Modelling breast cancer: one size does not fit all (original) (raw)

• American Cancer Society. Cancer facts and figures 2007. (American Cancer Society, 2007).
• Ferlay, J. et al. Estimates of the cancer incidence and mortality in Europe in 2006. Ann. Oncol. 18, 581–592 (2007).
  Article CAS PubMed Google Scholar
• Ravdin, P. M. et al. The decrease in breast-cancer incidence in 2003 in the United States. N. Engl. J. Med. 356, 1670–1674 (2007).
  Article CAS PubMed Google Scholar
• Lacroix, M. & Leclercq, G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res. Treat. 83, 249–289 (2004).
  Article CAS PubMed Google Scholar
• Hahn, W. C. & Weinberg, R. A. Rules for making human tumor cells. N. Engl. J. Med. 347, 1593–1603 (2002).
  Article CAS PubMed Google Scholar
• Rangarajan, A., Hong, S. J., Gifford, A. & Weinberg, R. A. Species- and cell type-specific requirements for cellular transformation. Cancer Cell 6, 171–183 (2004).
  Article CAS PubMed Google Scholar
• Rangarajan, A. & Weinberg, R. A. Comparative biology of mouse versus human cells: modelling human cancer in mice. Nature Rev. Cancer 3, 952–959 (2003).
  Article CAS Google Scholar
• Nandi, S., Guzman, R. C. & Yang, J. Hormones and mammary carcinogenesis in mice, rats, and humans: a unifying hypothesis. Proc. Natl Acad. Sci. USA 92, 3650–3657 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Burdall, S. E., Hanby, A. M., Lansdown, M. R. & Speirs, V. Breast cancer cell lines: friend or foe? Breast Cancer Res. 5, 89–95 (2003).
  Article PubMed PubMed Central Google Scholar
• Perou, C. M. et al. Molecular portraits of human breast tumours. Nature 406, 747–752 (2000). This seminal molecular profiling study of human breast cancers identified five distinct subtypes of ductal carcinoma.
  Article CAS PubMed Google Scholar
• Ross, D. T. et al. Systematic variation in gene expression patterns in human cancer cell lines. Nature Genet. 24, 227–235 (2000).
  Article CAS PubMed Google Scholar
• Charafe-Jauffret, E. et al. Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 25, 2273–2284 (2006).
  Article CAS PubMed Google Scholar
• Neve, R. M. et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515–527 (2006). This comprehensive study, which compares the molecular profiles and genomic alterations of 51 breast cancer cell lines and human breast tumours, highlights the similarities and differences between cell lines and primary tumours and suggests that when subtype cell lines are used as a system they provide powerful models for investigating breast cancer.
  Article CAS PubMed PubMed Central Google Scholar
• Van't Veer, L. J. & Weigelt, B. Road map to metastasis. Nature Med. 9, 999–1000 (2003).
  Article CAS PubMed Google Scholar
• Weigelt, B., Bosma, A. J., Hart, A. A., Rodenhuis, S. & van 't Veer, L. J. Marker genes for circulating tumour cells predict survival in metastasized breast cancer patients. Br. J. Cancer 88, 1091–1094 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Dontu, G. et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17, 1253–1270 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Villadsen, R. et al. Evidence for a stem cell hierarchy in the adult human breast. J. Cell Biol. 177, 87–101 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983–3988 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Ponti, D. et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65, 5506–5511 (2005).
  Article CAS PubMed Google Scholar
• Polyak, K. Molecular alterations in ductal carcinoma in situ of the breast. Curr. Opin. Oncol. 14, 92–96 (2002).
  Article CAS PubMed Google Scholar
• Reya, T., Morrison, S. J., Clarke, M. F. & Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105–111 (2001).
  Article CAS PubMed Google Scholar
• Wicha, M. S., Liu, S. & Dontu, G. Cancer stem cells: an old idea — a paradigm shift. Cancer Res. 66, 1883–1890; discussion 1895–1886 (2006).
  Article CAS PubMed Google Scholar
• Dalerba, P., Cho, R. W. & Clarke, M. F. Cancer stem cells: models and concepts. Annu. Rev. Med. 58, 267–284 (2007).
  Article CAS PubMed Google Scholar
• Kuperwasser, C. et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl Acad. Sci. USA 101, 4966–4971 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Dontu, G. & Wicha, M. S. Survival of mammary stem cells in suspension culture: implications for stem cell biology and neoplasia. J. Mammary Gland Biol. Neoplasia 10, 75–86 (2005).
