A new role of SNAI2 in postlactational involution of the mammary gland links it to luminal breast cancer development
Abstract
Breast cancer is a major cause of mortality in women. The transcription factor SNAI2 has been implicated in the pathogenesis of several types of cancer, including breast cancer of basal origin. Here we show that SNAI2 is also important in the development of breast cancer of luminal origin in MMTV-ErbB2 mice. SNAI2 deficiency leads to longer latency and fewer luminal tumors, both of these being characteristics of pretumoral origin. These effects were associated with reduced proliferation and a decreased ability to generate mammospheres in normal mammary glands. However, the capacity to metastasize was not modified. Under conditions of increased ERBB2 oncogenic activity after pregnancy plus SNAI2 deficiency, both pretumoral defects-latency and tumor load-were compensated. However, the incidence of lung metastases was dramatically reduced. Furthermore, SNAI2 was required for proper postlactational involution of the breast. At 3 days post lactational involution, the mammary glands of Snai2-deficient mice exhibited lower levels of pSTAT3 and higher levels of pAKT1, resulting in decreased apoptosis. Abundant noninvoluted ducts were still present at 30 days post lactation, with a greater number of residual ERBB2+ cells. These results suggest that this defect in involution leads to an increase in the number of susceptible target cells for transformation,more »
- Authors:
-
- Univ. de Salamanca/CSIC, Salamanca (Spain); Hospital Univ. de Salamanca, Salamanca (Spain)
- Univ. de Salamanca, Salamanca (Spain); Hospital Univ. de Salamanca, Salamanca (Spain)
- Centro Nacional de Investigaciones Oncologicas (CNIO), Madrid (Spain)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Maine Medical Center Research Institute, Scarborough, ME (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1257855
- Grant/Contract Number:
- AC02-05CH1123
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Oncogene
- Additional Journal Information:
- Journal Volume: 34; Journal Issue: 36; Journal ID: ISSN 0950-9232
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES
Citation Formats
Castillo-Lluva, Sonia, Hontecillas-Prieto, Lourdes, Blanco-Gómez, Adrian, del Mar Sáez-Freire, María, García-Cenador, Begona, García-Criado, Javier, Pérez-Andrés, Martín, Orfao, Alberto, Cañamero, Marta, Mao, Jian-Hua, Gridley, Thomas, Castellanos-Martín, Andres, and Pérez-Losada, Jesus. A new role of SNAI2 in postlactational involution of the mammary gland links it to luminal breast cancer development. United States: N. p., 2015.
Web. doi:10.1038/onc.2015.224.
Castillo-Lluva, Sonia, Hontecillas-Prieto, Lourdes, Blanco-Gómez, Adrian, del Mar Sáez-Freire, María, García-Cenador, Begona, García-Criado, Javier, Pérez-Andrés, Martín, Orfao, Alberto, Cañamero, Marta, Mao, Jian-Hua, Gridley, Thomas, Castellanos-Martín, Andres, & Pérez-Losada, Jesus. A new role of SNAI2 in postlactational involution of the mammary gland links it to luminal breast cancer development. United States. https://doi.org/10.1038/onc.2015.224
Castillo-Lluva, Sonia, Hontecillas-Prieto, Lourdes, Blanco-Gómez, Adrian, del Mar Sáez-Freire, María, García-Cenador, Begona, García-Criado, Javier, Pérez-Andrés, Martín, Orfao, Alberto, Cañamero, Marta, Mao, Jian-Hua, Gridley, Thomas, Castellanos-Martín, Andres, and Pérez-Losada, Jesus. Mon .
"A new role of SNAI2 in postlactational involution of the mammary gland links it to luminal breast cancer development". United States. https://doi.org/10.1038/onc.2015.224. https://www.osti.gov/servlets/purl/1257855.
