The impact of tumor stroma on drug response in breast cancer

Seminars in Cancer Biology

Volumn 31, Issue , 2015, Pages 3-15

  Dittmer, Jürgen ^a   Leyh, Benjamin ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Carcinoma associated fibroblast; Drug resistance; Extra cellular matrix; Mesenchymal stem cell; Tumor associated macrophage

Indexed keywords

CYTOKINE; INTERLEUKIN 6; INTERLEUKIN 8; SCATTER FACTOR; STROMAL CELL DERIVED FACTOR 1; TAMOXIFEN; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; ANTINEOPLASTIC AGENT;

BLOOD FLOW; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CARCINOMA ASSOCIATED FIBROBLAST; CELL ADHESION; DRUG RESPONSE; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMAN EPIDERMAL GROWTH FACTOR RECEPTOR POSITIVE BREAST CANCER; MESENCHYME CELL; NONHUMAN; PROTEIN FUNCTION; REVIEW; STROMA CELL; TREATMENT INDICATION; TRIPLE NEGATIVE BREAST CANCER; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; BIOLOGICAL MODEL; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; METABOLISM; NEOPLASM, RESIDUAL; PATHOLOGY; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MODELS, BIOLOGICAL; NEOPLASM, RESIDUAL; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84923217987     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.05.006     Document Type: Review

References (214)

