Epithelial and mesenchymal subpopulations within normal basal breast cell lines exhibit distinct stem cell/progenitor properties

Stem Cells

Volumn 30, Issue 2, 2012, Pages 292-303

  Sarrio, David ^a   Franklin, Chris K ^a   Mackay, Alan ^a   Reis Filho, Jorge S ^a   Isacke, Clare M ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Breast cancer; Differentiation; Epithelial mesenchymal transition; Progenitor cells; Stem cell plasticity; Tissue specific stem cells

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALPHA6 INTEGRIN; CD24 ANTIGEN; CD44V ANTIGEN; CLAUDIN; EPITHELIAL CELL ADHESION MOLECULE; FIBRONECTIN; IMMEDIATE EARLY PROTEIN BZLF1; NERVE CELL ADHESION MOLECULE; P CADHERIN; PROTEIN P63; TRANSCRIPTION FACTOR SLUG;

ARTICLE; BREAST EPITHELIUM; CANCER CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; CELL REGENERATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM BASAL CELL; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; MAMMARY GLAND; MESENCHYMAL STROMA CELL; META ANALYSIS (TOPIC); PHENOTYPE; PROTEIN EXPRESSION; STEM CELL; UPREGULATION;

ANTIGENS, DIFFERENTIATION; ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CELL ADHESION MOLECULES; CELL LINE; CELL LINE, TUMOR; CLAUDINS; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HOMEODOMAIN PROTEINS; HUMANS; MAMMARY GLANDS, HUMAN; MESENCHYMAL STEM CELLS; PHENOTYPE; SPHEROIDS, CELLULAR; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84856082583     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.791     Document Type: Article

References (50)