  Article PubMed Google Scholar
• Phillips, T. M., McBride, W. H. & Pajonk, F. The response of CD24−/low/CD44+ breast cancer-initiating cells to radiation. J. Natl Cancer Inst. 98, 1777–1785 (2006).
  Article PubMed Google Scholar
• Chen, M. S. et al. Wnt/β-catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line. J. Cell Sci. 120, 468–477 (2007).
  Article CAS PubMed Google Scholar
• Woodward, W. A. et al. WNT/β-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc. Natl Acad. Sci. USA 104, 618–623 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Sheridan, C. et al. CD44+/CD24− breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res. 8, R59 (2006).
  Article PubMed PubMed Central CAS Google Scholar
• Shipitsin, M. et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 11, 259–273 (2007).
  Article CAS PubMed Google Scholar
• Abraham, B. K. et al. Prevalence of CD44+/CD24−/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin. Cancer Res. 11, 1154–1159 (2005).
  CAS PubMed Google Scholar
• Liu, R. et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N. Engl. J. Med. 356, 217–226 (2007).
  Article CAS PubMed Google Scholar
• Armstrong, L. et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 22, 1142–1151 (2004).
  Article PubMed Google Scholar
• Fillmore, C. & Kuperwasser, C. Human breast cancer stem cell markers CD44 and CD24: enriching for cells with functional properties in mice or in man? Breast Cancer Res. 9, 303 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Ross, D. T. & Perou, C. M. A comparison of gene expression signatures from breast tumors and breast tissue derived cell lines. Dis. Markers 17, 99–109 (2001).
  Article CAS PubMed Google Scholar
• Kenny, P. A. et al. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol. Oncol. 1, 84–96 (2007). This study compares gene expression, genomic alterations and morphologies of 27 breast cancer cell lines cultured in 2D versus 3D conditions, which indicates that 3D cultures more precisely mimic the in vivo environment.
  Article CAS PubMed PubMed Central Google Scholar
• Li, C. et al. Cell type and culture condition-dependent alternative splicing in human breast cancer cells revealed by splicing-sensitive microarrays. Cancer Res. 66, 1990–1999 (2006).
  Article CAS PubMed Google Scholar
• Shaw, K. R., Wrobel, C. N. & Brugge, J. S. Use of three-dimensional basement membrane cultures to model oncogene-induced changes in mammary epithelial morphogenesis. J. Mammary Gland Biol. Neoplasia 9, 297–310 (2004).
  Article PubMed Google Scholar
• Debnath, J. & Brugge, J. S. Modelling glandular epithelial cancers in three-dimensional cultures. Nature Rev. Cancer 5, 675–688 (2005).
  Article CAS Google Scholar
• Paszek, M. J. & Weaver, V. M. The tension mounts: mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia 9, 325–342 (2004).
  Article PubMed Google Scholar
• Lee, G. Y., Kenny, P. A., Lee, E. H. & Bissell, M. J. Three-dimensional culture models of normal and malignant breast epithelial cells. Nature Methods 4, 359–365 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241–254 (2005).
  Article CAS PubMed Google Scholar
• Chan, S. K., Hill, M. E. & Gullick, W. J. The role of the epidermal growth factor receptor in breast cancer. J. Mammary Gland Biol. Neoplasia 11, 3–11 (2006).
  Article PubMed Google Scholar
• van Golen, K. L. Inflammatory breast cancer: relationship between growth factor signaling and motility in aggressive cancers. Breast Cancer Res. 5, 174–179 (2003).
  Article PubMed PubMed Central Google Scholar
• Dillon, R. L., White, D. E. & Muller, W. J. The phosphatidyl inositol 3-kinase signaling network: implications for human breast cancer. Oncogene 26, 1338–1345 (2007).
  Article CAS PubMed Google Scholar
• Kenny, P. A. & Bissell, M. J. Targeting TACE-dependent EGFR ligand shedding in breast cancer. J. Clin. Invest. 117, 337–345 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Joyce, J. A. Therapeutic targeting of the tumor microenvironment. Cancer Cell 7, 513–520 (2005).
  Article CAS PubMed Google Scholar
• Albini, A. & Sporn, M. B. The tumour microenvironment as a target for chemoprevention. Nature Rev. Cancer 7, 139–147 (2007).
  Article CAS Google Scholar
• Fukino, K., Shen, L., Patocs, A., Mutter, G. L. & Eng, C. Genomic instability within tumor stroma and clinicopathological characteristics of sporadic primary invasive breast carcinoma. JAMA 297, 2103–2111 (2007).
