Combinatorial treatment of mammospheres with trastuzumab and salinomycin efficiently targets HER2-positive cancer cells and cancer stem cells

International Journal of Cancer

Volumn 131, Issue 12, 2012, Pages 2808-2819

  Oak, Prajakta S ^a   Kopp, Florian ^a   Thakur, Chitra ^b   Ellwart, Joachim W ^c   Rapp, Ulf R ^b   Ullrich, Axel ^b   Wagner, Ernst ^a   Knyazev, Pjotr ^b   Roidl, Andreas ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

cancer stem cells; HER2; salinomycin

Indexed keywords

DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; OCTAMER TRANSCRIPTION FACTOR 4; PACLITAXEL; SALINOMYCIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRASTUZUMAB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CANCER STEM CELL; CELL FRACTIONATION; CELL GROWTH; CELL PROLIFERATION; CELL SELECTION; CELL STRAIN MCF 7; CONTROLLED STUDY; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; TUMOR XENOGRAFT; UPREGULATION;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA PRIMERS; FEMALE; HUMANS; NEOPLASTIC STEM CELLS; PYRANS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, ERBB-2;

EID: 84867873882     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27595     Document Type: Article

References (50)

1. Fisher B, Bryant J, Dignam JJ, et al. Tamoxifen, radiation therapy, or both for prevention of ipsilateral breast tumor recurrence after lumpectomy in women with invasive breast cancers of one centimeter or less. J Clin Oncol 2002; 20: 4141-49.
2. Wolff AC, Davidson NE,. Primary systemic therapy in operable breast cancer. J Clin Oncol 2000; 18: 1558-69.
3. Linn SC, Pinedo HM, van Ark-Otte J, et al. Expression of drug resistance proteins in breast cancer, in relation to chemotherapy. Int J Cancer 1997; 71: 787-95.
4. Grothey A, Voigt W, Schober C, et al. The role of insulin-like growth factor I and its receptor in cell growth, transformation, apoptosis, and chemoresistance in solid tumors. J Cancer Res Clin Oncol 1999; 125: 166-73.
5. Roidl A, Foo P, Wong W, et al. The FGFR4 Y367C mutant is a dominant oncogene in MDA-MB453 breast cancer cells. Oncogene 2010; 29: 1543-52.
6. Chen X, Yeung TK, Wang Z,. Enhanced drug resistance in cells coexpressing ErbB2 with EGF receptor or ErbB3. Biochem Biophys Res Commun 2000; 277: 757-63.
7. Zhang L, Hannay JA, Liu J, et al. Vascular endothelial growth factor overexpression by soft tissue sarcoma cells: implications for tumor growth, metastasis, and chemoresistance. Cancer Res 2006; 66: 8770-8.
8. Sharom FJ,. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 2008; 9: 105-27.
9. Coley HM,. Mechanisms and strategies to overcome chemotherapy resistance in metastatic breast cancer. Cancer Treat Rev 2008; 34: 378-90.
10. Chuthapisith S, Eremin J, El-Sheemey M, et al. Breast cancer chemoresistance: emerging importance of cancer stem cells. Surg Oncol 2010; 19: 27-32.
11. Dean M, Fojo T, Bates S,. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-84.
12. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-8.
13. Croker AK, Goodale D, Chu J, et al. 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 2009; 13: 2236-52.
14. Dontu G,. Breast cancer stem cell markers-the rocky road to clinical applications. Breast Cancer Res 2008; 10: 110.
15. Bao F, Polk P, Nordberg ML, et al. Comparative gene expression analysis of a chronic myelogenous leukemia cell line resistant to cyclophosphamide using oligonucleotide arrays and response to tyrosine kinase inhibitors. Leuk Res 2007; 31: 1511-20.
16. Phillips TM, McBride WH, Pajonk F,. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006; 98: 1777-85.
17. Zhou H, Wu S, Joo JY, et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009; 4: 381-4.
18. Ben-Porath I, Thomson MW, Carey VJ, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
19. Glinsky GV,. "Stemness" genomics law governs clinical behavior of human cancer: implications for decision making in disease management. J Clin Oncol 2008; 26: 2846-53.
20. Ma L, Lai D, Liu T, et al. Cancer stem-like cells can be isolated with drug selection in human ovarian cancer cell line SKOV3. Acta Biochim Biophys Sin (Shanghai) 2010; 42: 593-602.
