Tissue-based identification of stem cells and epithelial-to-mesenchymal transition in breast cancer

Human Pathology

Volumn 44, Issue 8, 2013, Pages 1457-1464

  Anwar, Talha E ^a   Kleer, Celina G ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

ALDH1; CD44; EMT; Epithelial to mesenchymal transition; Metastasis; Stem cells

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOFORM 1 PROTEIN; CD24 ANTIGEN; CELL ADHESION MOLECULE; HERMES ANTIGEN; MICRORNA; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BREAST BIOPSY; BREAST CANCER; CANCER CELL; CANCER DIAGNOSIS; CANCER RISK; CANCER STEM CELL; CELL ISOLATION; CELL SURFACE; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INVASIVE CARCINOMA; MIGRATION; PROTEIN EXPRESSION; STROMA CELL;

ALDH1; CD44; EMT; EPITHELIAL-TO-MESENCHYMAL TRANSITION; METASTASIS; STEM CELLS;

ANIMALS; BREAST NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; NEOPLASTIC STEM CELLS;

EID: 84880326175     PISSN: 00468177     EISSN: 15328392     Source Type: Journal    
DOI: 10.1016/j.humpath.2013.01.005     Document Type: Article

References (68)

1. S.A. Mani, W. Guo, and M.J. Liao The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
2. A.P. Morel, M. Lievre, C. Thomas, G. Hinkal, S. Ansieau, and A. Puisieux Generation of breast cancer stem cells through epithelial-mesenchymal transition PLoS One 3 2008 e2888
3. M.A. Nieto The ins and outs of the epithelial to mesenchymal transition in health and disease Annu Rev Cell Dev Biol 27 2011 347 376
4. C.J. Creighton, J.C. Chang, and J.M. Rosen Epithelial-mesenchymal transition (EMT) in tumor-initiating cells and its clinical implications in breast cancer J Mammary Gland Biol Neoplasia 15 2010 253 260
5. X. Li, M.T. Lewis, and J. Huang Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy J Natl Cancer Inst 100 2008 672 679
6. T.M. Phillips, W.H. McBride, and F. Pajonk The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation J Natl Cancer Inst 98 2006 1777 1785
7. M. Balic, H. Lin, and L. Young Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype Clin Cancer Res 12 2006 5615 5621
8. M. Kakarala, and M.S. Wicha Implications of the cancer stem-cell hypothesis for breast cancer prevention and therapy J Clin Oncol 26 2008 2813 2820
9. C. Ginestier, M.H. Hur, and E. Charafe-Jauffret ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 1 2007 555 567
10. R. Liu, X. Wang, and G.Y. Chen The prognostic role of a gene signature from tumorigenic breast-cancer cells N Engl J Med 356 2007 217 226
11. 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
12. J. Stingl, P. Eirew, and I. Ricketson Purification and unique properties of mammary epithelial stem cells Nature 439 2006 993 997
13. M. Shackleton, F. Vaillant, and K.J. Simpson Generation of a functional mammary gland from a single stem cell Nature 439 2006 84 88
14. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc Natl Acad Sci U S A 100 2003 3983 3988
15. [No authors] Julius Cohnheim (1839-1884) experimental pathologist JAMA 206 1968 1561 1562
16. G. Dontu, W.M. Abdallah, and J.M. Foley In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells Genes Dev 17 2003 1253 1270
17. R. Kalluri EMT: when epithelial cells decide to become mesenchymal-like cells J Clin Invest 119 2009 1417 1419
18. L. Vicovac, and J.D. Aplin Epithelial-mesenchymal transition during trophoblast differentiation Acta Anat (Basel) 156 1996 202 216
19. S. Yamakoshi, R. Bai, and T. Chaen Expression of mesenchymal-related genes by the bovine trophectoderm following conceptus attachment to the endometrial epithelium Reproduction 143 2012 377 387
