In Vitro Analysis of Breast Cancer Cell Line Tumourspheres and Primary Human Breast Epithelia Mammospheres Demonstrates Inter- and Intrasphere Heterogeneity

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Smart, Chanel E ^a,b   Morrison, Brian J ^b,c   Saunus, Jodi M ^a   Vargas, Ana Cristina ^a   Keith, Patricia ^a,b   Reid, Lynne ^a,b   Wockner, Leesa ^b   Amiri, Marjan Askarian ^a   Sarkar, Debina ^a   Simpson, Peter T ^a,b   Clarke, Catherine ^f   Schmidt, Chris W ^b   Reynolds, Brent A ^d   Lakhani, Sunil R ^a,e,f   Lopez, J Alejandro ^b,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c GRIFFITH UNIVERSITY   (Australia)

^d UNIVERSITY OF FLORIDA   (United States)

^e ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^f UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; MUCIN 1;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL CULTURE; CELL ADHESION; CELL DIVISION; CELL HETEROGENEITY; CELL RENEWAL; CELL SPECIFICITY; CELL TYPE; CLONOGENESIS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAMMOSPHERE; PHENOTYPE; STEM CELL; TUMORSPHERE;

BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; FLOW CYTOMETRY; HUMANS; MAMMARY GLANDS, HUMAN; PHENOTYPE; SPHEROIDS, CELLULAR;

EID: 84878623584     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064388     Document Type: Article

