Implications of stemness-related signaling pathways in breast cancer response to therapy

Seminars in Cancer Biology

Volumn 31, Issue , 2015, Pages 43-51

  Angeloni, Valentina ^a   Tiberio, Paola ^a   Appierto, Valentina ^a   Daidone, Maria Grazia ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Breast cancer initiating cell; Stemness marker; Stemness pathway; Targeted therapy; Treatment response

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD24 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HERMES ANTIGEN; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; STAT3 PROTEIN; TUMOR MARKER; WNT PROTEIN; ANTINEOPLASTIC AGENT;

APOPTOSIS; BREAST CANCER INITIATING CELL; CANCER RESISTANCE; CANCER STEM CELL; CELL FUNCTION; CELL POPULATION; CELL RENEWAL; CELL SURVIVAL; HUMAN; MOLECULAR INTERACTION; MOLECULARLY TARGETED THERAPY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; DISEASE COURSE; DRUG EFFECTS; METABOLISM; MOUSE; PATHOLOGY; PROCEDURES;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BREAST NEOPLASMS; DISEASE PROGRESSION; HUMANS; MICE; MOLECULAR TARGETED THERAPY; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84923211164     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.08.004     Document Type: Review

References (125)

1. Arteaga C.L. Progress in breast cancer: overview. Clin Cancer Res 2013, 19:6353-6359. 10.1158/1078-0432.CCR-13-2549.
2. Pinto C.A., Widodo E., Waltham M., Thompson E.W. Breast cancer stem cells and epithelial mesenchymal plasticity - implications for chemoresistance. Cancer Lett 2013, 341:56-62. 10.1016/j.canlet.2013.06.003.
3. Mannello F. Understanding breast cancer stem cell heterogeneity: time to move on to a new research paradigm. BMC Med 2013, 11:169. 10.1186/1741-7015-11-169.
4. Velasco-Velázquez M.A., Homsi N., De La Fuente M., Pestell R.G. Breast cancer stem cells. Int J Biochem Cell Biol 2012, 44:573-577. 10.1016/j.biocel.2011.12.020.
5. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100:3983-3988.
6. Williams S.A., Anderson W.C., Santaguida M.T., Dylla S.J. Patient-derived xenografts, the cancer stem cell paradigm, and cancer pathobiology in the 21st century. Lab Invest 2013, 93:970-982. 10.1038/labinvest.2013.92.
7. Croker A.K., Allan A.L. Cancer stem cells: implications for the progression and treatment of metastatic disease. J Cell Mol Med 2008, 12:374-390.
8. Alison M.R., Lin W.R., Lim S.M., Nicholson L.J. Cancer stem cells: in the line of fire. Cancer Treat Rev 2012, 38:589-598. 10.1016/j.ctrv.2012.03.003.
9. Balic M., Lin H., Young L., Hawes D., Giuliano A., McNamara G., et al. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 2006, 12:5615-5621.
10. Dick J.E. Acute myeloid leukemia stem cells. Ann N Y Acad Sci 2005, 1044:1-5.
11. Dalerba P., Cho R.W., Clarke M.F. Cancer stem cells: models and concepts. Annu Rev Med 2007, 58:267-284.
12. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003, 17:1253-1270.
13. Ponti D., Costa A., Zaffaroni N., Pratesi G., Petrangolini G., Coradini D., et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005, 65:5506-5511.
14. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., 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. 10.1016/j.stem.2007.08.014.
15. Huang E.H., Hynes M.J., Zhang T., Ginestier C., Dontu G., Appelman H., et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009, 69:3382-3389. 10.1158/0008-5472.CAN-08-4418.
16. Jiang F., Qiu Q., Khanna A., Todd N.W., Deepak J., Xing L., et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009, 7:330-338. 10.1158/1541-7786.MCR-08-0393.
17. Liu S., Cong Y., Wang D., Sun Y., Deng L., Liu Y., et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Rep 2013, 2:78-91. 10.1016/j.stemcr.2013.11.009.