@article{osti_1257855,
title = {A new role of SNAI2 in postlactational involution of the mammary gland links it to luminal breast cancer development},
author = {Castillo-Lluva, Sonia and Hontecillas-Prieto, Lourdes and Blanco-Gómez, Adrian and del Mar Sáez-Freire, María and García-Cenador, Begona and García-Criado, Javier and Pérez-Andrés, Martín and Orfao, Alberto and Cañamero, Marta and Mao, Jian-Hua and Gridley, Thomas and Castellanos-Martín, Andres and Pérez-Losada, Jesus},
abstractNote = {Breast cancer is a major cause of mortality in women. The transcription factor SNAI2 has been implicated in the pathogenesis of several types of cancer, including breast cancer of basal origin. Here we show that SNAI2 is also important in the development of breast cancer of luminal origin in MMTV-ErbB2 mice. SNAI2 deficiency leads to longer latency and fewer luminal tumors, both of these being characteristics of pretumoral origin. These effects were associated with reduced proliferation and a decreased ability to generate mammospheres in normal mammary glands. However, the capacity to metastasize was not modified. Under conditions of increased ERBB2 oncogenic activity after pregnancy plus SNAI2 deficiency, both pretumoral defects-latency and tumor load-were compensated. However, the incidence of lung metastases was dramatically reduced. Furthermore, SNAI2 was required for proper postlactational involution of the breast. At 3 days post lactational involution, the mammary glands of Snai2-deficient mice exhibited lower levels of pSTAT3 and higher levels of pAKT1, resulting in decreased apoptosis. Abundant noninvoluted ducts were still present at 30 days post lactation, with a greater number of residual ERBB2+ cells. These results suggest that this defect in involution leads to an increase in the number of susceptible target cells for transformation, to the recovery of the capacity to generate mammospheres and to an increase in the number of tumors. In conclusion, our work demonstrates the participation of SNAI2 in the pathogenesis of luminal breast cancer, and reveals an unexpected connection between the processes of postlactational involution and breast tumorigenesis in Snai2-null mutant mice.},
doi = {10.1038/onc.2015.224},
journal = {Oncogene},
number = 36,
volume = 34,
place = {United States},
year = {Mon Jun 22 00:00:00 EDT 2015},
month = {Mon Jun 22 00:00:00 EDT 2015}
}
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Works referenced in this record:
Isolation of mouse mammary epithelial progenitor cells with basal characteristics from the Comma-Dβ cell line
journal, May 2006
- Deugnier, Marie-Ange; Faraldo, Marisa M.; Teulière, Jérôme
- Developmental Biology, Vol. 293, Issue 2
Ultraviolet radiation stimulates expression of Snail family transcription factors in keratinocytes
journal, January 2007
- Hudson, Laurie G.; Choi, Changsun; Newkirk, Kimberly M.
- Molecular Carcinogenesis, Vol. 46, Issue 4
Theoretical and empirical issues for marker-assisted breeding of congenic mouse strains
journal, November 1997
- Markel, Paul; Shu, Pei; Ebeling, Chris
- Nature Genetics, Vol. 17, Issue 3
Stat3-induced apoptosis requires a molecular switch in PI(3)K subunit composition
journal, March 2005
- Abell, Kathrine; Bilancio, Antonio; Clarkson, Richard W. E.
- Nature Cell Biology, Vol. 7, Issue 4
Mammary Gland Involution Is Delayed by Activated Akt in Transgenic Mice
journal, June 2001
- Schwertfeger, Kathryn L.; Richert, Monica M.; Anderson, Steven M.
- Molecular Endocrinology, Vol. 15, Issue 6
I B kinase kinase activity is required for self-renewal of ErbB2/Her2-transformed mammary tumor-initiating cells
journal, September 2007
- Cao, Y.; Luo, J. -l.; Karin, M.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 40
Mammary stem cells have myoepithelial cell properties
journal, August 2014
- Prater, Michael D.; Petit, Valérie; Alasdair Russell, I.
- Nature Cell Biology, Vol. 16, Issue 10
Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3
journal, October 1999
- Chapman, R. S.; Lourenco, P. C.; Tonner, E.
- Genes & Development, Vol. 13, Issue 19
The basal-like breast carcinoma phenotype is regulated by SLUG gene expression
journal, January 2008
- Storci, G.; Sansone, P.; Trere, D.