  Article CAS PubMed Google Scholar
• Pukrop, T. et al. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc. Natl Acad. Sci. USA 103, 5454–5459 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Hagemann, T. et al. Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-α dependent up-regulation of matrix metalloproteases. Carcinogenesis 25, 1543–1549 (2004).
  Article CAS PubMed Google Scholar
• Goswami, S. et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 65, 5278–5283 (2005).
  Article CAS PubMed Google Scholar
• Tsutsui, S. et al. Macrophage infiltration and its prognostic implications in breast cancer: the relationship with VEGF expression and microvessel density. Oncol. Rep. 14, 425–431 (2005).
  CAS PubMed Google Scholar
• Leek, R. D., Landers, R. J., Harris, A. L. & Lewis, C. E. Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Br. J. Cancer 79, 991–995 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Lin, E. Y. et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66, 11238–11246 (2006).
  Article CAS PubMed Google Scholar
• Heppner, G. H., Miller, F. R. & Shekhar, P. M. Nontransgenic models of breast cancer. Breast Cancer Res. 2, 331–334 (2000).
  Article CAS PubMed Google Scholar
• Balkwill, F., Charles, K. A. & Mantovani, A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7, 211–217 (2005).
  Article CAS PubMed Google Scholar
• Schwertfeger, K. L., Rosen, J. M. & Cohen, D. A. Mammary gland macrophages: pleiotropic functions in mammary development. J. Mammary Gland Biol. Neoplasia 11, 229–238 (2006).
  Article PubMed Google Scholar
• Hovey, R. C., McFadden, T. B. & Akers, R. M. Regulation of mammary gland growth and morphogenesis by the mammary fat pad: a species comparison. J. Mammary Gland Biol. Neoplasia 4, 53–68 (1999).
  Article CAS PubMed Google Scholar
• Weigelt, B., Peterse, J. L. & van 't Veer, L. J. Breast cancer metastasis: markers and models. Nature Rev. Cancer 5, 591–602 (2005).
  Article CAS Google Scholar
• Minn, A. J. et al. Genes that mediate breast cancer metastasis to lung. Nature 436, 518–524 (2005). A breast cancer cell line xenograft metastasis model was used to identify a metastasis gene signature that could identify patients who would develop metastatic disease.
  Article CAS PubMed PubMed Central Google Scholar
• Kluger, H. M. et al. Using a xenograft model of human breast cancer metastasis to find genes associated with clinically aggressive disease. Cancer Res. 65, 5578–5587 (2005).
  Article CAS PubMed Google Scholar
• Montel, V., Huang, T. Y., Mose, E., Pestonjamasp, K. & Tarin, D. Expression profiling of primary tumors and matched lymphatic and lung metastases in a xenogeneic breast cancer model. Am. J. Pathol. 166, 1565–1579 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Liu, S. et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66, 6063–6071 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Prendergast, G. C. & Jaffee, E. M. Cancer immunologists and cancer biologists: why we didn't talk then but need to now. Cancer Res. 67, 3500–3504 (2007).
  Article CAS PubMed Google Scholar
• Voskoglou-Nomikos, T., Pater, J. L. & Seymour, L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin. Cancer Res. 9, 4227–4239 (2003).
  PubMed Google Scholar
• Shoemaker, R. H. The NCI60 human tumour cell line anticancer drug screen. Nature Rev. Cancer 6, 813–823 (2006).
  Article CAS Google Scholar
• Johnson, J. I. et al. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer 84, 1424–1431 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Sharpless, N. E. & Depinho, R. A. The mighty mouse: genetically engineered mouse models in cancer drug development. Nature Rev. Drug Discov. 5, 741–754 (2006).
  Article CAS Google Scholar
• Proia, D. A. & Kuperwasser, C. Reconstruction of human mammary tissues in a mouse model. Nature Protoc. 1, 206–214 (2006).
  Article CAS Google Scholar
• Orimo, A. et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121, 335–348 (2005).
  Article CAS PubMed Google Scholar
• MacDonald, I. C. & Chambers, A. F. Breast cancer metastasis progression as revealed by intravital videomicroscopy. Expert Rev. Anticancer Ther. 6, 1271–1279 (2006).
  Article PubMed Google Scholar
• Wyckoff, J. B. et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 67, 2649–2656 (2007).
  Article CAS PubMed Google Scholar
• Varticovski, L. et al. Accelerated preclinical testing using transplanted tumors from genetically engineered mouse breast cancer models. Clin. Cancer Res. 13, 2168–2177 (2007).
