Breast cancer stem cells: Obstacles to therapy

Cancer Letters

Volumn 338, Issue 1, 2013, Pages 57-62

  Smalley, Matthew ^a   Piggott, Luke ^b   Clarkson, Richard ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Breast; Cancer stem cells; EMT; Plasticity

Indexed keywords

DOXORUBICIN; PACLITAXEL; VINCRISTINE;

BREAST CANCER; CANCER GROWTH; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CELL ACTIVITY; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL POPULATION; CELL SELECTION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; SURVIVAL TIME; TUMOR MICROENVIRONMENT;

EID: 84882870024     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.04.023     Document Type: Review

References (65)

1. Vermeulen L., de Sousa e Melo F., Richel D.J., Medema J.P. The developing cancer stem-cell model: clinical challenges and opportunities. Lancet Oncol 2012, 13:e83-e89.
2. Bomken S., Fiser K., Heidenreich O., Vormoor J. Understanding the cancer stem cell. British Journal of Cancer 2010, 103:439-445.
3. Liu S., Wicha M.S. Targeting breast cancer stem cells. Journal of Clinical Oncology 2010, 28:4006-4012.
4. Iliopoulos D., Hirsch H.A., Struhl K. Metformin decreases the dose of chemotherapy for prolonging tumor remission in mouse xenografts involving multiple cancer cell types. Cancer Research 2011, 71:3196-3201.
5. Pajic M., Kersbergen A., van Diepen F., Pfauth A., Jonkers J., Borst P., Rottenberg S. Tumor-initiating cells are not enriched in cisplatin-surviving BRCA1; p53-deficient mammary tumor cells in vivo. Cell Cycle 2010, 9:3780-3791.
6. Shafee N., Smith C.R., Wei S., Kim Y., Mills G.B., Hortobagyi G.N., Stanbridge E.J., Lee E.Y. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Cancer Research 2008, 68:3243-3250.
7. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., Wicha M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes and Development 2003, 17:1253-1270.
8. Dontu G., Al-Hajj M., Abdallah W.M., Clarke M.F., Wicha M.S. Stem cells in normal breast development and breast cancer. Cell Proliferation 2003, 36(Suppl 1):59-72.
9. Moraes R.C., Zhang X., Harrington N., Fung J.Y., Wu M.F., Hilsenbeck S.G., Allred D.C., Lewis M.T. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development (Cambridge, England) 2007, 134:1231-1242.
10. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., Jacquemier J., Viens P., Kleer C.G., Liu S., Schott A., Hayes D., Birnbaum D., Wicha M.S., Dontu G. 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.
11. Harrison H., Farnie G., Howell S.J., Rock R.E., Stylianou S., Brennan K.R., Bundred N.J., Clarke R.B. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Research 2010, 70:709-718.
12. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., Brooks M., Reinhard F., Zhang C.C., Shipitsin M., Campbell L.L., Polyak K., Brisken C., Yang J., Weinberg R.A. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
13. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008, 3:e2888.
14. Piggott L., Omidvar N., Perez S.M., Eberl M., Clarkson R.W. Suppression of apoptosis inhibitor c-FLIP selectively eliminates breast cancer stem cell activity in response to the anti-cancer agent. TRAIL Breast Cancer Research 2011, 13:R88.
15. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:3983-3988.
16. Lim E., Vaillant F., Wu D., Forrest N.C., Pal B., Hart A.H., Asselin-Labat M.L., Gyorki D.E., Ward T., Partanen A., Feleppa F., Huschtscha L.I., Thorne H.J., Fox S.B., Yan M., French J.D., Brown M.A., Smyth G.K., Visvader J.E., Lindeman G.J. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nature Medicine 2009, 15:907-913.
17. Proia T.A., Keller P.J., Gupta P.B., Klebba I., Jones A.D., Sedic M., Gilmore H., Tung N., Naber S.P., Schnitt S., Lander E.S., Kuperwasser C. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011, 8:149-163.
18. Molyneux G., Geyer F.C., Magnay F.A., McCarthy A., Kendrick H., Natrajan R., Mackay A., Grigoriadis A., Tutt A., Ashworth A., Reis-Filho J.S., Smalley M.J. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 2010, 7:403-417.
19. Tavassoli F.A., Devilee P. World health organisation classification of tumours. Tumors of the breast and femal genital organs 2003, IARC Press, Lyon. F. Lyon (Ed.).
