Prospective isolation and functional analysis of stem and differentiated cells from the mouse mammary gland

Stem Cell Reviews

Volumn 3, Issue 2, 2007, Pages 124-136

  Regan, Joseph ^a   Smalley, Matthew ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Cancer; CD24; Mammary gland; Side population; Stem cells

Indexed keywords

DIFFERENTIATION ANTIGEN; ESTROGEN RECEPTOR;

ANIMAL; ARTICLE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL SEPARATION; CLONOGENIC ASSAY; CYTOLOGY; EPITHELIUM CELL; EXPERIMENTAL NEOPLASM; FEMALE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; STEM CELL; UDDER;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELL SEPARATION; COLONY-FORMING UNITS ASSAY; EPITHELIAL CELLS; FEMALE; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, ANIMAL; MICE; NEOPLASTIC STEM CELLS; RECEPTORS, ESTROGEN; STEM CELLS;

EID: 36248974147     PISSN: 15508943     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12015-007-0017-3     Document Type: Article

References (104)

1. Reya, T., Morrison, S. J., Clarke, M. F., & Weissman, I. L. (2001). Stem cells, cancer, and cancer stem cells. Nature, 414 (6859), 105-111, Nov 1.
2. Sell, S. (2004). Stem cell origin of cancer and differentiation therapy. Critical Reviews in Oncology/Hematology, 51(1), 1-28, Jul.
3. Singh, S. K., Clarke, I. D., Hide, T., & Dirks, P. B. (2004). Cancer stem cells in nervous system tumors. Oncogene, 23(43), 7267-7273, Sep 20.
4. Wang, J. C., & Dick, J. E. (2005). Cancer stem cells: Lessons from leukemia. Trends in Cell Biology, 15(9), 494-501, Sep.
5. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., & Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100(7), 3983-3988, Apr 1.
6. Bonnet, D., & Dick, J. E. (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med., 3(7), 730-737, Jul.
7. Galli, R., Binda, E., Orfanelli, U., et al. (2004). Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Research, 64(19), 7011-7021, Oct 1.
8. Lapidot, T., Sirard, C., Vormoor, J., et al. (1994). A cell initiating human acute myeloid leukaemia after transplantation, into SCID mice. Nature, 567(6464), 645-648, Feb 17.
9. Singh, S. K., Clarke, I. D., Terasaki, M., et al. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Research, 63(18), 5821-5828, Sep 15.
10. Singh, S. K., Hawkins, C., Clarke, I. D., et al. (2004). Identification of human brain tumour initiating cells. Nature, 432(7015), 396-401, Nov 18.
11. Alonso, L., & Fuchs, E. (2003). Stem cells in the skin: Waste not, Wnt not. Genes & Development, 17(10), 1189-1200, May 15.
12. Galli, R., Gritti, A., Bonfanti, L., & Vescovi, A. L. (2003). Neural stem cells: An overview. Circulation Research, 92(6), 598-608, Apr 4.
13. Porten, C. S., & Loeffler, M. (1990). Stem cells: Attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development, 110(4), 1001-1020, Dec.
14. Seaberg, R. M., & van der Kooy, D. (2003). Stem and progenitor cells: The premature desertion of rigorous definitions. Trends in Neurosciences, 26(3), 125-131, Mar.
15. Smith, C. (2003). Hematopoietic stem cells and hematopoiesis. Cancer Control, 10(1), 9-16, Jan-Feb.
16. Wicha, M. S., Liu, S., & Dontu, G. (2006). Cancer stem cells: An old idea - A paradigm, shift. Cancer Research, 66(4), 1883-1890; discussion 1895-1886, Feb 15.
17. Dontu, G., Abdallah, W. M., Foley, J. M., et al. (2003). In vitro propagation and transcriptional, profiling of human mammary stem/progenitor cells. Genes & Development, 17(10), 1253-1270, May 15.
