Mouse mammary stem cells express prognostic markers for triple-negative breast cancer

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Soady, Kelly J ^a,b   Kendrick, Howard ^c   Gao, Qiong ^a   Tutt, Andrew ^d,e   Zvelebil, Marketa ^a   Ordonez, Liliana D ^c   Quist, Jelmar ^d,e   Tan, David Wei Min ^f   Isacke, Clare M ^a   Grigoriadis, Anita ^d,e   Smalley, Matthew J ^c  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d GUY S HOSPITAL   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; RNA; TRANSCRIPTOME; BIOLOGICAL MARKER;

ANIMAL CELL; ARTICLE; BREAST CELL; BREAST EPITHELIUM; CANCER PROGNOSIS; CELL TRANSPLANTATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE ONTOLOGY; IMMUNOCYTOCHEMISTRY; METASTASIS; MOUSE; MYOEPITHELIUM CELL; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; TRIPLE NEGATIVE BREAST CANCER; ANIMAL; CLUSTER ANALYSIS; DISEASE FREE SURVIVAL; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOPHENOTYPING; METABOLISM; MORTALITY; PATHOLOGY; PHENOTYPE; PROGNOSIS; SINGLE CELL ANALYSIS; TRIPLE NEGATIVE BREAST NEOPLASMS; UDDER;

ANIMALS; BIOMARKERS; CLUSTER ANALYSIS; DISEASE-FREE SURVIVAL; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPHENOTYPING; MAMMARY GLANDS, ANIMAL; MICE; NEOPLASM METASTASIS; PHENOTYPE; PROGNOSIS; SINGLE-CELL ANALYSIS; STEM CELLS; TRANSCRIPTOME; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84925864724     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0539-6     Document Type: Article

References (74)

1. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, Van De Vijver MJ. WHO classification of tumors of the breast. 4th ed. Lyon, France: IARC Press; 2012.
2. Carey LA, Dees EC, Sawyer L, Gatti L, Moore DT, Collichio F, et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res. 2007;13:2329-34.
3. Reis-Filho JS, Milanezi F, Steele D, Savage K, Simpson PT, Nesland JM, et al. Metaplastic breast carcinomas are basal-like tumours. Histopathology. 2006;49:10-21.
4. Weigelt B, Reis-Filho JS. Histological and molecular types of breast cancer: is there a unifying taxonomy? Nat Rev Clin Oncol. 2009;6:718-30.
5. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012;486:346-52.
6. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A. 2003;100:8418-23.
7. van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002;415:530-6.
8. Liedtke C, Mazouni C, Hess KR, Andre F, Tordai A, Mejia JA, et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol. 2008;26:1275-81.
9. Smalley M, Piggott L, Clarkson R. Breast cancer stem cells: obstacles to therapy. Cancer Lett. 2013;338:57-62.
10. Lim E, Wu D, Pal B, Bouras T, Asselin-Labat ML, Vaillant F, et al. Transcriptome analyses of mouse and human mammary cell subpopulations reveals multiple conserved genes and pathways. Breast Cancer Res. 2010;12:R21.
11. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010;140:62-73.
12. 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.
13. Regan JL, Kendrick H, Magnay FA, Vafaizadeh V, Groner B, Smalley MJ. c-Kit is required for growth and survival of the cells of origin of Brca1-mutation-associated breast cancer. Oncogene. 2012;31:869-83.
14. Sleeman KE, Kendrick H, Robertson D, Isacke CM, Ashworth A, Smalley MJ. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol. 2007;176:19-26.
15. Significance analysis of microarrays. [ http://www-stat.stanford.edu/~tibs/SAM/ ]
16. 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.
17. Sims D, Bursteinas B, Gao Q, Jain E, MacKay A, Mitsopoulos C, Zvelebil M. ROCK: a breast cancer functional genomics resource. Breast Cancer Res Treat. 2010;124(2):567-72. http://www.ncbi.nlm.nih.gov/pubmed/20563840.
18. Ng A, Bursteinas B, Gao Q, Mollison E, Zvelebil M. pSTIING: a 'systems' approach towards integrating signalling pathways, interaction and transcriptional regulatory networks in inflammation and cancer. Nucleic Acids Res. 2006;34:D527-34.
19. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
20. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
21. VENNY. An interactive tool for comparing lists with Venn Diagrams. [ http://bioinfogp.cnb.csic.es/tools/venny/index.html ]
22. Tan DW, Jensen KB, Trotter MW, Connelly JT, Broad S, Watt FM. Single-cell gene expression profiling reveals functional heterogeneity of undifferentiated human epidermal cells. Development. 2013;140:1433-44.
23. Deugnier MA, Faraldo MM, Teuliere J, Thiery JP, Medina D, Glukhova MA. Isolation of mouse mammary epithelial progenitor cells with basal characteristics from the Comma-Dbeta cell line. Dev Biol. 2006;293:414-25.
24. Karn T, Pusztai L, Holtrich U, Iwamoto T, Shiang CY, Schmidt M, et al. Homogeneous datasets of triple negative breast cancers enable the identification of novel prognostic and predictive signatures. PLoS One. 2011;6:e28403.
25. de Rinaldis E, Gazinska P, Mera A, Modrusan Z, Fedorowicz GM, Burford B, et al. Integrated genomic analysis of triple-negative breast cancers reveals novel microRNAs associated with clinical and molecular phenotypes and sheds light on the pathways they control. BMC Genomics. 2013;14:643.
26. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121:2750-67.
27. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 2007;8:118-27.
28. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, et al. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med. 2002;347:1999-2009.
29. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B, et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res. 2007;13:3207-14.
30. Sotiriou C, Wirapati P, Loi S, Harris A, Fox S, Smeds J, et al. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst. 2006;98:262-72.
31. Jiao Y, Lawler K, Patel GS, Purushotham A, Jones AF, Grigoriadis A, et al. DART: Denoising Algorithm based on Relevance network Topology improves molecular pathway activity inference. BMC Bioinformatics. 2011;12:403.
32. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27:1160-7.
33. Chen X, Li J, Gray WH, Lehmann BD, Bauer JA, Shyr Y, et al. TNBCtype: a subtyping tool for triple-negative breast cancer. Cancer Inform. 2012;11:147-56.
34. Burstein MD, Tsimelzon A. Poage GM. Contreras A, Fuqua S, et al. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res: Covington KR; 2014.
35. R-project. [ http://www.r-project.org/ ]
36. Britt KL, Kendrick H, Regan JL, Molyneux G, Magnay FA, Ashworth A, et al. Pregnancy in the mature adult mouse does not alter the proportion of mammary epithelial stem/progenitor cells. Breast Cancer Res. 2009;11:R20.
37. Molyneux G, Geyer FC, Magnay FA, McCarthy A, Kendrick H, Natrajan R, et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell. 2010;7:403-17.
38. Mansson R, Hultquist A, Luc S, Yang L, Anderson K, Kharazi S, et al. Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors. Immunity. 2007;26:407-19.
