A Long-Lived Luminal Subpopulation Enriched with Alveolar Progenitors Serves as Cellular Origin of Heterogeneous Mammary Tumors

Stem Cell Reports

Volumn 5, Issue 1, 2015, Pages 60-74

  Tao, Luwei ^a,b   Van Bragt, Maaike P A ^a,b   Li, Zhe ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN;

ADENOVIRIDAE; ALVEOLAR PROGENITOR CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST EPITHELIUM CELL; BREAST TUMOR; CELL DIFFERENTIATION; CELL LINEAGE; CELL SUBPOPULATION; CONTROLLED STUDY; FEMALE; IMMUNOFLUORESCENCE; LACTATION; MOUSE; NONHUMAN; NULLIPARA; ONCOGENE; PREGNANCY; PRIORITY JOURNAL; STEM CELL; ANIMAL; BIOSYNTHESIS; EPITHELIUM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; PATHOLOGY; UDDER;

ADENOVIRIDAE; MUS;

ANIMALS; BREAST NEOPLASMS; CELL LINEAGE; EPITHELIAL CELLS; FEMALE; HUMANS; INTEGRIN BETA3; MAMMARY GLANDS, ANIMAL; MICE; PREGNANCY; STEM CELLS;

EID: 84937525619     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.05.014     Document Type: Article

References (45)