20. M.A. Nieto Epithelial-mesenchymal transitions in development and disease: old views and new perspectives Int J Dev Biol 53 2009 1541 1547
21. E.D. Hay An overview of epithelio-mesenchymal transformation Acta Anat (Basel) 154 1995 8 20
22. R. Kalluri, and R.A. Weinberg The basics of epithelial-mesenchymal transition J Clin Invest 119 2009 1420 1428
23. H. Hugo, M.L. Ackland, and T. Blick Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression J Cell Physiol 213 2007 374 383
24. J.P. Thiery, H. Acloque, R.Y. Huang, and M.A. Nieto Epithelial- mesenchymal transitions in development and disease Cell 139 2009 871 890
25. O. Schmalhofer, S. Brabletz, and T. Brabletz E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer Cancer Metastasis Rev 28 2009 151 166
26. D.S. Micalizzi, S.M. Farabaugh, and H.L. Ford Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression J Mammary Gland Biol Neoplasia 15 2010 117 134
27. A.J. Trimboli, K. Fukino, and A. de Bruin Direct evidence for epithelial-mesenchymal transitions in breast cancer Cancer Res 68 2008 937 945
28. E. Tomaskovic-Crook, E.W. Thompson, and J.P. Thiery Epithelial to mesenchymal transition and breast cancer Breast Cancer Res 11 2009 213
29. J.P. Thiery Epithelial-mesenchymal transitions in tumour progression Nat Rev Cancer 2 2002 442 454
30. U. Burk, J. Schubert, and U. Wellner A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells EMBO Rep 9 2008 582 589
31. T.R. Graham, H.E. Zhau, and V.A. Odero-Marah Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells Cancer Res 68 2008 2479 2488
32. S.E. Moody, D. Perez, and T.C. Pan The transcriptional repressor Snail promotes mammary tumor recurrence Cancer Cell 8 2005 197 209
33. J.I. Yook, X.Y. Li, and I. Ota A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells Nat Cell Biol 8 2006 1398 1406
34. E. Batlle, E. Sancho, and C. Franci The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells Nat Cell Biol 2 2000 84 89
35. A. Cano, M.A. Perez-Moreno, and I. Rodrigo The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat Cell Biol 2 2000 76 83
36. C. Vandewalle, F. Van Roy, and G. Berx The role of the ZEB family of transcription factors in development and disease Cell Mol Life Sci 66 2009 773 787
37. M.L. Grooteclaes, and S.M. Frisch Evidence for a function of CtBP in epithelial gene regulation and anoikis Oncogene 19 2000 3823 3828
38. S. Guaita, I. Puig, and C. Franci Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression J Biol Chem 277 2002 39209 39216
39. A. Eger, K. Aigner, and S. Sonderegger DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells Oncogene 24 2005 2375 2385
40. S. Spaderna, O. Schmalhofer, and M. Wahlbuhl The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer Cancer Res 68 2008 537 544
41. H.L. Chua, P. Bhat-Nakshatri, S.E. Clare, A. Morimiya, S. Badve, and H. Nakshatri NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2 Oncogene 26 2007 711 724
42. C.P. Bracken, P.A. Gregory, and N. Kolesnikoff A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition Cancer Res 68 2008 7846 7854
43. M. Korpal, E.S. Lee, G. Hu, and Y. Kang The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2 J Biol Chem 283 2008 14910 14914
44. W. Huang, Y. Zhang, and S. Varambally Inhibition of CCN6 (Wnt-1-induced signaling protein 3) down-regulates E-cadherin in the breast epithelium through induction of snail and ZEB1 Am J Pathol 172 2008 893 904
45. Y. Zhang, Q. Pan, H. Zhong, S.D. Merajver, and C.G. Kleer Inhibition of CCN6 (WISP3) expression promotes neoplastic progression and enhances the effects of insulin-like growth factor-1 on breast epithelial cells Breast Cancer Res 7 2005 R1080 R1089