- The Journal of Pathology, Vol. 214, Issue 1
Sca-1pos Cells in the Mouse Mammary Gland Represent an Enriched Progenitor Cell Population
journal, May 2002
- Welm, Bryan E.; Tepera, Stacey B.; Venezia, Teresa
- Developmental Biology, Vol. 245, Issue 1
Akt phosphorylates and activates HSF-1 independent of heat shock, leading to Slug overexpression and epithelial–mesenchymal transition (EMT) of HER2-overexpressing breast cancer cells
journal, January 2014
- Carpenter, R. L.; Paw, I.; Dewhirst, M. W.
- Oncogene, Vol. 34, Issue 5
Suppression of Neu-induced mammary tumor growth in cyclin D1 deficient mice is compensated for by cyclin E
journal, January 2002
- Bowe, Damon B.; Kenney, Nicholas J.; Adereth, Yair
- Oncogene, Vol. 21, Issue 2
The Comparative Pathology of Human and Mouse Mammary Glands
journal, January 1999
- Cardiff, Robert D.; Wellings, Sefton R.
- Journal of Mammary Gland Biology and Neoplasia, Vol. 4, Issue 1, p. 105-122
Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer
journal, May 1989
- Slamon, D.; Godolphin, W.; Jones, L.
- Science, Vol. 244, Issue 4905
A requirement for Nedd9 in luminal progenitor cells prior to mammary tumorigenesis in MMTV-HER2/ErbB2 mice
journal, January 2013
- Little, J. L.; Serzhanova, V.; Izumchenko, E.
- Oncogene, Vol. 33, Issue 4
Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease.
journal, November 1992
- Guy, C. T.; Webster, M. A.; Schaller, M.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 22
Slug Antagonizes p53-Mediated Apoptosis of Hematopoietic Progenitors by Repressing puma
journal, November 2005
- Wu, Wen-Shu; Heinrichs, Stefan; Xu, Dong
- Cell, Vol. 123, Issue 4
A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes
journal, December 2006
- Neve, Richard M.; Chin, Koei; Fridlyand, Jane
- Cancer Cell, Vol. 10, Issue 6
Effects of FVB/NJ and C57Bl/6J strain backgrounds on mammary tumor phenotype in inducible nitric oxide synthase deficient mice
journal, January 2007
- Davie, Sarah A.; Maglione, Jeannie E.; Manner, Cathyryne K.
- Transgenic Research, Vol. 16, Issue 2
Cre-lox-regulated conditional RNA interference from transgenes
journal, July 2004
- Ventura, A.; Meissner, A.; Dillon, C. P.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 28
Mammary Involution and Breast Cancer Risk: Transgenic Models and Clinical Studies
journal, April 2009
- Radisky, Derek C.; Hartmann, Lynn C.
- Journal of Mammary Gland Biology and Neoplasia, Vol. 14, Issue 2
Distinct Biological Roles for the Akt Family in Mammary Tumor Progression: Figure 1.
journal, April 2010
- Dillon, Rachelle L.; Muller, William J.
- Cancer Research, Vol. 70, Issue 11
Ductal growth is impeded in mammary glands of C-neu transgenic mice
journal, December 2000
- Mukherjee, S.; Louie, S. G.; Campbell, M.
- Oncogene, Vol. 19, Issue 52
CD49f and CD61 identify Her2/neu-induced mammary tumor-initiating cells that are potentially derived from luminal progenitors and maintained by the integrin–TGFβ signaling
journal, September 2011
- Lo, P-K; Kanojia, D.; Liu, X.
- Oncogene, Vol. 31, Issue 21
Molecular portraits of human breast tumours
journal, August 2000
- Perou, Charles M.; Sørlie, Therese; Eisen, Michael B.