1. Toriola A.T., Colditz G.A. Trends in breast cancer incidence and mortality in the United States: implications for prevention. Breast Cancer Res Treat 2013, 138:665-673.
2. Njor S., Nystrom L., Moss S., Paci E., Broeders M., Segnan N., et al. Breast cancer mortality in mammographic screening in Europe: a review of incidence-based mortality studies. J Med Screen 2012, 19:33-41.
3. Davies C., Godwin J., Gray R., Clarke M., Cutter D., Darby S., et al. Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet 2011, 378:771-784.
4. Hudis C.A. Trastuzumab - mechanism of action and use in clinical practice. N Engl J Med 2007, 357:39-51.
5. Perou C.M., Sorlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
6. Prat A., Perou C.M. Deconstructing the molecular portraits of breast cancer. Mol Oncol 2011, 5:5-23.
7. Sorlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874.
8. Parker J.S., Mullins M., Cheang M.C., Leung S., Voduc D., Vickery T., et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009, 27:1160-1167.
9. Prat A., Parker J.S., Karginova O., Fan C., Livasy C., Herschkowitz J.I., et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010, 12:R68.
10. Network C.G.A. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70.
11. Nandy A., Gangopadhyay S., Mukhopadhyay A. Individualizing breast cancer treatment - the dawn of personalized medicine. Exp Cell Res 2014, 320:1-11.
12. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
13. Whitfield M.L., George L.K., Grant G.D., Perou C.M. Common markers of proliferation. Nat Rev Cancer 2006, 6:99-106.
14. Greene J., Hennessy B. The role of anthracyclines in the treatment of early breast cancer. J Oncol Pharm Pract 2014, [in press].
15. Wilcken N., Zdenkowski N., White M., Snyder R., Pittman K., Mainwaring P., et al. Systemic treatment of HER2-positive metastatic breast cancer: a systematic review. Asia Pac J Clin Oncol 2014, 10:1-14.
16. Davis S.L., Eckhardt S.G., Tentler J.J., Diamond J.R. Triple-negative breast cancer: bridging the gap from cancer genomics to predictive biomarkers. Ther Adv Med Oncol 2014, 6:88-100.
17. Masuda H., Zhang D., Bartholomeusz C., Doihara H., Hortobagyi G.N., Ueno N.T. Role of epidermal growth factor receptor in breast cancer. Breast Cancer Res Treat 2012, 136:331-345.
18. Griffiths C.L., Olin J.L. Triple negative breast cancer: a brief review of its characteristics and treatment options. J Pharm Pract 2012, 25:319-323.
19. Lehmann B.D., Bauer J.A., Chen X., Sanders M.E., Chakravarthy A.B., Shyr Y., et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011, 121:2750-2767.
20. de Oliveira Niero E.L., Rocha-Sales B., Lauand C., Cortez B.A., de Souza M.M., Rezende-Teixeira P., et al. The multiple facets of drug resistance: one history, different approaches. J Exp Clin Cancer Res 2014, 33:37.
21. Bailey T.A., Luan H., Clubb R.J., Naramura M., Band V., Raja S.M., et al. Mechanisms of Trastuzumab resistance in ErbB2-driven breast cancer and newer opportunities to overcome therapy resistance. J Carcinog 2011, 10.
22. Musgrove E.A., Sutherland R.L. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 2009, 9:631-643.
23. Osborne C.K., Schiff R. Mechanisms of endocrine resistance in breast cancer. Annu Rev Med 2011, 62:233-247.
24. Nagata Y., Lan K.H., Zhou X., Tan M., Esteva F.J., Sahin A.A., et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 2004, 6:117-127.
25. Huang C., Park C.C., Hilsenbeck S.G., Ward R., Rimawi M.F., Wang Y.C., et al. beta1 integrin mediates an alternative survival pathway in breast cancer cells resistant to lapatinib. Breast Cancer Res 2011, 13:R84.
26. De Amicis F., Thirugnansampanthan J., Cui Y., Selever J., Beyer A., Parra I., et al. Androgen receptor overexpression induces tamoxifen resistance in human breast cancer cells. Breast Cancer Res Treat 2010, 121:1-11.
27. Mo Z., Liu M., Yang F., Luo H., Li Z., Tu G., et al. GPR30 as an initiator of tamoxifen resistance in hormone-dependent breast cancer. Breast Cancer Res 2013, 15:R114.
28. Ciruelos Gil E.M. Targeting the PI3K/AKT/mTOR pathway in estrogen receptor-positive breast cancer. Cancer Treat Rev 2014, 40(7):862-871.
29. Liu P., Cheng H., Roberts T.M., Zhao J.J. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov 2009, 8:627-644.
30. Magnuson B., Ekim B., Fingar D.C. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 2012, 441:1-21.
31. Baselga J., Campone M., Piccart M., Burris H.A., Rugo H.S., et al. Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med 2012, 366:520-529.
32. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011, 17:313-319.
33. Nguyen L.V., Vanner R., Dirks P., Eaves C.J. Cancer stem cells: an evolving concept. Nat Rev Cancer 2012, 12:133-143.
34. Visvader J.E. Cells of origin in cancer. Nature 2011, 469:314-322.
35. 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 2009, 16:45-55.
36. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8:755-768.
37. Mannello F. Understanding breast cancer stem cell heterogeneity: time to move on to a new research paradigm. BMC Med 2013, 11.
38. Proia T.A., Keller P.J., Gupta P.B., Klebba I., Jones A.D., Sedic M., et al. Genetic predisposition directs breast cancer phenotype by dictating progenitor cell fate. Cell Stem Cell 2011, 8:149-163.