1. M.L. Asselin-Labat, K.D. Sutherland, H. Barker, R. Thomas, M. Shackleton, N.C. Forrest, L. Hartley, L. Robb, F.G. Grosveld, J. van der Wees, and et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation Nat. Cell Biol. 9 2007 201 209
2. M.L. Asselin-Labat, K.D. Sutherland, F. Vaillant, D.E. Gyorki, D. Wu, S. Holroyd, K. Breslin, T. Ward, W. Shi, M.L. Bath, and 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. 31 2011 4609 4622
3. B.W. Booth, C.A. Boulanger, and G.H. Smith Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation J. Cell. Physiol. 212 2007 729 736
4. C.A. Boulanger, K.U. Wagner, and G.H. Smith Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression Oncogene 24 2005 552 560
5. T.H. Chang, K. Kunasegaran, G.A. Tarulli, D. De Silva, P.M. Voorhoeve, and A.M. Pietersen New insights into lineage restriction of mammary gland epithelium using parity-identified mammary epithelial cells Breast Cancer Res. 16 2014 R1
6. N. Choi, B. Zhang, L. Zhang, M. Ittmann, and L. Xin Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation Cancer Cell 21 2012 253 265
7. N. Forster, S.V. Saladi, M. van Bragt, M.E. Sfondouris, F.E. Jones, Z. Li, and L.W. Ellisen Basal cell signaling by p63 controls luminal progenitor function and lactation via NRG1 Dev. Cell 28 2014 147 160
8. S. Haricharan, J. Dong, S. Hein, J.P. Reddy, Z. Du, M. Toneff, K. Holloway, S.G. Hilsenbeck, S. Huang, R. Atkinson, and et al. Mechanism and preclinical prevention of increased breast cancer risk caused by pregnancy eLife 2 2013 e00996
9. S. Haricharan, S.M. Hein, J. Dong, M.J. Toneff, O.H. Aina, P.H. Rao, R.D. Cardiff, and Y. Li Contribution of an alveolar cell of origin to the high-grade malignant phenotype of pregnancy-associated breast cancer Oncogene 33 2014 5729 5739
10. M.D. Henry, A.A. Triplett, K.B. Oh, G.H. Smith, and K.U. Wagner Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice Oncogene 23 2004 6980 6985
11. R. Jeselsohn, N.E. Brown, L. Arendt, I. Klebba, M.G. Hu, C. Kuperwasser, and P.W. Hinds 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 17 2010 65 76
12. F.E. Jones, D.J. Jerry, B.C. Guarino, G.C. Andrews, and D.F. Stern Heregulin induces in vivo proliferation and differentiation of mammary epithelium into secretory lobuloalveoli Cell Growth Differ. 7 1996 1031 1038
13. E.C. Kordon, and G.H. Smith An entire functional mammary gland may comprise the progeny from a single cell Development 125 1998 1921 1930
14. Z. Li, C.E. Tognon, F.J. Godinho, L. Yasaitis, H. Hock, J.I. Herschkowitz, C.L. Lannon, E. Cho, S.J. Kim, R.T. Bronson, and et al. ETV6-NTRK3 fusion oncogene initiates breast cancer from committed mammary progenitors via activation of AP1 complex Cancer Cell 12 2007 542 558
15. W. Li, B.J. Ferguson, W.T. Khaled, M. Tevendale, J. Stingl, V. Poli, T. Rich, P. Salomoni, and C.J. Watson PML depletion disrupts normal mammary gland development and skews the composition of the mammary luminal cell progenitor pool Proc. Natl. Acad. Sci. USA 106 2009 4725 4730
16. E. Lim, F. Vaillant, D. Wu, N.C. Forrest, B. Pal, A.H. Hart, M.L. Asselin-Labat, D.E. Gyorki, T. Ward, A. Partanen kConFab Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers Nat. Med. 15 2009 907 913
17. E. Lim, D. Wu, B. Pal, T. Bouras, M.L. Asselin-Labat, F. Vaillant, H. Yagita, G.J. Lindeman, G.K. Smyth, and J.E. Visvader Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways Breast Cancer Res. 12 2010 R21
18. C. Liu, J.C. Sage, M.R. Miller, R.G. Verhaak, S. Hippenmeyer, H. Vogel, O. Foreman, R.T. Bronson, A. Nishiyama, L. Luo, and H. Zong Mosaic analysis with double markers reveals tumor cell of origin in glioma Cell 146 2011 209 221
19. L.A. Matulka, A.A. Triplett, and K.U. Wagner Parity-induced mammary epithelial cells are multipotent and express cell surface markers associated with stem cells Dev. Biol. 303 2007 29 44
20. G. Molyneux, F.C. Geyer, F.A. Magnay, A. McCarthy, H. Kendrick, R. Natrajan, A. Mackay, A. Grigoriadis, A. Tutt, A. Ashworth, and et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells Cell Stem Cell 7 2010 403 417
21. C.M. Perou, T. Sørlie, M.B. Eisen, M. van de Rijn, S.S. Jeffrey, C.A. Rees, J.R. Pollack, D.T. Ross, H. Johnsen, L.A. Akslen, and et al. Molecular portraits of human breast tumours Nature 406 2000 747 752
