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

Volumn 17, Issue 1, 2010, Pages 65-76

  Jeselsohn, Rinath ^a   Brown, Nelson E ^a   Arendt, Lisa ^a,b   Klebba, Ina ^a,b   Hu, Miaofen G ^a   Kuperwasser, Charlotte ^a,b   Hinds, Philip W ^a  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLCYCLE; STEMCELL

Indexed keywords

CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; WNT1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST CELL; BREAST EPITHELIUM; CARCINOGENESIS; CELL DIFFERENTIATION; CELL POPULATION; CELL REGENERATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

MOUSE MAMMARY TUMOR VIRUS;

EID: 73649115686     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2009.11.024     Document Type: Article

References (37)

1. Asselin-Labat M.L., Sutherland K.D., Barker H., Thomas R., Shackleton M., Forrest N.C., Hartley L., Robb L., Grosveld F.G., van der Wees J., et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat. Cell Biol. 9 (2007) 201-209
2. Baker G.L., Landis M.W., and Hinds P.W. Multiple functions of D-type cyclins can antagonize pRb-mediated suppression of proliferation. Cell Cycle 4 (2005) 330-338
3. Booth B.W., Boulanger C.A., and Smith G.H. Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation. J. Cell. Physiol. 212 (2007) 729-736
4. Boulanger C.A., Wagner K.U., and Smith G.H. Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression. Oncogene 24 (2005) 552-560
5. Chepko G., Slack R., Carbott D., Khan S., Steadman L., and Dickson R.B. Differential alteration of stem and other cell populations in ducts and lobules of TGFalpha and c-Myc transgenic mouse mammary epithelium. Tissue Cell 37 (2005) 393-412
6. Debnath J., Muthuswamy S.K., and Brugge J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30 (2003) 256-268
7. Deome K.B., Faulkin Jr. L.J., Bern H.A., and Blair P.B. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 19 (1959) 515-520
8. DiMeo T.A., Anderson K., Phadke P., Fan C., Perou C.M., Naber S., and Kuperwasser C. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 69 (2009) 5364-5373
9. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., and Wicha M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17 (2003) 1253-1270
10. Fantl V., Stamp G., Andrews A., Rosewell I., and Dickson C. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev. 9 (1995) 2364-2372
11. Gauthier M.L., Berman H.K., Miller C., Kozakeiwicz K., Chew K., Moore D., Rabban J., Chen Y.Y., Kerlikowske K., and Tlsty T.D. Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell 12 (2007) 479-491
12. Henry M.D., Triplett A.A., Oh K.B., Smith G.H., and Wagner K.U. Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice. Oncogene 23 (2004) 6980-6985
13. Herschkowitz J.I., Simin K., Weigman V.J., Mikaelian I., Usary J., Hu Z., Rasmussen K.E., Jones L.P., Assefnia S., Chandrasekharan S., et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 8 (2007) R76
14. Hinds P.W., Dowdy S.F., Eaton E.N., Arnold A., and Weinberg R.A. Function of a human cyclin gene as an oncogene. Proc. Natl. Acad. Sci. USA 91 (1994) 709-713
15. Kordon E.C., and Smith G.H. An entire functional mammary gland may comprise the progeny from a single cell. Development 125 (1998) 1921-1930
16. Kouros-Mehr H., Slorach E.M., Sternlicht M.D., and Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 127 (2006) 1041-1055
17. Landis M.W., Pawlyk B.S., Li T., Sicinski P., and Hinds P.W. Cyclin D1-dependent kinase activity in murine development and mammary tumorigenesis. Cancer Cell 9 (2006) 13-22
18. Li Y., Welm B., Podsypanina K., Huang S., Chamorro M., Zhang X., Rowlands T., Egeblad M., Cowin P., Werb Z., 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 (2003) 15853-15858
