation. Breast Cancer Res. 2011;13:R104.CrossRefPubMedPubMedCentral
63.
go back to reference Derksen PW, Braumuller TM, van der Burg E, Hornsveld M, Mesman E, Wesseling J, et al. Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice. Dis Model Mech. 2011;4:347–58.CrossRefPubMedPubMedCentral Derksen PW, Braumuller TM, van der Burg E, Hornsveld M, Mesman E, Wesseling J, et al. Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice. Dis Model Mech. 2011;4:347–58.CrossRefPubMedPubMedCentral
64.
go back to reference Mimata A, Fukamachi H, Eishi Y, Yuasa Y. Loss of E-cadherin in mouse gastric epithelial cells induces signet ring-like cells, a possible precursor lesion of diffuse gastric cancer. Cancer Sci. 2011;102:942–50.CrossRefPubMed Mimata A, Fukamachi H, Eishi Y, Yuasa Y. Loss of E-cadherin in mouse gastric epithelial cells induces signet ring-like cells, a possible precursor lesion of diffuse gastric cancer. Cancer Sci. 2011;102:942–50.CrossRefPubMed
65.
go back to reference Shimada S, Mimata A, Sekine M, Mogushi K, Akiyama Y, Fukamachi H, et al. Synergistic tumour suppressor activity of E-cadherin and p53 in a conditional mouse model for metastatic diffuse-type gastric cancer. Gut. 2012;61:344–53.CrossRefPubMed Shimada S, Mimata A, Sekine M, Mogushi K, Akiyama Y, Fukamachi H, et al. Synergistic tumour suppressor activity of E-cadherin and p53 in a conditional mouse model for metastatic diffuse-type gastric cancer. Gut. 2012;61:344–53.CrossRefPubMed
66.
go back to reference Park JW, Jang SH, Park DM, Lim NJ, Deng C, Kim DY, et al. Cooperativity of E-cadherin and Smad4 loss to promote diffuse-type gastric adenocarcinoma and metastasis. Mol Cancer Res. 2014;12:1088–99.CrossRefPubMedPubMedCentral Park JW, Jang SH, Park DM, Lim NJ, Deng C, Kim DY, et al. Cooperativity of E-cadherin and Smad4 loss to promote diffuse-type gastric adenocarcinoma and metastasis. Mol Cancer Res. 2014;12:1088–99.CrossRefPubMedPubMedCentral
67.
go back to reference Doornebal CW, Klarenbeek S, Braumuller TM, Klijn CN, Ciampricotti M, Hau CS, et al. A preclinical mouse model of invasive lobular breast cancer metastasis. Cancer Res. 2013;73:353–63.CrossRefPubMed Doornebal CW, Klarenbeek S, Braumuller TM, Klijn CN, Ciampricotti M, Hau CS, et al. A preclinical mouse model of invasive lobular breast cancer metastasis. Cancer Res. 2013;73:353–63.CrossRefPubMed
68.
go back to reference Tubiana-Hulin M, Stevens D, Lasry S, Guinebretiere JM, Bouita L, Cohen-Solal C, et al. Response to neoadjuvant chemotherapy in lobular and ductal breast carcinomas: a retrospective study on 860 patients from one institution. Ann Oncol. 2006;17:1228–33.CrossRefPubMed Tubiana-Hulin M, Stevens D, Lasry S, Guinebretiere JM, Bouita L, Cohen-Solal C, et al. Response to neoadjuvant chemotherapy in lobular and ductal breast carcinomas: a retrospective study on 860 patients from one institution. Ann Oncol. 2006;17:1228–33.CrossRefPubMed
69.
go back to reference Daniel JM, Reynolds AB. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol Cell Biol. 1999;19:3614–23.CrossRefPubMedPubMedCentral Daniel JM, Reynolds AB. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol Cell Biol. 1999;19:3614–23.CrossRefPubMedPubMedCentral
70.
go back to reference Vermeulen JF, van de Ven RA, Ercan C, van der Groep P, van der Wall E, Bult P, et al. Nuclear Kaiso expression is associated with high grade and triple-negative invasive breast cancer. PLoS One. 2012;7:e37864.CrossRefPubMedPubMedCentral Vermeulen JF, van de Ven RA, Ercan C, van der Groep P, van der Wall E, Bult P, et al. Nuclear Kaiso expression is associated with high grade and triple-negative invasive breast cancer. PLoS One. 2012;7:e37864.CrossRefPubMedPubMedCentral
71.
go back to reference Schackmann RC, Klarenbeek S, Vlug EJ, Stelloo S, van Amersfoort M, Tenhagen M, et al. Loss of p120-catenin induces metastatic progression of breast cancer by inducing anoikis resistance and augmenting growth factor receptor signaling. Cancer Res. 2013;73:4937–49.CrossRefPubMed Schackmann RC, Klarenbeek S, Vlug EJ, Stelloo S, van Amersfoort M, Tenhagen M, et al. Loss of p120-catenin induces metastatic progression of breast cancer by inducing anoikis resistance and augmenting growth factor receptor signaling. Cancer Res. 2013;73:4937–49.CrossRefPubMed
72.
go back to reference Arthur LM, Turnbull AK, Webber VL, Larionov AA, Renshaw L, Kay C, et al. Molecular changes in lobular breast cancers in response to endocrine therapy. Cancer Res. 2014;74:5371–6.CrossRefPubMed Arthur LM, Turnbull AK, Webber VL, Larionov AA, Renshaw L, Kay C, et al. Molecular changes in lobular breast cancers in response to endocrine therapy. Cancer Res. 2014;74:5371–6.CrossRefPubMed
73.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
Metadata
Title
Lobular breast cancer: molecular basis, mouse and cellular models
Authors
Matthias Christgen
Patrick WB Derksen
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 1/2015
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-015-0517-z

Other articles of this Issue 1/2015

Breast Cancer Research 1/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

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

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