Physical Intimacy of Breast Cancer Cells with Mesenchymal Stem Cells Elicits Trastuzumab Resistance through Src Activation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Daverey, Amita ^a   Drain, Allison P ^a   Kidambi, Srivatsan ^a,b,c  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; PROTEIN TYROSINE KINASE; TRASTUZUMAB;

BIOLOGICAL MODEL; BREAST TUMOR; CELL COMMUNICATION; CELL CULTURE; COCULTURE; DRUG RESISTANCE; ENZYME ACTIVATION; FEMALE; HUMAN; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; FEMALE; HUMANS; MESENCHYMAL STROMAL CELLS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRASTUZUMAB;

EID: 84941069370     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13744     Document Type: Article

References (51)

1. Krishnamurti, U. & Silverman, J. F. HER2 in breast cancer: a review and update. Adv Anat Pathol 21, 100-107 (2014).
2. Subbiah, I. M. & Gonzalez-Angulo, A. M. Advances and future directions in the targeting of HER2-positive breast cancer: implications for the future. Curr Treat Options Oncol 15, 41-54 (2014).
3. Bailey, T. A. et al. Mechanisms of Trastuzumab resistance in ErbB2-driven breast cancer and newer opportunities to overcome therapy resistance. Journal of carcinogenesis 10, 28, doi: 10.4103/1477-3163.90442 (2011).
4. Garrett, J. T. & Arteaga, C. L. Resistance to HER2-directed antibodies and tyrosine kinase inhibitors: mechanisms and clinical implications. Cancer biology & therapy 11, 793-800 (2011).
5. Fiszman, G. L. & Jasnis, M. A. Molecular Mechanisms of Trastuzumab Resistance in HER2 Overexpressing Breast Cancer. International journal of breast cancer 2011, 352182, doi: 10.4061/2011/352182 (2011).
6. Peiro, G. et al. Src, a potential target for overcoming trastuzumab resistance in HER2-positive breast carcinoma. British journal of cancer 111, 689-695, doi: 10.1038/bjc.2014.327 (2014).
7. Pohorelic, B. et al. Role of Src in breast cancer cell migration and invasion in a breast cell/bone-derived cell microenvironment. Breast cancer research and treatment 133, 201-214, doi: 10.1007/s10549-011-1753-2 (2012).
8. Zhang, S. et al. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nature medicine 17, 461-469, doi: 10.1038/nm.2309 (2011).
9. Junttila, M. R. & de Sauvage, F. J. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501, 346-354, doi: 10.1038/nature12626 (2013).
10. Correia, A. L. & Bissell, M. J. The tumor microenvironment is a dominant force in multidrug resistance. Drug resistance updates: reviews and commentaries in antimicrobial and anticancer chemotherapy 15, 39-49, doi: 10.1016/j.drup.2012.01.006 (2012).
11. Bissell, M. J. & Labarge, M. A. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer cell 7, 17-23, doi: 10.1016/j.ccr.2004.12.013 (2005).
12. Gorgun, G. T. et al. Tumor-promoting immune-suppressive myeloid-derived suppressor cells in the multiple myeloma microenvironment in humans. Blood 121, 2975-2987, doi: 10.1182/blood-2012-08-448548 (2013).
13. Sun, Z., Wang, S. & Zhao, R. C. The roles of mesenchymal stem cells in tumor inflammatory microenvironment. Journal of hematology & oncology 7, 14, doi: 10.1186/1756-8722-7-14 (2014).
14. D'Souza, N. et al. MSC and Tumors: Homing, Differentiation, and Secretion Influence Therapeutic Potential. Advances in biochemical engineering/biotechnology 130, 209-266, doi: 10.1007/10-2012-150 (2013).
15. Roodhart, J. M. et al. Mesenchymal stem cells induce resistance to chemotherapy through the release of platinum-induced fatty acids. Cancer cell 20, 370-383, doi: 10.1016/j.ccr.2011.08.010 (2011).
16. Li, H. J., Reinhardt, F., Herschman, H. R. & Weinberg, R. A. Cancer-stimulated mesenchymal stem cells create a carcinoma stem cell niche via prostaglandin E2 signaling. Cancer discovery 2, 840-855, doi: 10.1158/2159-8290.CD-12-0101 (2012).
17. Karnoub, A. E. et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449, 557-563, doi: 10.1038/nature06188 (2007).
18. Uchibori, R. et al. NF-kappaB activity regulates mesenchymal stem cell accumulation at tumor sites. Cancer research 73, 364-372, doi: 10.1158/0008-5472.CAN-12-0088 (2013).
19. Chaturvedi, P. et al. Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis. The Journal of clinical investigation 123, 189-205, doi: 10.1172/JCI64993 (2013).
20. Huang, W. H. et al. Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene 32, 4343-4354, doi: 10.1038/onc.2012.458 (2013).
21. Martin, F. T. et al. Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT). Breast cancer research and treatment 124, 317-326, doi: 10.1007/s10549-010-0734-1 (2010).
22. Beckermann, B. M. et al. VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. British journal of cancer 99, 622-631, doi: 10.1038/sj.bjc.6604508 (2008).
23. Bergfeld, S. A. & DeClerck, Y. A. Bone marrow-derived mesenchymal stem cells and the tumor microenvironment. Cancer metastasis reviews 29, 249-261, doi: 10.1007/s10555-010-9222-7 (2010).
24. Zhou, C. et al. Proteomic analysis of acquired tamoxifen resistance in MCF-7 cells reveals expression signatures associated with enhanced migration. Breast cancer research : BCR 14, R45, doi: 10.1186/bcr3144 (2012).