46. W. Huang, A. Pal, and C.G. Kleer On how CCN6 suppresses breast cancer growth and invasion J Cell Commun Signal 6 2012 5 10
47. T. Blick, H. Hugo, and E. Widodo 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 15 2010 235 252
48. J.H. Taube, J.I. Herschkowitz, and K. Komurov Core epithelial-to- mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes Proc Natl Acad Sci U S A 107 2010 15449 15454
49. C. Scheel, and R.A. Weinberg Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links Semin Cancer Biol 22 2012 396 403
50. L.P. Kunju, C. Cookingham, K.A. Toy, W. Chen, M.S. Sabel, and C.G. Kleer EZH2 and ALDH-1 mark breast epithelium at risk for breast cancer development Mod Pathol 24 2011 786 793
51. S. Deng, X. Yang, and H. Lassus Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers PLoS One 5 2010 e10277
52. E. Charafe-Jauffret, C. Ginestier, and F. lovino Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer Clin Cancer Res 16 2010 45 55
53. E. Resetkova, J.S. Reis-Filho, and R.K. Jain Prognostic impact of ALDH1 in breast cancer: a story of stem cells and tumor microenvironment Breast Cancer Res Treat 123 2010 97 108
54. G. Kristiansen, K.J. Winzer, and E. Mayordomo CD24 expression is a new prognostic marker in breast cancer Clin Cancer Res 9 2003 4906 4913
55. D. Jackson, R. Waibel, E. Weber, J. Bell, and R.A. Stahel CD24, a signal-transducing molecule expressed on human B cells, is a major surface antigen on small cell lung carcinomas Cancer Res 52 1992 5264 5270
56. S. Aigner, Z.M. Sthoeger, and M. Fogel CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells Blood 89 1997 3385 3395
57. G. Honeth, P.O. Bendahl, and M. Ringner The CD44+/CD24- phenotype is enriched in basal-like breast tumors Breast Cancer Res 10 2008 R53
58. + tumor cells in invasive breast carcinomas Hum Pathol 39 2008 1096 1102
59. Y. Zhang, K.A. Toy, and C.G. Kleer Metaplastic breast carcinomas are enriched in markers of tumor-initiating cells and epithelial to mesenchymal transition Mod Pathol 25 2012 178 184
60. S. Liu, S.G. Clouthier, and M.S. Wicha Role of microRNAs in the regulation of breast cancer stem cells J Mammary Gland Biol Neoplasia 17 2012 15 21
61. T.J. Liu, B.C. Sun, and X.L. Zhao CD133(+) cells with cancer stem cell characteristics associates with vasculogenic mimicry in triple-negative breast cancer Oncogene 3 17 2013 544 553
62. M.H. Wright, A.M. Calcagno, C.D. Salcido, M.D. Carlson, S.V. Ambudkar, and L. Varticovski Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics Breast Cancer Res 10 2008 R10
63. Z.Q. Wu, X.Y. Li, C.Y. Hu, M. Ford, C.G. Kleer, and S.J. Weiss Canonical Wnt signaling regulates Slug activity and links epithelial-mesenchymal transition with epigenetic Breast Cancer 1, Early Onset (BRCA1) repression Proc Natl Acad Sci U S A 109 2012 16654 16659
64. H. Oka, H. Shiozaki, and K. Kobayashi Expression of E-cadherin cell adhesion molecules in human breast cancer tissues and its relationship to metastasis Cancer Res 53 1993 1696 1701
65. K. Aigner, B. Dampier, and L. Descovich The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity Oncogene 26 2007 6979 6988
66. D. Sarrio, S.M. Rodriguez-Pinilla, D. Hardisson, A. Cano, G. Moreno-Bueno, and J. Palacios Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype Cancer Res 68 2008 989 997
67. V. Kumar, A. Abbas, N. Fausto, and J. Aster Robbins and Cotran Pathologic Basis of Disease 8th ed 2010 Elsevier
68. M. Mego, H. Gao, and B.N. Lee Prognostic value of EMT-circulating tumor cells in metastatic breast cancer patients undergoing high-dose chemotherapy with autologous hematopoietic stem cell transplantation J Cancer 3 2012 369 380