18. Conley S.J., Gheordunescu E., Kakarala P., Newman B., Korkaya H., Heath A.N., et al. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci U S A 2012, 109:2784-2789. 10.1073/pnas.1018866109.
19. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027.
20. Creighton C.J., Li X., Landis M., Dixon J.M., Neumeister V.M., Sjolund A., et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci U S A 2009, 106:13820-13825. 10.1073/pnas.0905718106.
21. 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, 10.1371/journal.pone.0002888.
22. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008, 14:818-829. 10.1016/j.devcel.2008.05.009.
23. Shin S.Y., Rath O., Zebisch A., Choo S.M., Kolch W., Cho K.H. Functional roles of multiple feedback loops in extracellular signal-regulated kinase and Wnt signaling pathways that regulate epithelial-mesenchymal transition. Cancer Res 2010, 70:6715-6724. 10.1158/0008-5472.CAN-10-1377.
24. Yoo Y.A., Kang M.H., Lee H.J., Kim B.H., Park J.K., Kim H.K., et al. Sonic hedgehog pathway promotes metastasis and lymphangiogenesis via activation of Akt, EMT, and MMP-9 pathway in gastric cancer. Cancer Res 2011, 71:7061-7070. 10.1158/0008-5472.CAN-11-1338.
25. Biddle A., Liang X., Gammon L., Fazil B., Harper L.J., Emich H., et al. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res 2011, 1(71):5317-5326. 10.1158/0008-5472.CAN-11-1059.
26. Thompson E.W., Haviv I. The social aspects of EMT-MET plasticity. Nat Med 2011, 17:1048-1049. 10.1038/nm.2437.
27. Klevebring D., Rosin G., Ma R., Lindberg J., Czene K., Kere J., et al. Sequencing of breast cancer stem cell populations indicates a dynamic conversion between differentiation states in vivo. Breast Cancer Res 2014, 16(4):R72.
28. Chaffer C.L., Brueckmann I., Scheel C., Kaestli A.J., Wiggins P.A., Rodrigues L.O., et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci U S A 2011, 108:7950-7955. 10.1073/pnas.1102454108.
29. Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011, 146:633-644. 10.1016/j.cell.07.026.
30. Li X., Lewis M.T., Huang J., Gutierrez C., Osborne C.K., Wu M.F., et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679. 10.1093/jnci/djn123.
31. Lee H.E., Kim J.H., Kim Y.J., Choi S.Y., Kim S.W., Kang E., et al. An increase in cancer stem cell population after primary systemic therapy is a poor prognostic factor in breast cancer. Br J Cancer 2011, 104:1730-1738. 10.1038/bjc.2011.
32. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
33. Abdullah L.N., Chow E. Mechanisms of chemoresistance in cancer stem cells. Clin Transl Med 2013, 2. 10.1186/2001-1326-2-3.
34. 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 Res 2008, 10:R25. 10.1186/bcr1982.
35. Calcagno A.M., Salcido C.D., Gillet J.P., Wu C.P., Fostel J.M., Mumau M.D., et al. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. J Natl Cancer Inst 2010, 102:1637-1652. 10.1093/jnci/djq361.
36. Li H.Z., Yi T.B., Wu Z.Y. Suspension culture combined with chemotherapeutic agents for sorting of breast cancer stem cells. BMC Cancer 2008, 8:135. 10.1186/1471-2407-8-135.
37. Yu F., Yao H., Zhu P., Zhang X., Pan Q., Gong C., et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007, 131:1109-1123.
38. Tanei T., Morimoto K., Shimazu K., Kim S.J., Tanji Y., Taguchi T., et al. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 2009, 15:4234-4241. 10.1158/1078-0432.
39. Kabos P., Haughian J.M., Wang X., Dye W.W., Finlayson C., Elias A., et al. Cytokeratin 5 positive cells represent a steroid receptor negative and therapy resistant subpopulation in luminal breast cancers. Breast Cancer Res Treat 2011, 128:45-55. 10.1007/s10549-010-1078-6.
40. Phillips T.M., McBride W.H., Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 98:1777-1785.
41. Lagadec C., Vlashi E., Della Donna L., Meng Y., Dekmezian C., Kim K., et al. Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 2010, 12:R13. 10.1186/bcr2479.
42. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783. 10.1038/nature07733.
43. Olsson E., Honeth G., Bendahl P.O., Saal L.H., Gruvberger-Saal S., Ringnér M., et al. CD44 isoforms are heterogeneously expressed in breast cancer and correlate with tumor subtypes and cancer stem cell markers. BMC Cancer 2011, 11:418. 10.1186/1471-2407-11-418.
44. Ababneh N., Alshaer W., Allozi O., Mahafzah A., El-Khateeb M., Hillaireau H., et al. In vitro selection of modified RNA aptamers against CD44 cancer stem cell marker. Nucleic Acid Ther 2013, 23:401-407. 10.1089/nat.2013.0423.
45. Deleo A.B. Targeting cancer stem cells with ALDH1A1-based immunotherapy. Oncoimmunology 2012, 1:385-387. 10.4161/onci.18826.
46. Malhotra G.K., Zhao X., Band H., Band V. Shared signaling pathways in normal and breast cancer stem cells. J Carcinog 2011, 10:38. 10.4103/1477-3163.91413.
47. Farnie G., Clarke R.B., Spence K., Pinnock N., Brennan K., Anderson N.G., et al. Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst 2007, 99:616-627.
48. Stylianou S., Clarke R.B., Brennan K. Aberrant activation of notch signaling in human breast cancer. Cancer Res 2006, 66:1517-1525.
49. Grudzien P., Lo S., Albain K.S., Robinson P., Rajan P., Strack P.R., et al. Inhibition of notch signaling reduces the stem-like population of breast cancer cells and prevents mammosphere formation. Anticancer Res 2010, 30:3853-3867.
50. Harrison H., Farnie G., Howell S.J., Rock R.E., Stylianou S., Brennan K.R., et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res 2010, 70:709-718. 10.1158/0008-5472.CAN-09-1681.
51. Clementz A.G., Rogowski A., Pandya K., Miele L., Osipo C. NOTCH-1 and NOTCH-4 are novel gene targets of PEA3 in breast cancer: novel therapeutic implications. Breast Cancer Res 2011, 13:R63. 10.1186/bcr2900.
52. Qiu M., Peng Q., Jiang I., Carroll C., Han G., Rymer I., et al. Specific inhibition of Notch1 signaling enhances the antitumor efficacy of chemotherapy in triple negative breast cancer through reduction of cancer stem cells. Cancer Lett 2013, 328:261-270. 10.1016/j.canlet.2012.09.023.
53. Schott A.F., Landis M.D., Dontu G., Griffith K.A., Layman R.M., Krop I., et al. Preclinical and clinical studies of gamma secretase inhibitors with docetaxel on human breast tumors. Clin Cancer Res 2013, 19:1512-1524. 10.1158/1078-0432.CCR-11-3326.
54. Olsauskas-Kuprys R., Zlobin A., Osipo C. Gamma secretase inhibitors of Notch signaling. Onco Targets Ther 2013, 6:943-955. 10.2147/OTT.S33766.
55. Zhang C.C., Pavlicek A., Zhang Q., Lira M.E., Painter C.L., Yan Z., et al. Biomarker and pharmacologic evaluation of the γ-secretase inhibitor PF-03084014 in breast cancer models. Clin Cancer Res 2012, 18:5008-5019. 10.1158/1078-0432.CCR-12-1379.
56. Suman S., Das T.P., Damodaran C. Silencing NOTCH signaling causes growth arrest in both breast cancer stem cells and breast cancer cells. Br J Cancer 2013, 109:2587-2596. 10.1038/bjc.2013.642.
57. Magnifico A., Albano L., Campaner S., Delia D., Castiglioni F., Gasparini P., et al. Tumor initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res 2009, 15:2010-2021. 10.1158/1078-0432.CCR-08-1327.
58. Miele L. Notch signaling. Clin Cancer Res 2006, 12:1074-1079.
59. Osipo C., Patel P., Rizzo P., Clementz A.G., Hao L., Golde T.E., et al. ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a gamma-secretase inhibitor. Oncogene 2008, 27:5019-5032. 10.1038/onc.2008.149.