- Nature, Vol. 406, Issue 6797
ErbB receptor tyrosine kinase/NF- B signaling controls mammosphere formation in human breast cancer
journal, April 2012
- Hinohara, K.; Kobayashi, S.; Kanauchi, H.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 17
A Detailed Mammosphere Assay Protocol for the Quantification of Breast Stem Cell Activity
journal, June 2012
- Shaw, Frances L.; Harrison, Hannah; Spence, Katherine
- Journal of Mammary Gland Biology and Neoplasia, Vol. 17, Issue 2
In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells
journal, May 2003
- Dontu, G.
- Genes & Development, Vol. 17, Issue 10
Unraveling heterogeneous susceptibility and the evolution of breast cancer using a systems biology approach
journal, February 2015
- Castellanos-Martín, Andrés; Castillo-Lluva, Sonia; Sáez-Freire, María del Mar
- Genome Biology, Vol. 16, Issue 1
SLUG in cancer development
journal, February 2005
- Pérez-Mancera, Pedro Antonio; González-Herrero, Inés; Pérez-Caro, María
- Oncogene, Vol. 24, Issue 19
Activation of Akt-1 (PKB-α) Can Accelerate ErbB-2-Mediated Mammary Tumorigenesis but Suppresses Tumor Invasion
journal, May 2004
- Hutchinson, John N.; Jin, Jing; Cardiff, Robert D.
- Cancer Research, Vol. 64, Issue 9
Collective Invasion in Breast Cancer Requires a Conserved Basal Epithelial Program
journal, December 2013
- Cheung, Kevin J.; Gabrielson, Edward; Werb, Zena
- Cell, Vol. 155, Issue 7
Factors controlling the expression of mouse mammary tumour virus
journal, May 1992
- Günzburg, W. H.; Salmons, B.
- Biochemical Journal, Vol. 283, Issue 3
Development of the mammary gland
journal, July 1982
- Knight, C. H.; Peaker, M.
- Reproduction, Vol. 65, Issue 2
A NIK-IKKα Module Expands ErbB2-Induced Tumor-Initiating Cells by Stimulating Nuclear Export of p27/Kip1
journal, May 2013
- Zhang, Weizhou; Tan, Wei; Wu, Xuefeng
- Cancer Cell, Vol. 23, Issue 5
Stem-cell hierarchy in skin cancer
journal, June 2003
- Perez-Losada, Jesus; Balmain, Allan
- Nature Reviews Cancer, Vol. 3, Issue 6
The Tumor Suppressor p53 Regulates Polarity of Self-Renewing Divisions in Mammary Stem Cells
journal, September 2009
- Cicalese, Angelo; Bonizzi, Giuseppina; Pasi, Cristina E.
- Cell, Vol. 138, Issue 6
The Snail genes as inducers of cell movement and survival: implications in development and cancer
journal, July 2005
- Barrallo-Gimeno, A.
- Development, Vol. 132, Issue 14
Remodeling mechanisms of the mammary gland during involution
journal, January 2011
- Watson, Christine J.; Kreuzaler, Peter A.
- The International Journal of Developmental Biology, Vol. 55, Issue 7-8-9
Snail and Slug Play Distinct Roles during Breast Carcinoma Progression
journal, September 2006
- Come, C.; Magnino, F.; Bibeau, F.
- Clinical Cancer Research, Vol. 12, Issue 18
The snail superfamily of zinc-finger transcription factors
journal, March 2002
- Nieto, M. Angela
- Nature Reviews Molecular Cell Biology, Vol. 3, Issue 3
Genetic Predisposition Directs Breast Cancer Phenotype by Dictating Progenitor Cell Fate
journal, February 2011
- Proia, Theresa A.; Keller, Patricia J.; Gupta, Piyush B.
- Cell Stem Cell, Vol. 8, Issue 2
Loss of Snail2 favors skin tumor progression by promoting the recruitment of myeloid progenitors
journal, March 2015
- Villarejo, Ana; Molina-Ortiz, Patricia; Montenegro, Yenny
- Carcinogenesis, Vol. 36, Issue 5
HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion
journal, June 2008
- Korkaya, H.; Paulson, A.; Iovino, F.
- Oncogene, Vol. 27, Issue 47
Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors
journal, January 2007
- Herschkowitz, Jason I.; Simin, Karl; Weigman, Victor J.