  Article CAS PubMed Google Scholar
• Guy, C. T., Cardiff, R. D. & Muller, W. J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954–961 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Guy, C. T. et al. Expression of the Neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl Acad. Sci. USA 89, 10578–10582 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Muller, W. J., Sinn, E., Pattengale, P. K., Wallace, R. & Leder, P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-Neu oncogene. Cell 54, 105–115 (1988).
  Article CAS PubMed Google Scholar
• Sinn, E. et al. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 49, 465–475 (1987).
  Article CAS PubMed Google Scholar
• Gunther, E. J. et al. A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology. FASEB J. 16, 283–292 (2002).
  Article CAS PubMed Google Scholar
• Wagner, K. U. et al. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res. 10, 545–553 (2001).
  Article CAS PubMed Google Scholar
• Wagner, K. U. et al. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res. 25, 4323–4330 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Jonkers, J. et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nature Genet. 29, 418–425 (2001).
  Article CAS PubMed Google Scholar
• Lin, S. C. et al. Somatic mutation of p53 leads to estrogen receptor α-positive and -negative mouse mammary tumors with high frequency of metastasis. Cancer Res. 64, 3525–3532 (2004).
  Article CAS PubMed Google Scholar
• Utomo, A. R., Nikitin, A. Y. & Lee, W. H. Temporal, spatial, and cell type-specific control of Cre-mediated DNA recombination in transgenic mice. Nature Biotech. 17, 1091–1096 (1999).
  Article CAS Google Scholar
• Loonstra, A. et al. Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc. Natl Acad. Sci. USA 98, 9209–9214 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Soyal, S. M. et al. Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 41, 58–66 (2005).
  Article CAS PubMed Google Scholar
• Mukherjee, A. et al. Targeting iCre expression to murine progesterone receptor cell-lineages using bacterial artificial chromosome transgenesis. Genesis 44, 601–610 (2006).
  Article CAS PubMed Google Scholar
• Du, Z. et al. Introduction of oncogenes into mammary glands in vivo with an avian retroviral vector initiates and promotes carcinogenesis in mouse models. Proc. Natl Acad. Sci. USA 103, 17396–17401 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Cardiff, R. D. et al. The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 19, 968–988 (2000). This is a seminal report on the comparative pathology and biology of mammary tumours from GEM and human breast cancers.
  Article CAS PubMed Google Scholar
• Russo, J. & Russo, I. H. Atlas and histologic classification of tumors of the rat mammary gland. J. Mammary Gland Biol. Neoplasia 5, 187–200 (2000).
  Article CAS PubMed Google Scholar
• Gunther, E. J. et al. Impact of p53 loss on reversal and recurrence of conditional Wnt-induced tumorigenesis. Genes Dev. 17, 488–501 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Desai, K. V. et al. Initiating oncogenic event determines gene-expression patterns of human breast cancer models. Proc. Natl Acad. Sci. USA 99, 6967–6972 (2002). This molecular profiling study compares six widely used genetically engineered mouse models of breast cancer with each other and with normal mammary glands to identify oncogene-specific and nonspecific pathways that contribute to tumour development and progression.
  Article CAS PubMed PubMed Central Google Scholar
• Moody, S. E. et al. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2, 451–461 (2002).
  Article CAS PubMed Google Scholar
• Boxer, R. B., Jang, J. W., Sintasath, L. & Chodosh, L. A. Lack of sustained regression of c-MYC-induced mammary adenocarcinomas following brief or prolonged MYC inactivation. Cancer Cell 6, 577–586 (2004).
  Article CAS PubMed Google Scholar
• Derksen, P. W. 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 10, 437–449 (2006).
  Article CAS PubMed Google Scholar
• Andrechek, E. R. et al. Amplification of the Neu/ErbB-2 oncogene in a mouse model of mammary tumorigenesis. Proc. Natl Acad. Sci. USA 97, 3444–3449 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Slamon, D. J. et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/Neu oncogene. Science 235, 177–182 (1987).
  Article CAS PubMed Google Scholar
• Elledge, R. M. & Allred, D. C. Prognostic and predictive value of p53 and p21 in breast cancer. Breast Cancer Res. Treat. 52, 79–98 (1998).
  Article CAS PubMed Google Scholar
• Hu, Y. et al. From mice to humans: identification of commonly deregulated genes in mammary cancer via comparative SAGE studies. Cancer Res. 64, 7748–7755 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Bouchard, L., Lamarre, L., Tremblay, P. J. & Jolicoeur, P. Stochastic appearance of mammary tumors in transgenic mice carrying the MMTV/c-Neu oncogene. Cell 57, 931–936 (1989).
