Runx2 is a novel regulator of mammary epithelial cell fate in development and breast cancer

Cancer Research

Volumn 74, Issue 18, 2014, Pages 5277-5286

  Owens, Thomas W ^a   Rogers, Renee L ^b   Best, Sarah A ^c,d   Ledger, Anita ^b   Mooney, Anne Marie ^a   Ferguson, Alison ^a   Shore, Paul ^e   Swarbrick, Alexander ^b,f   Ormandy, Christopher J ^b,f   Simpson, Peter T ^g   Carroll, Jason S ^h   Visvader, Jane E ^c,d   Naylor, Matthew J ^a,b,f  

^a UNIVERSITY OF SYDNEY   (Australia)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g UNIVERSITY OF QUEENSLAND   (Australia)

^h IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RUNX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR RUNX2;

ANIMAL; BAGG ALBINO MOUSE; CELL DIFFERENTIATION; CROSS-SECTIONAL STUDY; CYTOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LONGITUDINAL STUDY; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; PREGNANCY; UDDER;

ANIMALS; CELL DIFFERENTIATION; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CROSS-SECTIONAL STUDIES; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; LONGITUDINAL STUDIES; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; PREGNANCY;

EID: 84907494635     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0053     Document Type: Article

References (50)

1. Hennighausen L, Robinson GW. Signaling pathways in mammary gland development. Dev Cell 2001;1:467-75.
2. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-7.
3. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat M-L, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-8.
4. Visvader JE, Smith GH. Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harbor Perspect Biol 2011;3:pii: a004879.
5. Sale S, Lafkas D, Artavanis-Tsakonas S. Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nat Cell Biol 2013;15:451-60.
6. Sheta M, Teschendorff A, Sharp G, Novcic N, Russell A, Avril S, et al. Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland. Breast Cancer Res 2012;14:R134.
7. Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol 2007;9:201-9.
8. Oakes SR, Naylor MJ, Asselin-Labat ML, Blazek KD, Gardiner-Garden M, Hilton HN, et al. The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev 2008;22:581-6.
9. Bouras T, Pal B, Vaillant F, Harburg G, Asselin-Labat ML, Oakes SR, et al. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 2008;3:429-41.
10. Buono KD, Robinson GW, Martin C, Shi S, Stanley P, Tanigaki K, et al. The canonical Notch/RBP-J signaling pathway controls the balance of cell lineages in mammary epithelium during pregnancy. Dev Biol 2006;293:565-80.
11. Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006;127:1041-55.
12. Kouros-Mehr H, Bechis SK, Slorach EM, Littlepage LE, Egeblad M, Ewald AJ, et al. GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model. Cancer Cell 2008;13:141-52.
13. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res 2010;70:709-18.
14. Kalyuga M, Gallego-Ortega D, Lee HJ, Roden DL, Cowley MJ, Caldon CE, et al. ELF5 suppresses estrogen sensitivity and underpins the acquisition of antiestrogen resistance in luminal breast cancer. PLoS Biol 2012;10:e1001461.
15. Owens TW, Naylor MJ. Breast cancer stem cells. Front Physiol 2013;4:225.
16. Cohen MM Jr. Perspectives on RUNX genes: an update. Am J Med Genet Part A. 2009;149A:2629-46.
17. Chimge NO, Frenkel B. The RUNX family in breast cancer: relationships with estrogen signaling. Oncogene 2013;32:2121-30.
18. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997;89:755-64.
19. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997;89:765-71.
20. Kouros-Mehr H, Werb Z. Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis. Dev Dynamics 2006;235:3404-12.
21. Kendrick H, Regan JL, Magnay FA, Grigoriadis A, Mitsopoulos C, Zvelebil M, et al. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics 2008;9:591.
22. Inman CK, Shore P. The osteoblast transcription factor Runx2 is expressed in mammary epithelial cells and mediates osteopontin expression. J Biol Chem 2003;278:48684-9.
23. Barnes GL, Javed A, Waller SM, Kamal MH, Hebert KE, Hassan MQ, et al. Osteoblast-related transcription factors Runx2 (Cbfa1/AML3) and MSX2 mediate the expression of bone sialoprotein in human metastatic breast cancer cells. Cancer Res 2003;63:2631-7.
24. Chimge NO, Baniwal SK, Little GH, Chen YB, Kahn M, Tripathy D, et al. Regulation of breast cancer metastasis by Runx2 and estrogen signaling: the role of SNAI2. Breast Cancer Res 2011;13:R127.