1. Stingl J, Eirew P, Ricketson I et al. Purification and unique properties of mammary epithelial stem cells. Nature 2006;439:993-997. (Pubitemid 43292419)
2. Shackleton M, Vaillant F, Simpson KJ et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-88. (Pubitemid 43053633)
3. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009;23:2563-2577.
4. Stingl J, Caldas C. Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat Rev Cancer 2007;7:791-799. (Pubitemid 47463670)
5. Lim E, Vaillant F, Wu D et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 2009;15:907-913.
6. Chang CC. Recent translational research: Stem cells as the roots of breast cancer. Breast Cancer Res 2006;8:103.
7. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-768.
8. Thiery JP, Acloque H, Huang RY et al. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-890.
9. May CD, Sphyris N, Evans KW et al. Epithelial-mesenchymal transition and cancer stem cells: A dangerously dynamic duo in breast cancer progression. Breast Cancer Res 2011;13:202.
10. Prat A, Parker JS, Karginova O et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010;12:R68.
11. Neve RM, Chin K, Fridlyand J et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006;10:515-527. (Pubitemid 44854747)
12. Blick T, Hugo H, Widodo E et al. Epithelial mesenchymal transition traits in human breast cancer cell lines parallel the CD44(hi/)CD24 (lo/-) stem cell phenotype in human breast cancer. J Mammary Gland Biol Neoplasia 2010;15:235-252.
13. Hollier BG, Evans K, Mani SA. The epithelial-to-mesenchymal transition and cancer stem cells: A coalition against cancer therapies. J Mammary Gland Biol Neoplasia 2009;14:29-43.
14. Mani SA, Guo W, Liao MJ et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-715. (Pubitemid 351636299)
15. Morel AP, Lievre M, Thomas C et al. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008;3:e2888.
16. Pauley RJ, Soule HD, Tait L et al. The MCF10 family of spontaneously immortalized human breast epithelial cell lines: Models of neoplastic progression. Eur J Cancer Prev 1993;2 (suppl 3):67-76.
17. Bloushtain-Qimron N, Yao J, Snyder EL et al. Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci USA 2008;105:14076-14081.
18. Sarrio D, Rodriguez-Pinilla SM, Hardisson D et al. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008;68:989-997. (Pubitemid 351272216)
19. Holliday DL, Brouilette KT, Markert A et al. Novel multicellular organotypic models of normal and malignant breast: Tools for dissecting the role of the microenvironment in breast cancer progression. Breast Cancer Res 2009;11:R3.
20. Dontu G, Abdallah WM, Foley JM et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253-1270. (Pubitemid 36583168)
21. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003;30:256-268. (Pubitemid 36677560)
22. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001;98:5116-5121. (Pubitemid 32397092)
23. Weigelt B, Mackay A, A'Hern R et al. Breast cancer molecular profiling with single sample predictors: A retrospective analysis. Lancet Oncol 2010;11:339-349.
24. Taube JH, Herschkowitz JI, Komurov K et al. Core epithelial-to- mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci USA 2010;107:15449-15454.
25. Charafe-Jauffret E, Ginestier C, Monville F et al. Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 2006;25:2273-2284.
26. Eirew P, Stingl J, Raouf A et al. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat Med 2008;14:1384-1389.
27. Hwang WL, Yang MH, Tsai ML et al. SNAIL regulates interleukin-8 expression, stem cell-like activity, and tumorigenicity of human colorectal carcinoma cells. Gastroenterology 2011;141:279-291.
28. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-428. (Pubitemid 46809165)
29. Al-Hajj M, Wicha MS, Benito-Hernandez A et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003;100:3983-3988. (Pubitemid 36418143)
30. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008;10:R25.
31. Ginestier C, Hur MH, Charafe-Jauffret E et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-567.
32. Marcato P, Dean CA, Pan D et al. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cells 2011;29:32-45.
33. Villadsen R, Fridriksdottir AJ, Ronnov-Jessen L et al. Evidence for a stem cell hierarchy in the adult human breast. J Cell Biol 2007;177:87-101. (Pubitemid 46588404)
34. Raouf A, Zhao Y, To K et al. Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 2008;3:109-118.
35. Stingl J, Eaves CJ, Zandieh I et al. Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res Treat 2001;67:93-109. (Pubitemid 32744490)
36. Wellner U, Schubert J, Burk UC et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009;11:1487-1495.
37. Sun Y, Shao L, Bai H et al. Slug deficiency enhances self-renewal of hematopoietic stem cells during hematopoietic regeneration. Blood 2010;115:1709-1717.
38. Ince TA, Richardson AL, Bell GW et al. Transformation of different human breast epithelial cell types leads to distinct tumor phenotypes. Cancer Cell 2007;12:160-170. (Pubitemid 47199120)
39. Scheel C, Eaton EN, Li SH et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011;145:926-940.
40. Walia V, Elble RC. Enrichment for breast cancer cells with stem/progenitor properties by differential adhesion. Stem Cells Dev 2010;19:1175-1182.
41. Chaffer CL, Brueckmann I, Scheel C et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci USA 2011;108:7950-7955.
42. Biddle A, Liang X, Gammon L et al. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res 2011;71:5317-5326.
43. Creighton CJ, Chang JC, Rosen JM. Epithelial-mesenchymal transition (EMT) in tumor-initiating cells and its clinical implications in breast cancer. J Mammary Gland Biol Neoplasia 2010;15:253-260.
44. Keller PJ, Lin AF, Arendt LM et al. Mapping the cellular and molecular heterogeneity of normal and malignant breast tissues and cultured cell lines. Breast Cancer Res 2010;12:R87.
45. Meyer MJ, Fleming JM, Ali MA et al. Dynamic regulation of CD24 and the invasive, CD44posCD24neg phenotype in breast cancer cell lines. Breast Cancer Res 2009;11:R82.
46. Gupta PB, Fillmore CM, Jiang G et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011;146:633-644.
47. Lim E, Wu D, Pal B et al. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res 2010;12:R21.
48. Petersen OW, Lind Nielsen H, Gudjonsson T et al. The plasticity of human breast carcinoma cells is more than epithelial to mesenchymal conversion. Breast Cancer Res 2001;3:213-217. (Pubitemid 32631699)
49. Molyneux G, Geyer FC, Magnay FA et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010;7:403-417.
50. Proia TA, Keller PJ, Gupta PB et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011;8:149-163.