60. Harrison H., Farnie G., Brennan K.R., Clarke R.B. Breast cancer stem cells: something out of notching?. Cancer Res 2010, 70:8973-8976. 10.1158/0008-5472.CAN-10-1559.
61. Pandya K., Meeke K., Clementz A.G., Rogowski A., Roberts J., Miele L., et al. Targeting both Notch and ErbB-2 signalling pathways is required for prevention of ErbB-2-positive breast tumour recurrence. Br J Cancer 2011, 105:796-806. 10.1038/bjc.2011.321.
62. Rizzo P., Miao H., D'Souza G., Osipo C., Song L.L., Yun J., et al. Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches. Cancer Res 2008, 68:5226-5235. 10.1158/0008-5472.CAN-07-5744.
63. King T.D., Suto M.J., Li Y. The Wnt/β-catenin signaling pathway: a potential therapeutic target in the treatment of triple negative breast cancer. J Cell Biochem 2012, 113(1):13-18. 10.1002/jcb.23350.
64. Smalley M.J., Dale T.C. Wnt signaling and mammary tumorigenesis. J Mammary Gland Biol Neoplasia 2001, 6:37-52.
65. Tepera S.B., McCrea P.D., Rosen J.M. A beta-catenin survival signal is required for normal lobular development in the mammary gland. J Cell Sci 2003, 116:1137-1149.
66. Li Y., Welm B., Podsypanina K., Huang S., Chamorro M., Zhang X., et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci U S A 2003, 100:15853-15858.
67. Liu B.Y., McDermott S.P., Khwaja S.S., Alexander C.M. The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells. Proc Natl Acad Sci U S A 2004, 101:4158-4163.
68. Lindvall C., Evans N.C., Zylstra C.R., Li Y., Alexander C.M., Williams B.O. The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J Biol Chem 2006, 281:35081-35087.
69. Kakarala M., Brenner D.E., Korkaya H., Cheng C., Tazi K., Ginestier C., et al. Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res Treat 2010, 122:777-785. 10.1007/s10549-009-0612-x.
70. Li Y., Zhang T., Korkaya H., Liu S., Lee H.F., Newman B., et al. a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 2010, 16:2580-2590. 10.1158/1078-0432.CCR-09-2937.
71. Lu D., Choi M.Y., Yu J., Castro J.E., Kipps T.J., Carson D.A. Salinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cells. Proc Natl Acad Sci U S A 2011, 108:13253-13257. 10.1073/pnas.1110431108.
72. Gupta P.B., Onder T.T., Tao JiangG., Kuperwasser K., Weinberg C., Lander R.A.E.S. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659. 10.1016/j.cell.2009.06.034.
73. Xu Y., Wang J., Li X., Liu Y., Dai L., Wu X., et al. Selective inhibition of breast cancer stem cells by gold nanorods mediated plasmonic hyperthermia. Biomaterials 2014, 35:4667-4677. 10.1016/j.biomaterials.2014.02.035.
74. Ramírez A., Boulaiz H., Morata-Tarifa C., Perán M., Jiménez G., Picon-Ruiz M., et al. HER2-signaling pathway, JNK and ERKs kinases, and cancer stem-like cells are targets of Bozepinib small compound. Oncotarget 2014, 5:3590-3606.
75. Lewis M.T., Veltmaat J.M. Next stop, the twilight zone: hedgehog network regulation of mammary gland development. J Mammary Gland Biol Neoplasia 2004, 9:165-181.
76. Tanaka H., Nakamura M., Kameda C., Kubo M., Sato N., Kuroki S., et al. The Hedgehog signaling pathway plays an essential role in maintaining the CD44+ CD24-/low subpopulation and the side population of breast cancer cells. Anticancer Res 2009, 29:2147-2157.
77. Fiaschi M., Rozell B., Bergstrom A., Toftgard R. Development of mammary tumors by conditional expression of GLI1. Cancer Res 2009, 69:4810-4817. 10.1158/0008-5472.CAN-08-3938.