20. Reis-Filho J.S., Milanezi F., Steele D., Savage K., Simpson P.T., Nesland J.M., Pereira E.M., Lakhani S.R., Schmitt F.C. Metaplastic breast carcinomas are basal-like tumours. Histopathology 2006, 49:10-21.
21. Greaves M., Maley C.C. Clonal evolution in cancer. Nature 2012, 481:306-313.
22. Anderson K., Lutz C., van Delft F.W., Bateman C.M., Guo Y., Colman S.M., Kempski H., Moorman A.V., Titley I., Swansbury J., Kearney L., Enver T., Greaves M. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 2011, 469:356-361.
23. Hay E.D. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Developmental Dynamics 2005, 233:706-720.
24. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nature Reviews Molecular and Cellular Biology 2006, 7:131-142.
25. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anatomica(Basel) 1995, 154:8-20.
26. Charafe-Jauffret E., Ginestier C., Iovino F., Wicinski J., Cervera N., Finetti P., Hur M.H., Diebel M.E., Monville F., Dutcher J., Brown M., Viens P., Xerri L., Bertucci F., Stassi G., Dontu G., Birnbaum D., Wicha M.S. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Research 2009, 69:1302-1313.
27. Asiedu M.K., Ingle J.N., Behrens M.D., Radisky D.C., Knutson K.L. TGFbeta/TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Research 2011, 71:4707-4719.
28. Chao Y.L., Shepard C.R., Wells A. Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition. Molecular Cancer 2010, 9:179.
29. Aslakson C.J., Miller F.R. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Research 1992, 52:1399-1405.
30. Scheel C., Weinberg R.A. Phenotypic plasticity and epithelial-mesenchymal transitions in cancer and normal stem cells?. International Journal of Cancer 2011, 129:2310-2314.
31. Drasin D.J., Robin T.P., Ford H.L. Breast cancer epithelial-to-mesenchymal transition: examining the functional consequences of plasticity. Breast Cancer Research 2011, 13:226.
32. Polyak K., Weinberg R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature Reviews 2009, 9:265-273.
33. Chaffer C.L., Brueckmann I., Scheel C., Kaestli A.J., Wiggins P.A., Rodrigues L.O., Brooks M., Reinhardt F., Su Y., Polyak K., Arendt L.M., Kuperwasser C., Bierie B., Weinberg R.A. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:7950-7955.
34. Iliopoulos D., Hirsch H.A., Wang G., Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:1397-1402.
35. Meyer M.J., Fleming J.M., Ali M.A., Pesesky M.W., Ginsburg E., Vonderhaar B.K. Dynamic regulation of CD24 and the invasive, CD44posCD24neg phenotype in breast cancer cell lines. Breast Cancer Research 2009, 11:R82.
36. Sarrio D., Franklin C.K., Mackay A., Reis-Filho J.S., Isacke C.M. Epithelial and mesenchymal subpopulations within normal basal breast cell lines exhibit distinct stem cell/progenitor properties. Stem Cells 2012, 30:292-303.
37. Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., Lander E.S. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644.
38. Guo W., Keckesova Z., Donaher J.L., Shibue T., Tischler V., Reinhardt F., Itzkovitz S., Noske A., Zurrer-Hardi U., Bell G., Tam W.L., Mani S.A., van Oudenaarden A., Weinberg R.A. Slug and sox9 cooperatively determine the mammary stem cell state. Cell 2012, 148:1015-1028.
39. Li X., Lewis M.T., Huang J., Gutierrez C., Osborne C.K., Wu M.F., Hilsenbeck S.G., Pavlick A., Zhang X., Chamness G.C., Wong H., Rosen J., Chang J.C. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. Journal of the National Cancer Institute 2008, 100:672-679.
40. Yang M.H., Wu M.Z., Chiou S.H., Chen P.M., Chang S.Y., Liu C.J., Teng S.C., Wu K.J. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nature Cell Biology 2008, 10:295-305.
41. Zielske S.P., Spalding A.C., Wicha M.S., Lawrence T.S. Ablation of breast cancer stem cells with radiation. Translational Oncology 2011, 4:227-233.
42. Santisteban M., Reiman J.M., Asiedu M.K., Behrens M.D., Nassar A., Kalli K.R., Haluska P., Ingle J.N., Hartmann L.C., Manjili M.H., Radisky D.C., Ferrone S., Knutson K.L. Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Research 2009, 69:2887-2895.
43. Liu S., Ginestier C., Ou S.J., Clouthier S.G., Patel S.H., Monville F., Korkaya H., Heath A., Dutcher J., Kleer C.G., Jung Y., Dontu G., Taichman R., Wicha M.S. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Research 2011, 71:614-624.