18. Reynolds, B. A., & Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Developments in Biologicals, 175(1), 1-13, Apr 10.
19. Weiss, S., Reynolds, B. A., Vescovi, A. L., Morshead, C., Craig, C. G., & van der Kooy, D. (1996). Is there a neural stem cell in the mammalian forebrain? Trends in Neurosciences, 19(9), 387-393, Sep.
20. Miller, S. J., Lavker, R. M., & Sun, T. T. (2005). Interpreting epithelial cancer biology in the context of stem cells: Tumor properties and therapeutic implications. Biochimica et Biophysica Acta, 1756(1), 25-52, Sep 25.
21. Liu, S., Dontu, G., & Wicha, M. S. (2005). Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Research, 7(3), 86-95.
22. Salsbury, A. J. (1975). The significance of the circulating cancer cell. Cancer Treatment Reviews, 2(1), 55-72, Mar.
23. DeOme, K. B., Faulkin Jr., L. J., Bern, H. A., & Blair, P. B. (1959). Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-tree mammary fat pads of female C3H mice. Cancer Research, 19(5), 515-520, Jun.
24. Medina, D. (1996). The mammary gland: A unique organ for the study of development and tumorigenesis. Journal of Mammary Gland Biology and Neoplasia, 1(1), 5-19, Jan.
25. Kordon, E. C., & Smith, G. H. (1998).An entire functional mammary gland may comprise the progeny from a single cell. Development, 125(10), 1921-1930, May.
26. Smith, G. H. (1996). Experimental mammary epithelial morphogenesis in an in vivo model: Evidence for distinct cellular progenitors of the ductal and lobular phenotype. Breast Cancer Research and Treatment, 39(1), 21-31.
27. Shackleton, M., Vaillant, F., Simpson, K. J., et al. (2006). Generation of a functional mammary gland from a single stem cell. Nature, 439(7072), 84-88, Jan 5.
28. Stingl, J., Eirew, P., Ricketson, I., et al. (2006). Purification and unique properties of mammary epithelial stem cells. Nature, 439 (7079), 993-997, Feb 23.
29. WeIm, B. E., Tepera, S. B., Venezia, T., Graubert, T. A., Rosen, J. M., & Goodell, M. A. (2002). Sca-1 (pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Developments in Biologicals, 245(1), 42-56, May 1.
30. Kenney, N. J., Smith, G. H., Lawrence, E., Barrett, J. C., & Salomon, D. S. (2001).Identification of stem, cell units in the terminal end bud and duct of the mouse mammary gland. Journal of Biomedicine and Biotechnology, 1(3), 133-143.
31. Kichert, M. M., Schwertfeger, K. L., Ryder, J. W., & Anderson, S. M. (2000). An atlas of mouse mammary gland development. Journal of Mammary Gland Biology and Neoplasia, 5(2), 227-241, Apr.
32. Bartek, J., Durban, E. M., Hallowes, R. C., & Taylor-Papadimitriou, J. A (1985). subclass of luminal, epithelial cells in the human mammary gland, defined by antibodies to cytokeratins. Journal of Cell Science, 75, 17-33, Apr.
33. Smalley, M., & Ashworth, A. (2003). Stem cells and breast cancer: A field in transit. Nature Reviews. Cancer, 3(11), 832-844, Nov.
34. Williams, J. M., & Daniel, C. W. (1983). Mammary ductal elongation: Differentiation of myoepithelium and basal lamina during branching morphogenesis. Developments in Biologicals, 97(2), 274-290, Jun.
35. Srinivasan, K., Strickland, P., Valdes, A., Shin, G. C., & Hinck, L. (2003). Netri.n-1/neogenin interaction stabilizes multipotent progenitor cap cells during mammary gland morphogenesis. Developments in Cell, 4(3), 371-382, Mar.
36. Sapino, A., Macri, L., Gugliotta, P., et al. (1993). mmunophenotypic properties and estrogen dependency of budding cell structures in the developing mouse mammary gland. Differentiation, 55(1), 13-18, Dec.