25. Pratap J, Imbalzano KM, Underwood JM, Cohet N, Gokul K, Akech J, et al. Ectopic runx2 expression in mammary epithelial cells disrupts formation of normal acini structure: implications for breast cancer progression. Cancer Res 2009;69:6807-14.
26. Mendoza-Villanueva D, Zeef L, Shore P. Metastatic breast cancer cells inhibit osteoblast differentiation through the Runx2/CBFbeta-dependent expression of the Wnt antagonist, sclerostin. Breast Cancer Res 2011;13:R106.
27. Pratap J, Javed A, Languino LR, van Wijnen AJ, Stein JL, Stein GS, et al. The Runx2 osteogenic transcription factor regulates matrix metalloproteinase 9 in bone metastatic cancer cells and controls cell invasion. Mol Cell Biol 2005;25:8581-91.
28. Javed A, Barnes GL, Pratap J, Antkowiak T, Gerstenfeld LC, van Wijnen AJ, et al. Impaired intranuclear trafficking of Runx2 (AML3/CBFA1) transcription factors in breast cancer cells inhibits osteolysis in vivo. Proc Natl Acad Sci U S A 2005;102:1454-9.
29. Wagner K-U, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L, et al. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 1997;25:4323-30.
30. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 2003;163:2113-26.
31. Asselin-Labat ML, Sutherland KD, Vaillant F, Gyorki DE, Wu D, Holroyd S, et al. Gata-3 negatively regulates the tumor-initiating capacity of mammary luminal progenitor cells and targets the putative tumor suppressor caspase-14. Mol Cell Biol 2011;31:4609-22.
32. Ball RK, Friis RR, Schoenenberger CA, Doppler W, Groner B. Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line. EMBO J 1988;7:2089-95.
33. Simmons MJ, Serra R, Hermance N, Kelliher MA. NOTCH1 inhibition in vivo results in mammary tumor regression and reduced mammary tumorsphere-forming activity in vitro. Breast Cancer Res 2012;14:R126.
34. Pratap J, Wixted JJ, Gaur T, Zaidi SK, Dobson J, Gokul KD, et al. Runx2 transcriptional activation of Indian Hedgehog and a downstream bone metastatic pathway in breast cancer cells. Cancer Res 2008;68:7795-802.
35. Liu W, Toyosawa S, Furuichi T, Kanatani N, Yoshida C, Liu Y, et al. Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol 2001;155:157-66.
36. Ann EJ, Kim HY, Choi YH, Kim MY, Mo JS, Jung J, et al. Inhibition of Notch1 signaling by Runx2 during osteoblast differentiation. J Bone Miner Res 2011;26:317-30.
37. Xu N, Liu H, Qu F, Fan J, Mao K, Yin Y, et al. Hypoxia inhibits the differentiation of mesenchymal stem cells into osteoblasts by activation of Notch signaling. Exp Mol Path 2013;94:33-9.
38. Rios AC, Fu NY, Lindeman GJ, Visvader JE. In situ identification of bipotent stem cells in the mammary gland. Nature 2014:506:322-7.
39. Lucero CM, Vega OA, Osorio MM, Tapia JC, Antonelli M, Stein GS, et al. The cancer-related transcription factor Runx2 modulates cell proliferation in human osteosarcoma cell lines. J Cell Physiol 2013;228:714-23.
40. Shen R, Wang X, Drissi H, Liu F, O'Keefe RJ, Chen D. Cyclin D1-cdk4 induce runx2 ubiquitination and degradation. J Biol Chem 2006;281:16347-53.
41. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 2011;11:558-72.
42. Peurala E, Koivunen P, Haapasaari KM, Bloigu R, Jukkola-Vuorinen A. The prognostic significance and value of cyclin D1, CDK4 and p16 in human breast cancer. Breast Cancer Res 2013;15:R5.
43. Xu XL, Chen SZ, Chen W, Zheng WH, Xia XH, Yang HJ, et al. The impact of cyclin D1 overexpression on the prognosis of ER-positive breast cancers: a meta-analysis. Breast Cancer Res Treat 2013;139:329-39.
44. Casimiro MC, Wang C, Li Z, Di Sante G, Willmart NE, Addya S, et al. Cyclin D1 determines estrogen signaling in the mammary gland in vivo. Mol Endocrinol 2013;27:1415-28.
45. Jeselsohn R, Brown NE, Arendt L, Klebba I, Hu MG, Kuperwasser C, et al. Cyclin D1 kinase activity is required for the self-renewal of mammary stem and progenitor cells that are targets of MMTV-ErbB2 tumorigenesis. Cancer Cell 2010;17:65-76.
46. Ling H, Sylvestre JR, Jolicoeur P. Cyclin D1-dependent induction of luminal inflammatory breast tumors by activated notch3. Cancer Res 2013;73:5963-73.
47. Hernandez LL, Gregerson KA, Horseman ND. Mammary gland serotonin regulates parathyroid hormone-related protein and other bonerelated signals. Am J Physiology Endo Metab 2012;302:E1009-15.
48. Wagner KU, Booth BW, Boulanger CA, Smith GH. Multipotent PI-MECs are the true targets of MMTV-neu tumorigenesis. Oncogene 2013;32:1338.
49. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009;15:907-13.
50. Luo M, Zhao X, Chen S, Liu S, Wicha MS, Guan JL. Distinct FAK activities determine progenitor and mammary stem cell characteristics. Cancer Res 2013;73:5591-602.