  Article CAS PubMed Google Scholar
• Ursini-Siegel, J., Schade, B., Cardiff, R. D. & Muller, W. J. Insights from transgenic mouse models of ERBB2-induced breast cancer. Nature Rev. Cancer 7, 389–397 (2007).
  Article CAS Google Scholar
• Siegel, P. M., Dankort, D. L., Hardy, W. R. & Muller, W. J. Novel activating mutations in the Neu proto-oncogene involved in induction of mammary tumors. Mol. Cell. Biol. 14, 7068–7077 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Montagna, C., Andrechek, E. R., Padilla-Nash, H., Muller, W. J. & Ried, T. Centrosome abnormalities, recurring deletions of chromosome 4, and genomic amplification of HER2/Neu define mouse mammary gland adenocarcinomas induced by mutant HER2/Neu. Oncogene 21, 890–898 (2002).
  Article CAS PubMed Google Scholar
• Hodgson, J. G. et al. Copy number aberrations in mouse breast tumors reveal loci and genes important in tumorigenic receptor tyrosine kinase signaling. Cancer Res. 65, 9695–9704 (2005).
  Article CAS PubMed Google Scholar
• Andrechek, E. R. et al. Gene expression profiling of _Neu_-induced mammary tumors from transgenic mice reveals genetic and morphological similarities to _ErbB2_-expressing human breast cancers. Cancer Res. 63, 4920–4926 (2003).
  CAS PubMed Google Scholar
• Slamon, D. J. et al. Studies of the HER-2/Neu proto-oncogene in human breast and ovarian cancer. Science 244, 707–712 (1989).
  Article CAS PubMed Google Scholar
• Herschkowitz, J. I. et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 8, R76 (2007). This molecular profiling study compares 13 widely used genetically engineered mouse models of breast cancer with human breast cancers to provide a framework for comparing GEM and human breast cancer.
  Article PubMed PubMed Central CAS Google Scholar
• Li, Y. et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc. Natl Acad. Sci. USA 100, 15853–15858 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Gestl, S. A., Leonard, T. L., Biddle, J. L., Debies, M. T. & Gunther, E. J. Dormant Wnt-initiated mammary cancer can participate in reconstituting functional mammary glands. Mol. Cell. Biol. 27, 195–207 (2007).
  Article CAS PubMed Google Scholar
• Welm, A. L. et al. The macrophage-stimulating protein pathway promotes metastasis in a mouse model for breast cancer and predicts poor prognosis in humans. Proc. Natl Acad. Sci. USA 104, 7570–7575 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Kuperwasser, C. et al. A mouse model of human breast cancer metastasis to human bone. Cancer Res. 65, 6130–6138 (2005).
  Article CAS PubMed Google Scholar
• Westbrook, T. F. et al. A genetic screen for candidate tumor suppressors identifies REST. Cell 121, 837–848 (2005).
  Article CAS PubMed Google Scholar
• Dobie, K. W. et al. Variegated transgene expression in mouse mammary gland is determined by the transgene integration locus. Proc. Natl Acad. Sci. USA 93, 6659–6664 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Choi, Y. W., Henrard, D., Lee, I. & Ross, S. R. The mouse mammary tumor virus long terminal repeat directs expression in epithelial and lymphoid cells of different tissues in transgenic mice. J. Virol. 61, 3013–3019 (1987).
  CAS PubMed PubMed Central Google Scholar
• Henrard, D. & Ross, S. R. Endogenous mouse mammary tumor virus is expressed in several organs in addition to the lactating mammary gland. J. Virol. 62, 3046–3049 (1988).
  CAS PubMed PubMed Central Google Scholar
• Wen, J., Kawamata, Y., Tojo, H., Tanaka, S. & Tachi, C. Expression of whey acidic protein (WAP) genes in tissues other than the mammary gland in normal and transgenic mice expressing mWAP/hGH fusion gene. Mol. Reprod. Dev. 41, 399–406 (1995).
  Article CAS PubMed Google Scholar
• Cardiff, R. D. Validity of mouse mammary tumour models for human breast cancer: comparative pathology. Microsc. Res. Tech. 52, 224–230 (2001).
  Article CAS PubMed Google Scholar
• Wagner, K. U. Models of breast cancer: quo vadis, animal modeling? Breast Cancer Res. 6, 31–38 (2004).