19. Li Z., Tognon C.E., Godinho F.J., Yasaitis L., Hock H., Herschkowitz J.I., Lannon C.L., Cho E., Kim S.J., Bronson R.T., et al. ETV6-NTRK3 fusion oncogene initiates breast cancer from committed mammary progenitors via activation of AP1 complex. Cancer Cell 12 (2007) 542-558
20. Liu J.C., Deng T., Lehal R.S., Kim J., and Zacksenhaus E. Identification of Tumorsphere- and Tumor-Initiating Cells in HER2/Neu-Induced Mammary Tumors. Cancer Res. 67 (2007) 8671-8681
21. Matulka L.A., Triplett A.A., and Wagner K.U. Parity-induced mammary epithelial cells are multipotent and express cell surface markers associated with stem cells. Dev. Biol. 303 (2007) 29-44
22. Muller W.J., Sinn E., Pattengale P.K., Wallace R., and Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54 (1988) 105-115
23. Perou C.M., Sorlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., Pollack J.R., Ross D.T., Johnsen H., Akslen L.A., et al. Molecular portraits of human breast tumours. Nature 406 (2000) 747-752
24. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., and Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 456 (2008) 593-598
25. Rowlands T.M., Pechenkina I.V., Hatsell S.J., Pestell R.G., and Cowin P. Dissecting the roles of beta-catenin and cyclin D1 during mammary development and neoplasia. Proc. Natl. Acad. Sci. USA 100 (2003) 11400-11405
26. Shackleton M., Vaillant F., Simpson K.J., Stingl J., Smyth G.K., Asselin-Labat M.L., Wu L., Lindeman G.J., and Visvader J.E. Generation of a functional mammary gland from a single stem cell. Nature 439 (2006) 84-88
27. Sicinski P., Donaher J.L., Parker S.B., Li T., Fazeli A., Gardner H., Haslam S.Z., Bronson R.T., Elledge S.J., and Weinberg R.A. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82 (1995) 621-630
28. Sleeman K.E., Kendrick H., Ashworth A., Isacke C.M., and Smalley M.J. CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res. 8 (2006) R7
29. Sleeman K.E., Kendrick H., Robertson D., Isacke C.M., Ashworth A., and Smalley M.J. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J. Cell Biol. 176 (2007) 19-26
30. Smith G.H. Experimental mammary epithelial morphogenesis in an in vivo model: Evidence for distinct cellular progenitors of the ductal and lobular phenotype. Breast Cancer Res. Treat. 39 (1996) 21-31
31. Smith G.H., and Medina D. Re-evaluation of mammary stem cell biology based on in vivo transplantation. Breast Cancer Res. 10 (2008) 203
32. Smith G.H., Mehrel T., and Roop D.R. Differential keratin gene expression in developing, differentiating, preneoplastic, and neoplastic mouse mammary epithelium. Cell Growth Differ. 1 (1990) 161-170
33. Stingl J., Eaves C.J., Zandieh I., and Emerman J.T. Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res. Treat. 67 (2001) 93-109
34. Stingl J., Eirew P., Ricketson I., Shackleton M., Vaillant F., Choi D., Li H.I., and Eaves C.J. Purification and unique properties of mammary epithelial stem cells. Nature 439 (2006) 993-997
35. Villadsen R., Fridriksdottir A.J., Ronnov-Jessen L., Gudjonsson T., Rank F., LaBarge M.A., Bissell M.J., and Petersen O.W. Evidence for a stem cell hierarchy in the adult human breast. J. Cell Biol. 177 (2007) 87-101
36. Wagner K.U., Boulanger C.A., Henry M.D., Sgagias M., Hennighausen L., and Smith G.H. An adjunct mammary epithelial cell population in parous females: Its role in functional adaptation and tissue renewal. Development 129 (2002) 1377-1386
37. Yu Q., Geng Y., and Sicinski P. Specific protection against breast cancers by cyclin D1 ablation. Nature 411 (2001) 1017-1021