21. Shaw KR, Wrobel CN, Brugge JS,. Use of three-dimensional basement membrane cultures to model oncogene-induced changes in mammary epithelial morphogenesis. J Mammary Gland Biol Neoplasia 2004; 9: 297-310.
22. Korkaya H, Paulson A, Iovino F, et al. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 2008; 27: 6120-30.
23. Grimshaw MJ, Cooper L, Papazisis K, et al. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res 2008; 10: R52.
24. Pickl M, Ries CH,. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene 2009; 28: 461-8.
25. Slamon DJ, Clark GM, Wong SG, et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235: 177-82.
26. Ginestier C, Hur MH, Charafe-Jauffret E, 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: 555-67.
27. Yaziji H, Goldstein LC, Barry TS, et al. HER-2 testing in breast cancer using parallel tissue-based methods. JAMA 2004; 291: 1972-7.
28. Harari D, Yarden Y,. Molecular mechanisms underlying ErbB2/HER2 action in breast cancer. Oncogene 2000; 19: 6102-14.
29. Magnifico A, Albano L, Campaner S, 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: 2010-21.
30. Li X, Lewis MT, Huang J, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008; 100: 672-9.
31. Neve RM, Lane HA, Hynes NE,. The role of overexpressed HER2 in transformation. Ann Oncol 2001; 12 (Suppl 1): S9-13.
32. Yarden Y,. The EGFR family and its ligands in human cancer. Signalling mechanisms and therapeutic opportunities. Eur J Cancer 2001; 37 (Suppl 4): S3-8.
33. Reim F, Dombrowski Y, Ritter C, et al. Immunoselection of breast and ovarian cancer cells with trastuzumab and natural killer cells: selective escape of CD44high/CD24low/HER2low breast cancer stem cells. Cancer Res 2009; 69: 8058-66.
34. LaBarge MA, Nelson CM, Villadsen R, et al. Human mammary progenitor cell fate decisions are products of interactions with combinatorial microenvironments. Integr Biol (Camb) 2009; 1: 70-9.
35. Rapp UR, Korn C, Ceteci F, et al. MYC is a metastasis gene for non-small-cell lung cancer. PLoS One 2009; 4: e6029.
36. Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138: 645-59.
37. Visvader JE, Lindeman GJ,. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8: 755-68.
38. Dontu G, Abdallah WM, Foley JM, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17: 1253-70.
39. Hynes NE, Lane HA,. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 2005; 5: 341-54.
40. Cicenas J, Urban P, Küng W, et al. Phosphorylation of tyrosine 1248-ERBB2 measured by chemiluminescence-linked immunoassay is independent predictor of poor prognosis in primary breast cancer patients. Eur J Cancer 2006; 42: 636-45.
41. Thor AD, Liu S, Edgerton S, et al. Activation (tyrosine phosphorylation) of ERBB-2 (Her-2/neu): a study of incidence and correlation with outcome in breast cancer. J Clin Oncol 2000; 18: 3230-9.
42. Haenssen KK, Caldwell SA, Shahriari KS, et al. ErbB2 requires integrin alpha5 for anoikis resistance via Src regulation of receptor activity in human mammary epithelial cells. J Cell Sci 2010; 123: 1373-82.
43. Pohlmann PR, Mayer IA, Mernaugh R,. Resistance to Trastuzumab in breast cancer. Clin Cancer Res 2009; 15: 7479-91.
44. O'Brien NA, Browne BC, Chow L, et al. Activated phosphoinositide 3-kinase/AKT signaling confers resistance to trastuzumab but not lapatinib. Mol Cancer Ther 2010; 9: 1489-502.
45. Fuchs D, Daniel V, Sadeghi M, et al. Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 2010; 394: 1098-104.
46. Mitani M, Yamanishi T, Miyazaki Y, et al. Salinomycin effects on mitochondrial ion translocation and respiration. Antimicrob Agents Chemother 1976; 9: 655-60.
47. Matsumori N, Morooka A, Murata M,. Conformation and location of membrane-bound salinomycin-sodium complex deduced from NMR in isotropic bicelles. J Am Chem Soc 2007; 129: 14989-95.
48. Kim JH, Chae M, Kim WK, et al. Salinomycin sensitizes cancer cells to the effects of doxorubicin and etoposide treatment by increasing DNA damage and reducing p21 protein. Br J Pharmacol 2011; 162: 773-84.
49. Dong TT, Zhou HM, Wang LL, et al. Salinomycin selectively targets 'CD133+' cell subpopulations and decreases malignant traits in colorectal cancer lines. Ann Surg Oncol 2011; 18: 1797-804.
50. Weir HK, Thun MJ, Hankey BF, et al. Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control. J Natl Cancer Inst 2003; 95: 1276-99.