- Genome Biology, Vol. 8, Issue 5
Sustained trophism of the mammary gland is sufficient to accelerate and synchronize development of ErbB2/Neu-induced tumors
journal, January 2006
- Landis, M. D.; Seachrist, D. D.; Abdul-Karim, F. W.
- Oncogene, Vol. 25, Issue 23
Cyclin D1 Kinase Activity Is Required for the Self-Renewal of Mammary Stem and Progenitor Cells that Are Targets of MMTV-ErbB2 Tumorigenesis
journal, January 2010
- Jeselsohn, Rinath; Brown, Nelson E.; Arendt, Lisa
- Cancer Cell, Vol. 17, Issue 1
From The Cover: Reconstruction of functionally normal and malignant human breast tissues in mice
journal, March 2004
- Kuperwasser, C.; Chavarria, T.; Wu, M.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 14
Slug Controls Stem/Progenitor Cell Growth Dynamics during Mammary Gland Morphogenesis
journal, December 2012
- Nassour, Mayssa; Idoux-Gillet, Ysia; Selmi, Abdelkader
- PLoS ONE, Vol. 7, Issue 12
Strain-Dependent Susceptibility to Radiation-Induced Mammary Cancer Is a Result of Differences in Epithelial Cell Sensitivity to Transformation
journal, September 1996
- Ullrich, R. L.; Bowles, N. D.; Satterfield, L. C.
- Radiation Research, Vol. 146, Issue 3
Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland
journal, October 2012
- Shehata, Mona; Teschendorff, Andrew; Sharp, Gemma
- Breast Cancer Research, Vol. 14, Issue 5
Function of the Zinc-Finger Transcription Factor SNAI2 in Cancer and Development
journal, December 2007
- Cobaleda, César; Pérez-Caro, María; Vicente-Dueñas, Carolina
- Annual Review of Genetics, Vol. 41, Issue 1
The Epithelial-Mesenchymal Transition Generates Cells with Properties of Stem Cells
journal, May 2008
- Mani, Sendurai A.; Guo, Wenjun; Liao, Mai-Jing
- Cell, Vol. 133, Issue 4
The increasing complexity of the Snail gene superfamily in metazoan evolution
journal, April 2001
- Manzanares, M.
- Trends in Genetics, Vol. 17, Issue 4
Generation of a functional mammary gland from a single stem cell
journal, January 2006
- Shackleton, Mark; Vaillant, François; Simpson, Kaylene J.
- Nature, Vol. 439, Issue 7072
Purification and unique properties of mammary epithelial stem cells
journal, January 2006
- Stingl, John; Eirew, Peter; Ricketson, Ian
- Nature, Vol. 439, Issue 7079
Slug and Sox9 Cooperatively Determine the Mammary Stem Cell State
journal, March 2012
- Guo, Wenjun; Keckesova, Zuzana; Donaher, Joana Liu
- Cell, Vol. 148, Issue 5
Cell-State Transitions Regulated by SLUG Are Critical for Tissue Regeneration and Tumor Initiation
journal, May 2014
- Phillips, Sarah; Prat, Aleix; Sedic, Maja
- Stem Cell Reports, Vol. 2, Issue 5
SLUG, a ces-1-Related Zinc Finger Transcription Factor Gene with Antiapoptotic Activity, Is a Downstream Target of the E2A-HLF Oncoprotein
journal, September 1999
- Inukai, Takeshi; Inoue, Akira; Kurosawa, Hidemitsu
- Molecular Cell, Vol. 4, Issue 3
The slug gene is not essential for mesoderm or neural crest development in mice
journal, June 1998
- Jiang, Rulang; Lan, Yu; Norton, Christine R.
- Developmental Biology, Vol. 198, Issue 2
The Crossroads of Oncogenesis and Metastasis
journal, January 2009
- Sánchez-García, Isidro
- New England Journal of Medicine, Vol. 360, Issue 3
Identification of Tumorsphere- and Tumor-Initiating Cells in HER2/Neu-Induced Mammary Tumors
journal, September 2007
- Liu, J. C.; Deng, T.; Lehal, R. S.