78. Ng J.M., Curran T. The Hedgehog's tale: developing strategies for targeting cancer. Nat Rev Cancer 2011, 11:493-501. 10.1038/nrc3079.
79. O'Toole S.A., Machalek D.A., Shearer R.F., Millar E.K., Nair R., Schofield P., et al. Hedgehog overexpression is associated with stromal interactions and predicts for poor outcome in breast cancer. Cancer Res 2011, 71(June (11)):4002-40014. 10.1158/0008-5472.CAN-10-3738.
80. Das S., Samant R.S., Shevde L.A. The hedgehog pathway conditions the bone microenvironment for osteolytic metastasis of breast cancer. Int J Breast Cancer 2012, 2012:298623. 10.1155/2012/298623.
81. Das S., Tucker J.A., Khullar S., Samant R.S., Shevde L.A. Hedgehog signaling in tumor cells facilitates osteoblast-enhanced osteolytic metastases. PLOS ONE 2012, 7:e34374. 10.1371/journal.pone.0034374.
82. Zhou J., Wulfkuhle J., Zhang H., Gu P., Yang Y., Deng J., et al. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci U S A 2007, 104:16158-16163.
83. Hardt O., Wild S., Oerlecke I., Hofmann K., Luo S., Wiencek Y., et al. Highly sensitive profiling of CD44+/CD24- breast cancer stem cells by combining global mRNA amplification and next generation sequencing: evidence for a hyperactive PI3K pathway. Cancer Lett 2012, 325:165-174. 10.1016/j.canlet.2012.06.010.
84. Berns K., Horlings H.M., Hennessy B.T., Madiredjo M., Hijmans E.M., Beelen K., et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007, 12:395-402.
85. - stem cell-like breast cancer cells in human tumors. J Clin Invest 2011, 121:2723-2735. 10.1172/JCI44745.
86. Miller T.W., Rexer B.N., Garrett J.T., Arteaga C.L. Mutations in the phosphatidylinositol 3-kinase pathway: role in tumor progression and therapeutic implications in breast cancer. Breast Cancer Res 2011, 13(6):224. 10.1186/bcr3039.
87. Chang W.W., Lin R.J., Yu J., Chang W.Y., Fu C.H., Lai A.C., et al. The expression and significance of insulin-like growth factor-1 receptor and its pathway on breast cancer stem/progenitors. Breast Cancer Res 2013, 15(3):R39.
88. Hanker A.B., Pfefferle A.D., Balko J.M., Kuba M.G., Young C.D., Sánchez V., et al. PIK3CA accelerates HER2-driven transgenic mammary tumors and induces resistance to combinations of anti-HER2 therapies. Proc Natl Acad Sci U S A 2013, 110:14372-14377. 10.1073/pnas.1303204110.
89. Korkaya H., Paulson A., Charafe-Jauffret Ginestier C., Brown M., Dutcher J., Clouthier S.G., et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 2009, 7:e1000121. 10.1371/journal.pbio.1000121.
90. Zhang M., Atkinson R.L., Rosen J.M. Selective targeting of radiation-resistant tumor-initiating cells. Proc Natl Acad Sci U S A 2010, 107:3522-3527. 10.1158/0008-5472.CAN-07-6353.
91. Chin Y.R., Yoshida T., Marusyk A., Beck A.H., Polyak K., Toker A. Targeting Akt3 signaling in triple-negative breast cancer. Cancer Res 2014, 74:964-973. 10.1158/0008-5472.CAN-13-2175.
92. Wei W., Tweardy D.J., Zhang M., Zhang X., Landua J., Petrovic I., et al. STAT3 signaling is activated preferentially in tumor-initiating cells in claudin-low models of human breast cancer. Stem Cells 2014, 10.1002/stem.1752.
93. Dave B., Landis M.D., Tweardy D.J., Chang J.C., Dobrolecki L.E., Wu M.F., et al. Selective small molecule Stat3 inhibitor reduces breast cancer tumor-initiating cells and improves recurrence free survival in a human-xenograft model. PLOS ONE 2012, 7(8):e30207. 10.1371/journal.pone.0030207.