37. Chepko, G., & Smith, G. H. (1997). Three division-competent, structurally-distinct cell populations contribute to murine mammary epithelial, renewal, Tissue & Cell, 29(2), 239-253, Apr.
38. Smalley, M. J. (1995). Clonal characterisation of mouse mammary luminal epithelial and myoepithelial cells. University of London.
39. Smalley, M. J., Titley, J., & O'Hare, M. J. (1998). Clonal characterization of mouse mammary luminal epithelial and myoepithelial cells separated by fluorescence-activated cell sorting. In vitro Cellular & Developmental Biology. Animal, 34(9), 711-721, Oct.
40. Smalley, M. J., Titley, J., Paterson, H., Perusinghe, N., Clarke, C., & O'Hare, M. J. (1999). Differentiation of separated mouse mammary luminal epithelial and myoepithelial cells cultured on EHS matrix analyzed by indirect immunofluorescence of cytoskeletal antigens. Journal of Histochemistry and Cytochemistry, 47(12), 1513-1524, Dec.
41. O'Hare, M. J., Ormerod, M. G., Monaghan, P., Lane, E. B., & Gusterson, B. A. (1991). Characterization, in vitro of luminal and myoepithelial cells isolated from the human mammary gland by cell sorting. Differentiation, 46(3), 209-221, Apr.
42. Dundas, S. R., Ormerod, M. G., Gusterson, B. A., & O'Hare, M. J. (1991). Characterization of luminal and basal cells flow-sorted from the adult rat mammary parenchyma. Journal of Cell Science, 100(Pt 3), 459-471, Nov.
43. Naylor, S., Smalley, M. J., Robertson, D., Gusterson, B. A., Edwards, P. A., & Dale, T. C. (2000). Retroviral expression of Wnt-1 and Wnt-7b produces different effects in mouse mammary epithelium. Journal of Cell Science, 113(Pt 12), 2129-2138, Jun.
44. Sleeman, K. E., Kendrick, H., Ashworth, A., Isacke, C.M., Smalley, M. J. (2006). CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and nonepithelial cells. Breast Cancer Research, 8(1), R7.
45. Sonnenberg, A., Daams, H., Van der Valk, M. A., Hilkens, J., & Hilgers, J. (1986). Development of mouse mammary gland: Identification of stages in differentiation of luminal and myoepithelial cells using monoclonal antibodies and polyvalent antiserum against keratin. Journal of Histochemistry and Cytochemistry, 34(8), 1037-1046, Aug.
46. Das, N. K., Hosick, H. L., & Nandi, S. (1974). Influence of seeding density on multicellular organization and nuclear events in cultures of normal and neoplastic mouse mammary epithelium. Journal of the National Cancer Institute, 52(3), 849-861, Mar.
47. Singh, S., & Gupta, P. D. (1994). Tampering with cytokeratin expression results in. cell dysfunction. Epithelial Cell Biology, 3 (2), 79-83.
48. Vassar, R., Coulombe, P. A., Degenstein, L., Albers, K., & Fuchs, E. (1991). Mutant keratin, expression in transgenic mice causes marked abnormalities resembling a human genetic skin disease. Cell, 64(2), 365-380, Jan 25.
49. Kumemura, H., Harada, M., Omary, M. B., et al. (2004). Aggregation and loss of cytokeratin filament networks inhibit golgi organization, in liver-derived epithelial cell lines. Cell Motility and the Cytoskeleton, 57(1), 37-52, Jan.
50. Parry, G., Beck, J. C., Moss, L., Bartley, J., & Ojakian, G. K. (1990). Determination of apical membrane polarity in mammary epithelial cell cultures: the role of cell-cell, cell-substratum, and membrane-cytoskeleton interactions. Experimental Cell Research, 188(2), 302-311, Jun.