39. Spike BT, Engle DD, Lin JC, Cheung SK, La J, Wahl GM. A mammary stem cell population identified and characterized in late embryogenesis reveals similarities to human breast cancer. Cell Stem Cell. 2012;10:183-97.
40. Wansbury O, Mackay A, Kogata N, Mitsopoulos C, Kendrick H, Davidson K, et al. Transcriptome analysis of embryonic mammary cells reveals insights into mammary lineage establishment. Breast Cancer Res. 2011;13:R79.
41. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E. NFATc1 balances quiescence and proliferation of skin stem cells. Cell. 2008;132:299-310.
42. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 2009;138:592-603.
43. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell. 2008;2:333-44.
44. Frings O, Augsten M, Tobin NP, Carlson J, Paulsson J, Pena C, et al. Prognostic significance in breast cancer of a gene signature capturing stromal PDGF signaling. Am J Pathol. 2013;182:2037-47.
45. Hope KJ, Cellot S, Ting SB, MacRae T, Mayotte N, Iscove NN, et al. An RNAi screen identifies Msi2 and Prox1 as having opposite roles in the regulation of hematopoietic stem cell activity. Cell Stem Cell. 2010;7:101-13.
46. Ernst A, Hofmann S, Ahmadi R, Becker N, Korshunov A, Engel F, et al. Genomic and expression profiling of glioblastoma stem cell-like spheroid cultures identifies novel tumor-relevant genes associated with survival. Clin Cancer Res. 2009;15:6541-50.
47. Wang D, Cai C, Dong X, Yu QC, Zhang XO, Yang L, et al. Identification of multipotent mammary stem cells by protein C receptor expression. Nature. 2015;517:81-4.
48. Shan T, Liu W, Kuang S. Fatty acid binding protein 4 expression marks a population of adipocyte progenitors in white and brown adipose tissues. Faseb J. 2013;27:277-87.
49. Iliopoulos D, Hirsch HA, Wang G, Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci U S A. 2011;108:1397-402.
50. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704-15.
51. Smalley MJ, Titley J, O'Hare MJ. Clonal characterization of mouse mammary luminal epithelial and myoepithelial cells separated by fluorescence-activated cell sorting. In Vitro Cell Dev Biol Anim. 1998;34:711-21.
52. Smalley MJ. Clonal characterisation of mouse mammary luminal epithelial and myoepithelial cells. London: University of London; 1995.
53. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983-8.
54. Nakshatri H, Srour EF, Badve S. Breast cancer stem cells and intrinsic subtypes: controversies rage on. Curr Stem Cell Res Ther. 2009;4:50-60.
55. Haffty BG, Yang Q, Reiss M, Kearney T, Higgins SA, Weidhaas J, et al. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol. 2006;24:5652-7.
56. Reis-Filho JS, Pusztai L. Gene expression profiling in breast cancer: classification, prognostication, and prediction. Lancet. 2011;378:1812-23.
57. Sotiriou C, Pusztai L. Gene-expression signatures in breast cancer. N Engl J Med. 2009;360:790-800.
58. Irshad S, Grigoriadis A, Lawler K, Ng T, Tutt A. Profiling the immune stromal interface in breast cancer and its potential for clinical impact. Breast Care (Basel). 2012;7:273-80.
59. Lee U, Frankenberger C, Yun J, Bevilacqua E, Caldas C, Chin SF, et al. A prognostic gene signature for metastasis-free survival of triple negative breast cancer patients. PLoS One. 2013;8:e82125.
60. Al-Ejeh F, Simpson PT, Sanus JM, Klein K, Kalimutho M, Shi W, et al. Meta-analysis of the global gene expression profile of triple-negative breast cancer identifies genes for the prognostication and treatment of aggressive breast cancer. Oncogenesis. 2014;3:e100.
61. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13:4429-34.
62. SOURCE Database. [ http://smd.stanford.edu/cgi-bin/source/sourceSearch ]
63. Hill RP, Marie-Egyptienne DT, Hedley DW. Cancer stem cells, hypoxia and metastasis. Semin Radiat Oncol. 2009;19:106-11.
64. Wend P, Holland JD, Ziebold U, Birchmeier W. Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol. 2010;21:855-63.
65. Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell. 2010;6:568-77.
66. Meier-Abt F, Milani E, Roloff T, Brinkhaus H, Duss S, Meyer DS, et al. Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium. Breast Cancer Res. 2013;15:R36.
67. Lee H, Jung SY, Ro JY, Kwon Y, Sohn JH, Park IH, et al. Metaplastic breast cancer: clinicopathological features and its prognosis. J Clin Pathol. 2012;65:441-6.
68. Fulford LG, Easton DF, Reis-Filho JS, Sofronis A, Gillett CE, Lakhani SR, et al. Specific morphological features predictive for the basal phenotype in grade 3 invasive ductal carcinoma of breast. Histopathology. 2006;49:22-34.
69. Smalley MJ, Kendrick H, Sheridan JM, Regan JL, Prater MD, Lindeman GJ, et al. Isolation of mouse mammary epithelial subpopulations: a comparison of leading methods. J Mammary Gland Biol Neoplasia. 2012;17:91-7.
70. Rios AC, Fu NY, Lindeman GJ, Visvader JE. In situ identification of bipotent stem cells in the mammary gland. Nature. 2014;506:322-7.
71. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature. 2011;479:189-93.
72. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature. 2008;456:593-8.
73. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439:84-8.
74. Cumming G, Fidler F, Vaux DL. Error bars in experimental biology. J Cell Biol. 2007;177:7-11.