22. A.D. Pfefferle, J.I. Herschkowitz, J. Usary, J.C. Harrell, B.T. Spike, J.R. Adams, M.I. Torres-Arzayus, M. Brown, S.E. Egan, G.M. Wahl, and et al. Transcriptomic classification of genetically engineered mouse models of breast cancer identifies human subtype counterparts Genome Biol. 14 2013 R125
23. A. Prat, J.S. Parker, O. Karginova, C. Fan, C. Livasy, J.I. Herschkowitz, X. He, and C.M. Perou Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer Breast Cancer Res. 12 2010 R68
24. M.D. Prater, V. Petit, I. Alasdair Russell, R.R. Giraddi, M. Shehata, S. Menon, R. Schulte, I. Kalajzic, N. Rath, M.F. Olson, and et al. Mammary stem cells have myoepithelial cell properties Nat. Cell Biol. 16 2014 942 950
25. T.A. Proia, P.J. Keller, P.B. Gupta, I. Klebba, A.D. Jones, M. Sedic, H. Gilmore, N. Tung, S.P. Naber, S. Schnitt, and et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate Cell Stem Cell 8 2011 149 163
26. A.C. Rios, N.Y. Fu, G.J. Lindeman, and J.E. Visvader In situ identification of bipotent stem cells in the mammary gland Nature 506 2014 322 327
27. G.W. Robinson, R.A. McKnight, G.H. Smith, and L. Hennighausen Mammary epithelial cells undergo secretory differentiation in cycling virgins but require pregnancy for the establishment of terminal differentiation Development 121 1995 2079 2090
28. V. Rodilla, A. Dasti, M. Huyghe, D. Lafkas, C. Laurent, F. Reyal, and S. Fre Luminal progenitors restrict their lineage potential during mammary gland development PLoS Biol. 13 2015 e1002069
29. S. Šale, D. Lafkas, and S. Artavanis-Tsakonas Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages Nat. Cell Biol. 15 2013 451 460
30. M. Shackleton, F. Vaillant, K.J. Simpson, J. Stingl, G.K. Smyth, M.L. Asselin-Labat, L. Wu, G.J. Lindeman, and J.E. Visvader Generation of a functional mammary gland from a single stem cell Nature 439 2006 84 88
31. M. Shehata, A. Teschendorff, G. Sharp, N. Novcic, I.A. Russell, S. Avril, M. Prater, P. Eirew, C. Caldas, C.J. Watson, and J. Stingl Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland Breast Cancer Res. 14 2012 R134
32. A. Skibinski, and C. Kuperwasser The origin of breast tumor heterogeneity Oncogene 2015
33. K.E. Sleeman, H. Kendrick, D. Robertson, C.M. Isacke, A. Ashworth, and M.J. Smalley Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland J. Cell Biol. 176 2007 19 26
34. G.H. Smith 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
35. T. Sorlie, R. Tibshirani, J. Parker, T. Hastie, J.S. Marron, A. Nobel, S. Deng, H. Johnsen, R. Pesich, S. Geisler, and et al. Repeated observation of breast tumor subtypes in independent gene expression data sets Proc. Natl. Acad. Sci. USA 100 2003 8418 8423
36. J. Stingl, P. Eirew, I. Ricketson, M. Shackleton, F. Vaillant, D. Choi, H.I. Li, and C.J. Eaves Purification and unique properties of mammary epithelial stem cells Nature 439 2006 993 997
37. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. USA 102 2005 15545 15550
38. L. Tao, M.P.A. van Bragt, E. Laudadio, and Z. Li Lineage tracing of mammary epithelial cells using cell-type-specific cre-expressing adenoviruses Stem Cell Reports 2 2014 770 779
39. R. van Amerongen, A.N. Bowman, and R. Nusse Developmental stage and time dictate the fate of Wnt/β-catenin-responsive stem cells in the mammary gland Cell Stem Cell 11 2012 387 400
40. A. Van Keymeulen, A.S. Rocha, M. Ousset, B. Beck, G. Bouvencourt, J. Rock, N. Sharma, S. Dekoninck, and C. Blanpain Distinct stem cells contribute to mammary gland development and maintenance Nature 479 2011 189 193
41. J.E. Visvader Cells of origin in cancer Nature 469 2011 314 322
42. K.U. Wagner, R.J. Wall, L. St-Onge, P. Gruss, A. Wynshaw-Boris, L. Garrett, M. Li, P.A. Furth, and L. Hennighausen Cre-mediated gene deletion in the mammary gland Nucleic Acids Res. 25 1997 4323 4330
43. K.U. Wagner, C.A. Boulanger, M.D. Henry, M. Sgagias, L. Hennighausen, and G.H. Smith An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal Development 129 2002 1377 1386
44. Z.A. Wang, A. Mitrofanova, S.K. Bergren, C. Abate-Shen, R.D. Cardiff, A. Califano, and M.M. Shen Lineage analysis of basal epithelial cells reveals their unexpected plasticity and supports a cell-of-origin model for prostate cancer heterogeneity Nat. Cell Biol. 15 2013 274 283
45. D. Wang, C. Cai, X. Dong, Q.C. Yu, X.O. Zhang, L. Yang, and Y.A. Zeng Identification of multipotent mammary stem cells by protein C receptor expression Nature 517 2015 81 84