94. Barbieri I., Pensa S., Pannellini T., Quaglino E., Maritano D., Demaria M., et al. Constitutively active Stat3 enhances neu-mediated migration and metastasis in mammary tumors via upregulation of Cten. Cancer Res 2010, 70:2558-2567. 10.1158/0008-5472.CAN-09-2840.
95. Barbieri I., Quaglino E., Maritano D., Pannellini T., Riera L., Cavallo F., et al. Stat3 is required for anchorage-independent growth and metastasis but not for mammary tumor development downstream of the ErbB-2 oncogene. Mol Carcinog 2010, 49:114-120. 10.1002/mc.20605.
96. Kendrick J.E., Estes J.M., Straughn J.M., Alvarez R.D., Buchsbaum D.J. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and its therapeutic potential in breast and gynecologic cancers. Gynecol Oncol 2007, 106:614-621.
97. Piggott L., Omidvar N., Marti-Perez S., Eberl M., Clarkson R.W. Suppression of apoptosis inhibitor c-FLIP selectively eliminates breast cancer stem cell activity in response to the anticancer agent, TRAIL. Breast Cancer Res 2011, 13:R88. 10.1186/bcr2945.
98. Lang J.Y., Hsu J.L., Meric-Bernstam F., Chang C.J., Wang Q., Bao Y., et al. BikDD eliminates breast cancer initiating cells and synergizes with lapatinib for breast cancer treatment. Cancer Cell 2011, 20:341-356. 10.1016/j.ccr.2011.07.017.
99. Katayama R., Koike S., Sato S., Sugimoto Y., Tsuruo T., Fujita N. Dofequidar fumarate sensitizes cancer stem-like side population cells to chemotherapeutic drugs by inhibiting ABCG2/BCRP-mediated drug export. Cancer Sci 2009, 100:2060-2068. 10.1111/j.1349-7006.2009.01288.
100. Ohno R., Asou N., Ohnishi K. Treatment of acute promyelocytic leukemia: strategy toward further increase of cure rate. Leukemia 2003, 17:1454-1463.
101. Cruz F.D., Matushansky I. Solid tumor differentiation therapy - is it possible. Oncotarget 2012, 3:559-567.
102. Roy R., Willan P.M., Clarke R., Farnie G. Differentiation therapy: targeting breast cancer stem cells to reduce resistance to radiotherapy and chemotherapy. Breast Cancer Res 2010, 12(Suppl. 1):O5. 10.1186/bcr2496.
103. + human breast cancer cells. Breast Cancer Res Treat 2012, 133:75-87. 10.1007/s10549-011-1692-y.
104. Charafe-Jauffret E., Ginestier C., Iovino F., Tarpin C., Diebel M., Esterni B., et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010, 16:45-55. 10.1158/1078-0432.CCR-09-1630.
105. Singh J.K1, Farnie G., Bundred N.J., Simões B.M., Shergill A., Landberg G., et al. Targeting CXCR1/2 significantly reduces breast cancer stem cell activity and increases the efficacy of inhibiting HER2 via HER2-dependent and -independent mechanisms. Clin Cancer Res 2013, 19:643-656. 10.1158/1078-0432.CCR-12-1063.
106. Ginestier C., Liu S., Diebel M.E., Korkaya H., Luo M., Brown M., et al. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest 2010, 120:485-497. 10.1172/JCI39397.
107. Korkaya H., Liu S., Wicha M.S. Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J Clin Invest 2011, 121:3804-3809. 10.1172/JCI57099.
108. Bournazou E., Bromberg J. Targeting the tumor microenvironment: JAK-STAT3 signaling. JAKSTAT 2013, 2:e23828. 10.4161/jkst.23828.
109. Liu S., Ginestier C., Ou S.J., Clouthier S.G., Patel S.H., Monville F., et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 2011, 71:614-624. 10.1158/0008-5472.CAN-10-0538.