  Article CAS PubMed Google Scholar
• Davis, M. A. & Reynolds, A. B. Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev. Cell 10, 21–31 (2006).
  Article CAS PubMed Google Scholar
• Huggins, C., Grand, L. C. & Brillantes, F. P. Mammary cancer induced by a single feeding of polymucular hydrocarbons, and its suppression. Nature 189, 204–207 (1961).
  Article CAS PubMed Google Scholar
• Russo, I. H. & Russo, J. Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenz[a]anthracene. J. Natl Cancer Inst. 61, 1439–1449 (1978).
  CAS PubMed Google Scholar
• Thompson, H. J., Adlakha, H. & Singh, M. Effect of carcinogen dose and age at administration on induction of mammary carcinogenesis by 1-methyl-1-nitrosourea. Carcinogenesis 13, 1535–1539 (1992).
  Article CAS PubMed Google Scholar
• Thompson, H. J. & Meeker, L. D. Induction of mammary gland carcinomas by the subcutaneous injection of 1-methyl-1-nitrosourea. Cancer Res. 43, 1628–1629 (1983).
  CAS PubMed Google Scholar
• Russo, J. et al. Molecular basis of pregnancy-induced breast cancer protection. Eur. J. Cancer Prev. 15, 306–342 (2006).
  Article CAS PubMed Google Scholar
• Russo, J. et al. The genomic signature of breast cancer prevention. Recent Results Cancer Res. 174, 131–150 (2007).
  Article CAS PubMed Google Scholar
• Blakely, C. M. et al. Hormone-induced protection against mammary tumorigenesis is conserved in multiple rat strains and identifies a core gene expression signature induced by pregnancy. Cancer Res. 66, 6421–6431 (2006).
  Article CAS PubMed Google Scholar
• Russo, J. et al. Comparative study of human and rat mammary tumorigenesis. Lab. Invest. 62, 244–278 (1990).
  CAS PubMed Google Scholar
• Zan, Y. et al. Production of knockout rats using ENU mutagenesis and a yeast-based screening assay. Nature Biotech. 21, 645–651 (2003).
  Article CAS Google Scholar
• Nguyen, D. X. & Massague, J. Genetic determinants of cancer metastasis. Nature Rev. Genet. 8, 341–352 (2007).
  Article CAS PubMed Google Scholar
• Tan, B. T., Park, C. Y., Ailles, L. E. & Weissman, I. L. The cancer stem cell hypothesis: a work in progress. Lab. Invest. 86, 1203–1207 (2006).
  Article CAS PubMed Google Scholar
• Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869–10874 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Sorlie, T. et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 100, 8418–8423 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Zhao, H. et al. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol. Biol. Cell 15, 2523–2536 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Carey, L. A. et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin. Cancer Res. 13, 2329–2334 (2007).
  Article CAS PubMed Google Scholar
• Al-Hajj, M., Becker, M. W., Wicha, M., Weissman, I. & Clarke, M. F. Therapeutic implications of cancer stem cells. Curr. Opin. Genet. Dev. 14, 43–47 (2004).
  Article CAS PubMed Google Scholar
• Bissell, M. J., Radisky, D. C., Rizki, A., Weaver, V. M. & Petersen, O. W. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 70, 537–546 (2002).
  Article PubMed PubMed Central Google Scholar
• Bissell, M. J. & Labarge, M. A. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 7, 17–23 (2005).
  CAS PubMed PubMed Central Google Scholar
• Bissell, M. J., Rizki, A. & Mian, I. S. Tissue architecture: the ultimate regulator of breast epithelial function. Curr. Opin. Cell Biol. 15, 753–762 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Debnath, J., Muthuswamy, S. K. & Brugge, J. S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256–268 (2003).
  Article CAS PubMed Google Scholar
• MacDonald, I. C., Groom, A. C. & Chambers, A. F. Cancer spread and micrometastasis development: quantitative approaches for in vivo models. Bioessays 24, 885–893 (2002).
  Article CAS PubMed Google Scholar
• Wyckoff, J. B., Jones, J. G., Condeelis, J. S. & Segall, J. E. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 60, 2504–2511 (2000).
  CAS PubMed Google Scholar
• Chambers, A. F., Naumov, G. N., Vantyghem, S. A. & Tuck, A. B. Molecular biology of breast cancer metastasis. Clinical implications of experimental studies on metastatic inefficiency. Breast Cancer Res. 2, 400–407 (2000).
  Article CAS PubMed PubMed Central Google Scholar