- Cancer Research, Vol. 67, Issue 18
Activation of Stat3 in Primary Tumors from High-Risk Breast Cancer Patients Is Associated with Elevated Levels of Activated Src and Survivin Expression
journal, January 2006
- Diaz, N.
- Clinical Cancer Research, Vol. 12, Issue 1
SLUG-induced Elevation of D1 Cyclin in Breast Cancer Cells through the Inhibition of Its Ubiquitination
journal, November 2010
- Mittal, Mukul K.; Singh, Kshipra; Misra, Smita
- Journal of Biological Chemistry, Vol. 286, Issue 1
ErbB2/Neu-Induced, Cyclin D1-Dependent Transformation Is Accelerated in p27-Haploinsufficient Mammary Epithelial Cells but Impaired in p27-Null Cells
journal, April 2002
- Muraoka, Rebecca S.; Lenferink, Anne E. G.; Law, Brian
- Molecular and Cellular Biology, Vol. 22, Issue 7
Over-expression of erbB-2/neu is paralleled by inhibition of mouse-mammary-epithelial-cell differentiation and developmental apoptosis
journal, February 2000
- Lazar, Hedvika; Baltzer, Anna; Gimmi, Claude
- International Journal of Cancer, Vol. 85, Issue 4
PIK3R3 Induces Epithelial-to-Mesenchymal Transition and Promotes Metastasis in Colorectal Cancer
journal, May 2014
- Wang, G.; Yang, X.; Li, C.
- Molecular Cancer Therapeutics, Vol. 13, Issue 7
Molecular portraits of human breast tumours
text, January 2000
- Cheryl, Williams,; Hilde, Johnsen,; A., Akslen, Lars
- The University of North Carolina at Chapel Hill University Libraries
Cell-State Transitions Regulated by SLUG Are Critical for Tissue Regeneration and Tumor Initiation
text, January 2014
- Ania, Wronski,; Aleix, Prat,; B., Gupta, Piyush
- The University of North Carolina at Chapel Hill University Libraries
Slug and Sox9 cooperatively determine the mammary stem cell state
text, January 2012
- Guo, Wenjun; Keckesova, Zuzana; Donaher, Joana Liu
- Elsevier
The basal-like breast carcinoma phenotype is regulated by SLUG gene expression
journal, January 2008
- Storci, G.; Sansone, P.; Trere, D.
- The Journal of Pathology, Vol. 214, Issue 1
Sca-1pos Cells in the Mouse Mammary Gland Represent an Enriched Progenitor Cell Population
journal, May 2002
- Welm, Bryan E.; Tepera, Stacey B.; Venezia, Teresa
- Developmental Biology, Vol. 245, Issue 1
Mammary Involution and Breast Cancer Risk: Transgenic Models and Clinical Studies
journal, April 2009
- Radisky, Derek C.; Hartmann, Lynn C.
- Journal of Mammary Gland Biology and Neoplasia, Vol. 14, Issue 2
A Detailed Mammosphere Assay Protocol for the Quantification of Breast Stem Cell Activity
journal, June 2012
- Shaw, Frances L.; Harrison, Hannah; Spence, Katherine
- Journal of Mammary Gland Biology and Neoplasia, Vol. 17, Issue 2
A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes
journal, December 2006
- Neve, Richard M.; Chin, Koei; Fridlyand, Jane
- Cancer Cell, Vol. 10, Issue 6
Cyclin D1 Kinase Activity Is Required for the Self-Renewal of Mammary Stem and Progenitor Cells that Are Targets of MMTV-ErbB2 Tumorigenesis
journal, January 2010
- Jeselsohn, Rinath; Brown, Nelson E.; Arendt, Lisa
- Cancer Cell, Vol. 17, Issue 1
Slugging It out: Fine Tuning the p53-PUMA Death Connection
journal, November 2005
- Zilfou, Jack T.; Spector,, Mona S.; Lowe, Scott W.