44. McDermott S.P., Wicha M.S. Targeting breast cancer stem cells. Molecular Oncology 2010, 4:404-419.
45. Hardy K.M., Booth B.W., Hendrix M.J., Salomon D.S., Strizzi L. ErbB/EGF signaling and EMT in mammary development and breast cancer. Journal of Mammary Gland Biology and Neoplasia 2010, 15:191-199.
46. Yook J.I., Li X.Y., Ota I., Hu C., Kim H.S., Kim N.H., Cha S.Y., Ryu J.K., Choi Y.J., Kim J., Fearon E.R., Weiss S.J. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nature Cell Biology 2006, 8:1398-1406.
47. Leong K.G., Niessen K., Kulic I., Raouf A., Eaves C., Pollet I., Karsan A. Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. The Journal of Experimental Medicine 2007, 204:2935-2948.
48. Kasper M., Jaks V., Fiaschi M., Toftgard R. Hedgehog signalling in breast cancer. Carcinogenesis 2009, 30:903-911.
49. Yu F., Yao H., Zhu P., Zhang X., Pan Q., Gong C., Huang Y., Hu X., Su F., Lieberman J., Song E. Let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007, 131:1109-1123.
50. Phillips T.M., McBride W.H., Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. Journal of the National Cancer Institute 2006, 98:1777-1785.
51. Patrawala L., Calhoun T., Schneider-Broussard R., Zhou J., Claypool K., Tang D.G. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Research 2005, 65:6207-6219.
52. Farnie G., Clarke R.B., Spence K., Pinnock N., Brennan K., Anderson N.G., Bundred N.J. Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways. Journal of the National Cancer Institute 2007, 99:616-627.
53. Sajithlal G.B., Rothermund K., Zhang F., Dabbs D.J., Latimer J.J., Grant S.G., Prochownik E.V. Permanently blocked stem cells derived from breast cancer cell lines. Stem Cells 2010, 28:1008-1018.
54. Woodward W.A., Chen M.S., Behbod F., Alfaro M.P., Buchholz T.A., Rosen J.M. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:618-623.
55. Creighton C.J., Li X., Landis M., Dixon J.M., Neumeister V.M., Sjolund A., Rimm D.L., Wong H., Rodriguez A., Herschkowitz J.I., Fan C., Zhang X., He X., Pavlick A., Gutierrez M.C., Renshaw L., Larionov A.A., Faratian D., Hilsenbeck S.G., Perou C.M., Lewis M.T., Rosen J.M., Chang J.C. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:13820-13825.
56. Li Q.Q., Xu J.D., Wang W.J., Cao X.X., Chen Q., Tang F., Chen Z.Q., Liu X.P., Xu Z.D. Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clinical Cancer Research 2009, 15:2657-2665.
57. O'Brien C.S., Howell S.J., Farnie G., Clarke R.B. Resistance to endocrine therapy: are breast cancer stem cells the culprits?. Journal of Mammary Gland Biology and Neoplasia 2009, 14:45-54.
58. Fillmore C.M., 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 Research 2008, 10:R25.
59. Hiscox S., Jiang W.G., Obermeier K., Taylor K., Morgan L., Burmi R., Barrow D., Nicholson R.I. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation. International Journal of Cancer 2006, 118:290-301.
60. Fehm T., Krawczyk N., Solomayer E.F., Becker-Pergola G., Durr-Storzer S., Neubauer H., Seeger H., Staebler A., Wallwiener D., Becker S. ERalpha-status of disseminated tumour cells in bone marrow of primary breast cancer patients. Breast Cancer Research 2008, 10:R76.
61. Ye Y., Xiao Y., Wang W., Yearsley K., Gao J.X., Barsky S.H. ERalpha suppresses slug expression directly by transcriptional repression. The Biochemical Journal 2008, 416:179-187.
62. Hirsch H.A., Iliopoulos D., Tsichlis P.N., Struhl K. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Research 2009, 69:7507-7511.
63. E.A. Eisenhauer, P. Therasse, J. Bogaerts, L.H. Schwartz, D. Sargent, R. Ford, J. Dancey, S. Arbuck, S. Gwyther, M. Mooney, L. Rubinstein, L. Shankar, L. Dodd, R. Kaplan, D. Lacombe, J. Verweij, New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1), European Journal of Cancer, 45 (2009) 228-247 (Oxford, England).
64. Huff C.A., Matsui W.H., Smith B.D., Jones R.J. Strategies to eliminate cancer stem cells: clinical implications. European Journal of Cancer 2006, 42:1293-1297. (Oxford, England).
65. Adjei A.A., Christian M., Ivy P. Novel designs and end points for phase II clinical trials. Clinical Cancer Research 2009, 15:1866-1872.