51. Taylor-Papadimitriou, J., & Lane, E. B. (1987). Keratin, expression in the mammary gland. In C. M. Neville, & C. W. Daniel. (Eds.), The mammary gland: Development, regulation and fonction (pp. 181-215). New York: Plenum.
52. Fatal J. E., Werb, Z., & Bissell, M. J. (2004). Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Research, 6(1), 1-11.
53. Blum, J. L., & Wicha, M. S. (1988). Role of the cytoskeleton in laminin induced mammary gene expression. Journal of Cellular Physiology, 135(1), 13-22, Apr.
54. Li ML, Aggeler, J., Farson, D. A., Hatier, C., Hassell, J., & Bissell, M. J. (1987). Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proceedings of the National Academy of Sciences of the United States of America, 84(1), 136-140, Jan.
55. Deugnier, M. A., Faraldo, M. M., Rousselle, P., Thiery, J. P., & Glukhova, M. A. (1999). Cell-extracellular matrix interactions and EGF are important regulators of the basal mammary epithelial cell phenotype. Journal of Cell Science, 112(Pt 7), 1035-1044, Apr.
56. Streuli, C. H., Bailey, N., & Bissell, M. J. (1991). Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. Journal of Cell Biology, 115(5), 1383-1395, Dec.
57. Kleinman, H. K., McGarvey, M. L., Hassell, J. R., et al. (1986). Basement membrane complexes with biological activity. Biochemistry, 25(2), 312-318, Jan 28.
58. Farrelly, N., Lee, Y. J., Oliver, J., Dive, C., & Streuli, C. H. (1999). Extracellular matrix regulates apoptosis in mammary epithelium through a control on insulin signaling. Journal of Cell Biology, 144(6), 1337-1348, Mar 22.
59. Streuli, C. H., & Gilmore, A. P. (1999). Adhesion-mediated signaling in the regulation of mammary epithelial cell survival. Journal of Mammary Gland Biology and Neoplasia, 4(2), 183-191, Apr.
60. Pullan, S., Wilson, J., Metcalfe, A., et al. (1996). Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. Journal of Cell Science, 109(Pt 3), 631-642, Mar.
61. Cary, L. A., Han, D. C., & Guan, J. L. (1999). Integrin-mediated signal transduction pathways. Histology and Histopathology, 14(3), 1001-1009, Jul.
62. Hynes, R. O. (2002). Integrins: Bidirectional, allosteric signaling machines. Cell, 110(6), 673-687, Sep 20.
63. Pozzi, A., & Zent, R. (2003). Integrins: Sensors of extracellular matrix and modulators of cell function. Nephron Exp Nephrology, 94(3), e77-e84.
64. Schatzmann, F., Marlow, R., & Streuli, C. H. (2003). Integrin signaling and mammary cell function. Journal of Mammary Gland Biology and Neoplasia, 8(4), 395-408, Oct.
65. Taddei, I., Faraldo, M. M., Teuliere, J., Deugnier, M. A., Thiery, J. P., & Glukhova, M. A. (2003). ntegrins in mammary gland development and differentiation of mammary epithelium. Journal of Mammary Gland Biology and Neoplasia, 8(4), 383-394, Oct.
66. de la Cruz, L., Steffgen, K., Martin, A., McGee, C., & Hathaway, H. (2004). Apoptosis and involution in the mammary gland are altered in mice lacking a novel receptor, betal, 4-Galactosyltransferase I. Developments in Biologicals, 272(2), 286-309, Aug 15.
67. Hathaway, H. J. (2003). Cell surface betal,4-galactosyltransferase function in mammary gland morphogenesis: Insights from transgenic and knockout mouse models. Journal of Mammary Gland Biology and Neoplasia, 8(4), 421-433, Oct.
68. Hathaway, H. J., & Shur, B. D. (1996). Mammary gland morphogenesis is inhibited in transgenic mice that overexpress cell, surface betal,4-galactosyltransferase. Development, 122(9), 2859-2872, Sep.