- Cell, Vol. 123, Issue 4
The Tumor Suppressor p53 Regulates Polarity of Self-Renewing Divisions in Mammary Stem Cells
journal, September 2009
- Cicalese, Angelo; Bonizzi, Giuseppina; Pasi, Cristina E.
- Cell, Vol. 138, Issue 6
Slug and Sox9 Cooperatively Determine the Mammary Stem Cell State
journal, March 2012
- Guo, Wenjun; Keckesova, Zuzana; Donaher, Joana Liu
- Cell, Vol. 148, Issue 5
Isolation of mouse mammary epithelial progenitor cells with basal characteristics from the Comma-Dβ cell line
journal, May 2006
- Deugnier, Marie-Ange; Faraldo, Marisa M.; Teulière, Jérôme
- Developmental Biology, Vol. 293, Issue 2
The increasing complexity of the Snail gene superfamily in metazoan evolution
journal, April 2001
- Manzanares, M.
- Trends in Genetics, Vol. 17, Issue 4
Generation of a functional mammary gland from a single stem cell
journal, January 2006
- Shackleton, Mark; Vaillant, François; Simpson, Kaylene J.
- Nature, Vol. 439, Issue 7072
Purification and unique properties of mammary epithelial stem cells
journal, January 2006
- Stingl, John; Eirew, Peter; Ricketson, Ian
- Nature, Vol. 439, Issue 7079
Stat3-induced apoptosis requires a molecular switch in PI(3)K subunit composition
journal, March 2005
- Abell, Kathrine; Bilancio, Antonio; Clarkson, Richard W. E.
- Nature Cell Biology, Vol. 7, Issue 4
Mammary stem cells have myoepithelial cell properties
journal, August 2014
- Prater, Michael D.; Petit, Valérie; Alasdair Russell, I.
- Nature Cell Biology, Vol. 16, Issue 10
Theoretical and empirical issues for marker-assisted breeding of congenic mouse strains
journal, November 1997
- Markel, Paul; Shu, Pei; Ebeling, Chris
- Nature Genetics, Vol. 17, Issue 3
Stem-cell hierarchy in skin cancer
journal, June 2003
- Perez-Losada, Jesus; Balmain, Allan
- Nature Reviews Cancer, Vol. 3, Issue 6
The snail superfamily of zinc-finger transcription factors
journal, March 2002
- Nieto, M. Angela
- Nature Reviews Molecular Cell Biology, Vol. 3, Issue 3
HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion
journal, June 2008
- Korkaya, H.; Paulson, A.; Iovino, F.
- Oncogene, Vol. 27, Issue 47
A requirement for Nedd9 in luminal progenitor cells prior to mammary tumorigenesis in MMTV-HER2/ErbB2 mice
journal, January 2013
- Little, J. L.; Serzhanova, V.; Izumchenko, E.
- Oncogene, Vol. 33, Issue 4
Ductal growth is impeded in mammary glands of C-neu transgenic mice
journal, December 2000
- Mukherjee, S.; Louie, S. G.; Campbell, M.
- Oncogene, Vol. 19, Issue 52
SLUG in cancer development
journal, February 2005
- Pérez-Mancera, Pedro Antonio; González-Herrero, Inés; Pérez-Caro, María
- Oncogene, Vol. 24, Issue 19
Sustained trophism of the mammary gland is sufficient to accelerate and synchronize development of ErbB2/Neu-induced tumors
journal, January 2006
- Landis, M. D.; Seachrist, D. D.; Abdul-Karim, F. W.
- Oncogene, Vol. 25, Issue 23
Factors controlling the expression of mouse mammary tumour virus
journal, May 1992
- Günzburg, W. H.; Salmons, B.