110. Chang Q., Bournazou E., Sansone P., Berishaj M., Gao S.P., Daly L., et al. The IL-6/JAK/Stat3 feed-forward loop drives tumorigenesis and metastasis. Neoplasia 2013, 15:848-862.
111. Korkaya H., Kim G.I., Davis A., Malik F., Henry N.L., Ithimakin S., et al. Activation of an IL6 inflammatory loop mediates trastuzumab resistance in HER2+ breast cancer by expanding the cancer stem cell population. Mol Cell 2012, 47:570-584. 10.1016/j.molcel.2012.06.014.
112. 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 Res 2009, 69:7507-7511.
113. Cufi S., Corominas-Faja B., Vazquez-Martin A., Oliveras-Ferraros C., Dorca J., Bosch-Barrera J., et al. Metformin-induced preferential killing of breast cancer initiating CD44+ CD24-/low cells is sufficient to overcome primary resistance to trastuzumab in HER2+ human breast cancer xenografts. Oncotarget 2012, 3:395-398.
114. Jung J.W., Park S.B., Lee S.J., Seo M.S., Trosko J.E., Kang K.S. Metformin represses self-renewal of the human breast carcinoma stem cells via inhibition of estrogen receptor-mediated OCT4 expression. PLoS ONE 2011, 6:e28068. 10.1371/journal.pone.0028068.
115. Hirsch H.A., Iliopoulos D., Struhl K. Metformin inhibits the inflammatory response associated with cellular transformation and cancer stem cell growth. Proc Natl Acad Sci U S A 2013, 110:972-977. 10.1073/pnas.1221055110.
116. Zhu P., Davis M., Blackwelder A.J., Bachman N., Liu B., Edgerton S., et al. Metformin selectively targets tumor-initiating cells in ErbB2-overexpressing breast cancer models. Cancer Prev Res (Phila) 2014, 7:199-210. 10.1158/1940-6207.CAPR-13-0181.
117. Vazquez-Martin A., Oliveras-Ferraros C., Cufí S., Del Barco S., Martin-Castillo B., Menendez J.A. Metformin regulates breast cancer stem cell ontogeny by transcriptional regulation of the epithelial-mesenchymal transition (EMT) status. Cell Cycle 2010, 9:3807-3814.
118. Wang Y.C., Chao T.K., Chang C.C., Yo Y.T., Yu M.H., Lai H.C. Drug screening identifies niclosamide as an inhibitor of breast cancer stem-like cells. PLOS ONE 2013, 8:e74538. 10.1371/journal.pone.0074538.
119. Yip N.C., Fombon I.S., Liu P., Brown S., Kannappan V., Armesilla A.L., et al. Disulfiram modulated ROS-MAPK and NFκB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br J Cancer 2011, 104:1564-1574. 10.1038/bjc.2011.126.
120. Zielske S.P., Spalding A.C., Lawrence T.S. Loss of tumor-initiating cell activity in cyclophosphamide-treated breast xenografts. Transl Oncol 2010, 3:149-152.
121. Grimshaw M.J., Cooper L., Papazisis K., Coleman J.A., Bohnenkamp H.R., Chiapero-Stanke L., et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 2008, 10:R52. 10.1186/bcr2106.
122. Sheridan C., Kishimoto H., Fuchs R.K., Mehrotra S., Bhat-Nakshatri P., Turner C.H., et al. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 2006, 8:R59.
123. Hwang-Verslues W.W., Kuo W.H., Chang P.H., Pan C.C., Wang H.H., Tsai S.T., et al. Multiple lineages of human breast cancer stem/progenitor cells identified by profiling with stem cell markers. PLoS ONE 2009, 4:e8377. 10.1371/journal.pone.0008377.
124. Park S.Y., Lee H.E., Li H., Shipitsin M., Gelman R., Polyak K. Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 2010, 16:876-887. 10.1158/1078-0432.CCR-09-1532.
125. Christgen M., Ballmaier M., Bruchhardt H., von Wasielewski R., Kreipe H., Lehmann U. Identification of a distinct side population of cancer cells in the Cal-51 human breast carcinoma cell line. Mol Cell Biochem 2007, 306:201-212.