69. Barcellos-Hoff, M. H. (1992). Mammary epithelial reorganization on extracellular matrix is mediated by cell surface galactosyltransferase. Experimental Cell Research, 201(1), 225-234, Jul.
70. Li N, Zhang, Y., Naylor, M. J., et al. (2005). Betal integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. EMBO Journal, 24(11), 1942-1953, Jun 1.
71. Faraldo, M. M., Deugnier, M. A., Lukashev, M., Thiery, J. P., & Glukhova, M. A. (1998). Perturbation of betol-integrin function alters the development of murine mammary gland. EMBO Journal, 17(8), 2139-2147, Apr 15.
72. Wang, F., Hansen, R. K., Radisky, D., et al. (2002). Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. Journal of the National Cancer Institute, 94(19), 1494-1503, Oct 2.
73. Weaver, V. M., Petersen, O. W., Wang, F., et al. (1997). Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. Journal of Cell Biology, 137(1), 231-245, Apr 7.
74. Pechoux, C., Gudjonsson, T., Ronnov-Jessen, L., Bissell, M. J., & Petersen, O. W. (1999). Human mammary luminal epithelial cells contain progenitors to myoepithelial cells. Developments in Biologicals, 206(1), 88-99, Feb 1.
75. Emerman, J. T., & Vogl, A. W. (1986). Cell size and shape changes in the myoepithelium of the mammary gland during differentiation. Anatomical Record, 216(3), 405-415, Nov.
76. Streuli, C. H. (1993). Extracellular matrix and gene expression in mammary epithelium. Seminars in Cell Biology, 4(3), 203-212, Jun.
77. Goodell, M. A., Brose, K., Paradis, G., Conner, A. S., & Mulligan, R. C. (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. Journal of Experimental Medicine, 183(4), 1797-1806, Apr 1.
78. Zhou, S., Schuetz, J. D., Bunting, K. D., et al. (2001). The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med., 7(9), 1028-1034, Sep.
79. Goodell, M. A., Rosenzweig, M., Kim, H., et al. (1997). Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med., 3(12), 1337-1345, Dec.
80. Hulspas, R., & Quesenberry, P. J. (2000). Characterization of neurosphere cell phenotypes by flow cytometry. Cytometry, 40 (3), 245-250, Jul 1.
81. Alvi, A. J., Clayton, H., Joshi, C., et al. (2003). Functional and molecular characterisation of mammary side population cells. Breast Cancer Research, 5(1), R1-R8.
82. Smalley, M. J., Titley, I., & Ashworth, A. (2005). An improved definition of mouse mammary epithelial side population cells. Cytotherapy, 7(6), 497-508.
83. Jonker, J. W., Merino, G., Musters, S., et al. (2005). The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat. Med., 11(2), 127-129, Feb.
84. Ee P. L., Kamalakaran, S., Tonetti, D., He X, Ross, D. D., & Beck, W. T. (2004). Identification of a novel estrogen response element in the breast cancer resistance protein (ABCG2) gene. Cancer Research, 64(4), 1247-1251, Feb 15.
85. Petersen, T. W., Ibrahim, S. F., Diercks, A. H., & van. den Engh, G. (2004). Chromatic shifts in the fluorescence emitted by murine thymocytes stained with Hoechst 33342. Cytometry, 60A (2), 173-181, Aug.
86. Pirruccello, S. J., & LeBien, T. W. (1986). The human. B cell-associated antigen CD24 is a single chain sialoglycoprotein. Journal of Immunology, 136(10), 3779-3784, May 15.
87. Akashi, T., Shirasawa, T., & Hirokawa, K. (1994). Gene expression of CD24 core polypeptide molecule in normal rat tissues and human tumor cell lines. Virchows Archiv, 425(4), 399-406.
88. Jackson, D., Waibel, R., Weber, E., Bell, J., & Stahel, R. A. (1992). CD24, a signal-transducing molecule expressed on human B cells, is a major surface antigen on small cell lung carcinomas. Cancer Research, 52(19), 5264-5270, Oct 1.