References (55)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
2. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, et al. (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69: 1302-1313.
3. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, et al. (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511.
4. Korkaya H, Paulson A, Iovino F, Wicha MS, (2008) HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 27: 6120-6130.
5. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, et al. (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100: 672-679.
6. Cariati M, Naderi A, Brown JP, Smalley MJ, Pinder SE, et al. (2008) Alpha-6 integrin is necessary for the tumourigenicity of a stem cell-like subpopulation within the MCF7 breast cancer cell line. Int J Cancer 122: 298-304.
7. Wicha MS (2007) Breast cancer stem cells: the other side of the story. Stem Cell Rev 3: 110-112; discussion 113.
8. Morrison BJ, Schmidt CW, Lakhani SR, Reynolds BA, Lopez JA, (2008) Breast cancer stem cells: implications for therapy of breast cancer. Breast Cancer Res 10: 210.
9. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, et al. (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17: 1253-1270.
10. Reynolds BA, Weiss S, (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175: 1-13.
11. Farnie G, Clarke RB, Spence K, Pinnock N, Brennan K, et al. (2007) Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst 99: 616-627.
12. Grimshaw MJ, Cooper L, Papazisis K, Coleman JA, Bohnenkamp HR, et al. (2008) Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 10: R52.
13. Fillmore CM, Kuperwasser C, (2008) Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10: R25.
14. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, et al. (2008) High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med.
15. Xie G, Zhan J, Tian Y, Liu Y, Chen Z, et al. (2012) Mammosphere cells from high-passage MCF7 cell line show variable loss of tumorigenicity and radioresistance. Cancer Lett 316: 53-61.
16. Kok M, Koornstra RH, Margarido TC, Fles R, Armstrong NJ, et al. (2009) Mammosphere-derived gene set predicts outcome in patients with ER-positive breast cancer. J Pathol 218: 316-326.
17. Magnifico A, Albano L, Campaner S, Delia D, Castiglioni F, et al. (2009) Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res 15: 2010-2021.
18. Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, et al. (2009) Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 7: e1000121.
19. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, et al. (2010) Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140: 62-73.
20. Pastrana E, Silva-Vargas V, Doetsch F, (2011) Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8: 486-498.
21. Dey D, Saxena M, Paranjape AN, Krishnan V, Giraddi R, et al. (2009) Phenotypic and functional characterization of human mammary stem/progenitor cells in long term culture. PLoS One 4: e5329.
22. Peng T, Qinghua M, Zhenning T, Kaifa W, Jun J, (2011) Long-term sphere culture cannot maintain a high ratio of cancer stem cells: a mathematical model and experiment. PLoS One 6: e25518.
23. Matilainen H, Yu XW, Tang CW, Berridge MV, McConnell MJ (2012) Sphere formation reverses the metastatic and cancer stem cell phenotype of the murine mammary tumour 4T1, independently of the putative cancer stem cell marker Sca-1. Cancer Lett.
24. Kurebayashi J, Kurosumi M, Sonoo H, (1995) A new human breast cancer cell line, KPL-1 secretes tumour-associated antigens and grows rapidly in female athymic nude mice. Br J Cancer 71: 845-853.
25. Whitehead RH, Monaghan P, Webber LM, Bertoncello I, Vitali AA, (1983) A new human breast carcinoma cell line (PMC42) with stem cell characteristics. II. Characterization of cells growing as organoids. J Natl Cancer Inst 71: 1193-1203.
26. Reynolds BA, Weiss S, (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
27. Clarke CL, Sandle J, Jones AA, Sofronis A, Patani NR, et al. (2006) Mapping loss of heterozygosity in normal human breast cells from BRCA1/2 carriers. Br J Cancer 95: 515-519.
28. Stingl J, Emerman JT, Eaves CJ, (2005) Enzymatic dissociation and culture of normal human mammary tissue to detect progenitor activity. Methods Mol Biol 290: 249-263.
29. Maguer-Satta V, Chapellier M, Delay E, Bachelard-Cascales E (2011) CD10: a tool to crack the role of stem cells in breast cancer. Proc Natl Acad Sci U S A 108: E1264; author reply E1265.
30. Deleyrolle LP, Ericksson G, Morrison BJ, Lopez JA, Burrage K, et al. (2011) Determination of somatic and cancer stem cell self-renewing symmetric division rate using sphere assays. PLoS One 6: e15844.
31. Heppner GH, Wolman SR, (1999) MCF-10AT: A Model for Human Breast Cancer Development. Breast J 5: 122-129.
32. Hollestelle A, Nagel JH, Smid M, Lam S, Elstrodt F, et al. (2009) Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res Treat.
33. Lacroix M, Leclercq G, (2004) Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat 83: 249-289.
34. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, et al. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10: 515-527.
35. Lacroix M, (2008) Persistent use of "false" cell lines. Int J Cancer 122: 1-4.
36. Kenny PA, Lee GY, Myers CA, Neve RM, Semeiks JR, et al. (2007) The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol Oncol 1: 84-96.
37. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, et al. (2009) Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4: e6146.
38. Prat A, Parker JS, Karginova O, Fan C, Livasy C, et al. (2010) Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 12: R68.
39. Yoshino K, Iimura E, Saijo K, Iwase S, Fukami K, et al. (2006) Essential role for gene profiling analysis in the authentication of human cell lines. Hum Cell 19: 43-48.
40. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, et al. (2009) Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 15: 907-913.
41. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 Is a Marker of Normal and Malignant Human Mammary Stem Cells and a Predictor of Poor Clinical Outcome. Cell Stem Cell 1: 555-567.
42. Chu JS, Chang KJ, (1999) Mucin expression in mucinous carcinoma and other invasive carcinomas of the breast. Cancer Lett 142: 121-127.
43. Raouf A, Zhao Y, To K, Stingl J, Delaney A, et al. (2008) Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 3: 109-118.
44. Storci G, Sansone P, Trere D, Tavolari S, Taffurelli M, et al. (2008) The basal-like breast carcinoma phenotype is regulated by SLUG gene expression. The Journal of Pathology 214: 25-37.
45. Proia TA, Keller PJ, Gupta PB, Klebba I, Jones AD, et al. (2011) Genetic Predisposition Directs Breast Cancer Phenotype by Dictating Progenitor Cell Fate. Cell Stem Cell 8: 149-163.
46. Keller PJ, Lin AF, Arendt LM, Klebba I, Jones AD, et al. (2010) Mapping the cellular and molecular heterogeneity of normal and malignant breast tissues and cultured cell lines. Breast cancer research: BCR 12: R87.
47. Stingl J, Eaves CJ, Kuusk U, Emerman JT, (1998) Phenotypic and functional characterization in vitro of a multipotent epithelial cell present in the normal adult human breast. Differentiation 63: 201-213.
48. Bachelard-Cascales E, Chapellier M, Delay E, Pochon G, Voeltzel T, et al. (2010) The CD10 enzyme is a key player to identify and regulate human mammary stem cells. Stem Cells 28: 1081-1088.
49. Keller PJ, Arendt LM, Skibinski A, Logvinenko T, Klebba I, et al. (2012) Defining the cellular precursors to human breast cancer. Proc Natl Acad Sci U S A 109: 2772-2777.
50. Kern SE, Shibata D, (2007) The fuzzy math of solid tumor stem cells: a perspective. Cancer Res 67: 8985-8988.
51. Visvader JE, Lindeman GJ, (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768.
52. Wang F, Weaver VM, Petersen OW, Larabell CA, Dedhar S, et al. (1998) Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc Natl Acad Sci U S A 95: 14821-14826.
53. Inch WR, McCredie JA, Sutherland RM, (1970) Growth of nodular carcinomas in rodents compared with multi-cell spheroids in tissue culture. Growth 34: 271-282.
54. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA, (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4: 309-324.
55. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, et al. (2010) Multicellular tumor spheroids: An underestimated tool is catching up again. J Biotechnol.