25. Klopp, A. H. et al. Mesenchymal stem cells promote mammosphere formation and decrease E-cadherin in normal and malignant breast cells. PloS one 5, e12180, doi: 10.1371/journal.pone.0012180 (2010).
26. Weaver, V. M. et al. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer cell 2, 205-216 (2002).
27. Shekhar, M. P., Santner, S., Carolin, K. A. & Tait, L. Direct involvement of breast tumor fibroblasts in the modulation of tamoxifen sensitivity. The American journal of pathology 170, 1546-1560, doi: 10.2353/ajpath.2007.061004 (2007).
28. Korkaya, H. & Wicha, M. S. HER-2, notch, and breast cancer stem cells: targeting an axis of evil. Clinical cancer research : an official journal of the American Association for Cancer Research 15, 1845-1847, doi: 10.1158/1078-0432.CCR-08-3087 (2009).
29. Miki, Y. et al. The advantages of co-culture over mono cell culture in simulating in vivo environment. The Journal of steroid biochemistry and molecular biology 131, 68-75, doi: 10.1016/j.jsbmb.2011.12.004 (2012).
30. Kidambi, S., Lee, I. & Chan, C. Primary Neuron/Astrocyte Co-Culture on Polyelectrolyte Multilayer Films: A Template for Studying Astrocyte-Mediated Oxidative Stress in Neurons. Advanced functional materials 18, 294-301, doi: 10.1002/adfm.200601237 (2008).
31. Kidambi, S. et al. Patterned co-culture of primary hepatocytes and fibroblasts using polyelectrolyte multilayer templates. Macromolecular bioscience 7, 344-353, doi: 10.1002/mabi.200600205 (2007).
32. Khademhosseini, A. et al. Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates. Biomaterials 27, 5968-5977, doi: 10.1016/j.biomaterials.2006.06.035 (2006).
33. Fukuda, J. et al. Micropatterned cell co-cultures using layer-by-layer deposition of extracellular matrix components. Biomaterials 27, 1479-1486, doi: doi: 10.1016/j.biomaterials.2005.09.015 (2006).
34. Souter, L. H. et al. Human 21T breast epithelial cell lines mimic breast cancer progression in vivo and in vitro and show stage-specific gene expression patterns. Lab Invest 90, 1247-1258 (2010).
35. Daverey, A., Mytty, A. & Kidambi, S. Topography Mediated Regulation of HER-2 Expression in Breast Cancer Cells. NanoLife 2, doi: 10.1142/S1793984412410097 (2012).
36. Frame, M. C. Src in cancer: deregulation and consequences for cell behaviour. Biochimica et biophysica acta 1602, 114-130 (2002).
37. Rosivatz, E. et al. A small molecule inhibitor for phosphatase and tensin homologue deleted on chromosome 10 (PTEN). ACS chemical biology 1, 780-790, doi: 10.1021/cb600352f (2006).
38. Schmid, A. C., Byrne, R. D., Vilar, R. & Woscholski, R. Bisperoxovanadium compounds are potent PTEN inhibitors. FEBS letters 566, 35-38, doi: 10.1016/j.febslet.2004.03.102 (2004).
39. Mouw, J. K. et al. Tissue mechanics modulate microRNA-dependent PTEN expression to regulate malignant progression. Nature medicine 20, 360-367, doi: 10.1038/nm.3497 (2014).
40. Korkaya, H. et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 7, e1000121, doi: 10.1371/journal.pbio.1000121 (2009).
41. Mise-Omata, S., Obata, Y., Iwase, S., Mise, N. & Doi, T. S. Transient strong reduction of PTEN expression by specific RNAi induces loss of adhesion of the cells. Biochem Biophys Res Commun 328, 1034-1042, doi: 10.1016/j.bbrc.2005.01.066 (2005).
42. Nagata, Y. et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer cell 6, 117-127, doi: 10.1016/j.ccr.2004.06.022 (2004).
43. Berns, K. et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 12, 395-402, doi: 10.1016/j.ccr.2007.08.030 (2007).
44. Albanell, J. & Baselga, J. Trastuzumab, a humanized anti-HER2 monoclonal antibody, for the treatment of breast cancer. Drugs Today (Barc) 35, 931-946 (1999).
45. Brunton, V. G. & Frame, M. C. Src and focal adhesion kinase as therapeutic targets in cancer. Current opinion in pharmacology 8, 427-432, doi: 10.1016/j.coph.2008.06.012 (2008).
46. Belsches-Jablonski, A. P. et al. Src family kinases and HER2 interactions in human breast cancer cell growth and survival. Oncogene 20, 1465-1475, doi: 10.1038/sj.onc.1204205 (2001).
47. Clarke, M. R., Imhoff, F. M. & Baird, S. K. Mesenchymal stem cells inhibit breast cancer cell migration and invasion through secretion of tissue inhibitor of metalloproteinase-1 and -2. Molecular carcinogenesis, doi: 10.1002/mc.22178 (2014).
48. Zhu, Y. et al. Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia 23, 925-933, doi: 10.1038/leu.2008.384 (2009).
49. Ma, Y., Hao, X., Zhang, S. & Zhang, J. The in vitro and in vivo effects of human umbilical cord mesenchymal stem cells on the growth of breast cancer cells. Breast cancer research and treatment 133, 473-485, doi: 10.1007/s10549-011-1774-x (2012).
50. Usha, L. R. G., Christopherson, Ii K. & Xu, X. Mesenchymal stem cells develop tumor tropism but do not accelerate breast cancer tumorigenesis in a somatic mouse breast cancer model. PloS one 8, e67895 (2013).
51. Dasari, V. R. et al. Upregulation of PTEN in glioma cells by cord blood mesenchymal stem cells inhibits migration via downregulation of the PI3K/Akt pathway. PLoS One 5, e10350, doi: 10.1371/journal.pone.0010350 (2010).