- Biochemical Journal, Vol. 283, Issue 3
From The Cover: Reconstruction of functionally normal and malignant human breast tissues in mice
journal, March 2004
- Kuperwasser, C.; Chavarria, T.; Wu, M.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 14
I B kinase kinase activity is required for self-renewal of ErbB2/Her2-transformed mammary tumor-initiating cells
journal, September 2007
- Cao, Y.; Luo, J. -l.; Karin, M.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 40
ErbB receptor tyrosine kinase/NF- B signaling controls mammosphere formation in human breast cancer
journal, April 2012
- Hinohara, K.; Kobayashi, S.; Kanauchi, H.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 17
Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease.
journal, November 1992
- Guy, C. T.; Webster, M. A.; Schaller, M.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 22
Loss of Snail2 favors skin tumor progression by promoting the recruitment of myeloid progenitors
journal, March 2015
- Villarejo, Ana; Molina-Ortiz, Patricia; Montenegro, Yenny
- Carcinogenesis, Vol. 36, Issue 5
In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells
journal, May 2003
- Dontu, G.
- Genes & Development, Vol. 17, Issue 10
Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3
journal, October 1999
- Chapman, R. S.; Lourenco, P. C.; Tonner, E.
- Genes & Development, Vol. 13, Issue 19
Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer
journal, May 1989
- Slamon, D.; Godolphin, W.; Jones, L.
- Science, Vol. 244, Issue 4905
Activation of Akt-1 (PKB-α) Can Accelerate ErbB-2-Mediated Mammary Tumorigenesis but Suppresses Tumor Invasion
journal, May 2004
- Hutchinson, John N.; Jin, Jing; Cardiff, Robert D.
- Cancer Research, Vol. 64, Issue 9
Distinct Biological Roles for the Akt Family in Mammary Tumor Progression: Figure 1.
journal, April 2010
- Dillon, Rachelle L.; Muller, William J.
- Cancer Research, Vol. 70, Issue 11
Snail and Slug Play Distinct Roles during Breast Carcinoma Progression
journal, September 2006
- Come, C.; Magnino, F.; Bibeau, F.
- Clinical Cancer Research, Vol. 12, Issue 18
Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland
journal, October 2012
- Shehata, Mona; Teschendorff, Andrew; Sharp, Gemma
- Breast Cancer Research, Vol. 14, Issue 5
Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors
journal, January 2007
- Herschkowitz, Jason I.; Simin, Karl; Weigman, Victor J.
- Genome Biology, Vol. 8, Issue 5
Mammary Gland Involution Is Delayed by Activated Akt in Transgenic Mice
journal, June 2001
- Schwertfeger, Kathryn L.; Richert, Monica M.; Anderson, Steven M.
- Molecular Endocrinology, Vol. 15, Issue 6
The Snail genes as inducers of cell movement and survival: implications in development and cancer
journal, July 2005
- Barrallo-Gimeno, A.
- Development, Vol. 132, Issue 14
Slug Controls Stem/Progenitor Cell Growth Dynamics during Mammary Gland Morphogenesis
journal, December 2012
- Nassour, Mayssa; Idoux-Gillet, Ysia; Selmi, Abdelkader
- PLoS ONE, Vol. 7, Issue 12
Remodeling mechanisms of the mammary gland during involution
journal, January 2011
- Watson, Christine J.; Kreuzaler, Peter A.
- The International Journal of Developmental Biology, Vol. 55, Issue 7-8-9
Development of the mammary gland
journal, July 1982
- Knight, C. H.; Peaker, M.
- Reproduction, Vol. 65, Issue 2
Molecular portraits of human breast tumours
text, January 2000
- Cheryl, Williams,; Hilde, Johnsen,; A., Akslen, Lars
- The University of North Carolina at Chapel Hill University Libraries
EGFR dependent expression of STAT3 (but not STAT1) in breast cancer
journal, December 2001
- Berclaz, Gilles; Altermatt, Hans; Rohrbach, Valeria
- International Journal of Oncology
Predicting genome-wide DNA methylation using methylation marks, genomic position, and DNA regulatory elements
text, January 2013
- Zhang, Weiwei; Spector, Tim D.; Deloukas, Panos
- arXiv
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- Zuo, Dongqing; Zhou, Zifei; Wang, Hongsheng
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journal, February 2019
- Wallace, Taylor R.; Tarullo, Sarah E.; Crump, Lyndsey S.
- Journal of Cancer Metastasis and Treatment, Vol. 2019