89. Kristiansen, G., Denkert, C., Schluns, K., Dahl, E., Pilarsky, C., & Hauptmann, S. (2002). CD24 is expressed in ovarian cancer and is a new independent prognostic marker of patient survival. American Journal of Pathology, 161(4), 1215-1221, Oct.
90. Kristiansen, G., Pilarsky, C., Pervan, J., et al. (2004). CD24 expression is a significant predictor of PSA relapse and poor prognosis in low grade or organ confined prostate cancer. Prostate, 58(2), 183-192, Feb 1.
91. Kristiansen, G., Winzer, K. J., Mayordomo, E., et al. (2003). CD24 expression is a new prognostic marker in breast cancer. Clinical Cancer Research, 9(13), 4906-4913, Oct 15.
92. Aigner, S., Sthoeger, Z. M., Fogei, M., et al. (1997). CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood, 89(9), 3385-3395, May 1.
93. Sammar, M., Aigner, S., Hubbe, M., et al. (1994). Heat-stable antigen (CD24) as ligand for mouse P-selectin. International Immunology, 6(7), 1027-1036, Jul.
94. Baumann, P., Cremers, N., Kroese, F., et al. (2005). CD24 expression, causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Research, 65(23), 10783-10793, Dec 1.
95. Kristiansen, G., Schluns, K., Yongwei, Y., Denkert, C., Dietel, M., & Petersen, I. (2003). CD24 is an independent prognostic marker of survival in nonsmall cell lung cancer patients. British Journal of Cancer, 88(2), 231-236, Jan 27.
96. Anderson, E., Clarke, R. B., & Howell, A. (1998). Estrogen responsiveness and control of normal human, breast proliferation. Journal of Mammary Gland Biology and Neoplasia, 3(1), 23-35, Jan.
97. Bocchinfuso, W. P., & Korach, K. S. (1997). Mammary gland development and tumorigenesis in estrogen receptor knockout mice. Journal of Mammary Gland Biology and Neoplasia, 2(4), 323-334, Oct.
98. Yager, J. D., & Davidson, N. E. (2006).Estrogen carcinogenesis in breast cancer. New England Journal of Medicine, 354(3), 270-282, Jan 19.
99. Cheng, G., Weihua, Z., Warner, M., & Gustafsson, J. A. (2004). Estrogen receptors ER alpha and ER beta in proliferation in the rodent mammary gland. Proceedings of the National Academy of Sciences of the United States of America, 101(11), 3739-3746, Mar 16.
100. Clarke, R. B., Spence, K., Anderson, E., Howell, A., Okano, H., & Porten, C. S. (2005). A. putative human breast stem cell population is enriched for steroid receptor-positive cells. Developments in Biologicals, 277(2), 443-456, Jan. 15.
101. Booth, B. W., & Smith, G. H. (2006). Estrogen receptor-alpha and progesterone receptor are expressed in label-retaining mammary epithelial cells that divide asymmetrically and retain their template DNA strands. Breast Cancer Research, 8(4), R49, Aug 1.
102. Sotgia, F., Rui, H., Bonuccelli, G., Mercier, I., Pestell, R. G., & Lisanti, M. P. (2006). Caveolin-1, mammary stem cells, and estrogen-dependent breast cancers. Cancer Research, 66(22), 10647-10651, Nov 15.
103. Mallepell, S., Krust, A., Chambon, P., & Brisken, C. (2006). Paracrine signaling through the epithelial estrogen receptor alpha is required for proliferation and morphogenesis in the mammary gland. Proceedings of the National Academy of Sciences of the United States of America, 103(7), 2196-2201, Feb 14.
104. Sleeman, K. E., Kendrick, H., Robertson, D., Isacke, C. M., & Ashworth, A., Smalley, M. J. (2007). Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. Journal of Cell Biology 176(1), 19-26.