39. Dave B., Mittal V., Tan N.M., Chang J.C. Epithelial-mesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res 2012, 14:202.
40. Sotiropoulou P.A., Christodoulou M.S., Silvani A., Herold-Mende C., Passarella D. Chemical approaches to targeting drug resistance in cancer stem cells. Drug Discov Today 2014, [in press].
41. 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.
42. Harrison H., Simoes B.M., Rogerson L., Howell S.J., Landberg G., Clarke R.B. Oestrogen increases the activity of oestrogen receptor negative breast cancer stem cells through paracrine EGFR and Notch signalling. Breast Cancer Res 2013, 15:R21.
43. Tieu K.S., Tieu R.S., Martinez-Agosto J.A., Sehl M.E. Stem cell niche dynamics: from homeostasis to carcinogenesis. Stem Cells Int 2012, 2012.
44. Dittmer J., Rody A. Stem cells in breast cancer. Histol Histopathol 2013, 28:827-838.
45. Correia A.L., Bissell M.J. The tumor microenvironment is a dominant force in multidrug resistance. Drug Resist Updat 2012, 15:39-49.
46. Klein G. Evolutionary aspects of cancer resistance. Semin Cancer Biol 2014, 25:10-14.
47. Junttila M.R., de Sauvage F.J. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 2013, 501:346-354.
48. Egeblad M., Nakasone E.S., Werb Z. Tumors as organs: complex tissues that interface with the entire organism. Dev Cell 2010, 18:884-901.
49. Castano Z., Fillmore C.M., Kim C.F., McAllister S.S. The bed and the bugs: interactions between the tumor microenvironment and cancer stem cells. Semin Cancer Biol 2012, 22:462-470.
50. Meads M.B., Gatenby R.A., Dalton W.S. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat Rev Cancer 2009, 9:665-674.
51. Teicher B.A., Herman T.S., Holden S.A., Wang Y.Y., Pfeffer M.R., Crawford J.W., et al. Tumor resistance to alkylating agents conferred by mechanisms operative only in vivo. Science 1990, 247:1457-1461.
52. Nakasone E.S., Askautrud H.A., Kees T., Park J.H., Plaks V., Ewald A.J., et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 2012, 21:488-503.
53. Sethi T., Rintoul R.C., Moore S.M., MacKinnon A.C., Salter D., Choo C., et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 1999, 5:662-668.
54. Berube M., Talbot M., Collin C., Paquet-Bouchard C., Germain L., Guerin S.L., et al. Role of the extracellular matrix proteins in the resistance of SP6.5 uveal melanoma cells toward cisplatin. Int J Oncol 2005, 26:405-413.
55. DuFort C.C., Paszek M.J., Weaver V.M. Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 2011, 12:308-319.
56. Hattar R., Maller O., McDaniel S., Hansen K.C., Hedman K.J., Lyons T.R., et al. Tamoxifen induces pleiotrophic changes in mammary stroma resulting in extracellular matrix that suppresses transformed phenotypes. Breast Cancer Res 2009, 11:R5.
57. Tokes A.M., Szasz A.M., Farkas A., Toth A.I., Dank M., Harsanyi L., et al. Stromal matrix protein expression following preoperative systemic therapy in breast cancer. Clin Cancer Res 2009, 15:731-739.
58. Sherman-Baust C.A., Weeraratna A.T., Rangel L.B., Pizer E.S., Cho K.R., Schwartz D.R., et al. Remodeling of the extracellular matrix through overexpression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cell 2003, 3:377-386.
59. Netti P.A., Berk D.A., Swartz M.A., Grodzinsky A.J., Jain R.K. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000, 60:2497-2503.
60. Loeffler M., Kruger J.A., Niethammer A.G., Reisfeld R.A. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 2006, 116:1955-1962.
61. Watt F.M., Huck W.T. Role of the extracellular matrix in regulating stem cell fate. Nat Rev Mol Cell Biol 2013, 14:467-473.
62. Weigelt B., Lo A.T., Park C.C., Gray J.W., Bissell M.J. HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is dependent strongly on the 3D microenvironment. Breast Cancer Res Treat 2010, 122:35-43.
63. Aoudjit F., Vuori K. Integrin signaling inhibits paclitaxel-induced apoptosis in breast cancer cells. Oncogene 2001, 20:4995-5004.
64. Park C.C., Zhang H.J., Yao E.S., Park C.J., Bissell M.J. Beta1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts. Cancer Res 2008, 68:4398-4405.
65. Huang S., Holzel M., Knijnenburg T., Schlicker A., Roepman P., McDermott U., et al. MED12 controls the response to multiple cancer drugs through regulation of TGF-beta receptor signaling. Cell 2012, 151:937-950.
66. Pontiggia O., Sampayo R., Raffo D., Motter A., Xu R., Bissell M.J., et al. The tumor microenvironment modulates tamoxifen resistance in breast cancer: a role for soluble stromal factors and fibronectin through beta1 integrin. Breast Cancer Res Treat 2012, 133:459-471.
67. Zhang H., Ozaki I., Mizuta T., Matsuhashi S., Yoshimura T., Hisatomi A., et al. Beta 1-integrin protects hepatoma cells from chemotherapy induced apoptosis via a mitogen-activated protein kinase dependent pathway. Cancer 2002, 95:896-906.
68. Shain K.H., Landowski T.H., Dalton W.S. Adhesion-mediated intracellular redistribution of c-Fas-associated death domain-like IL-1-converting enzyme-like inhibitory protein-long confers resistance to CD95-induced apoptosis in hematopoietic cancer cell lines. J Immunol 2002, 168:2544-2553.
69. de la Fuente M.T., Casanova B., Cantero E., Hernandez del Cerro M., Garcia-Marco J., Silva A., et al. Involvement of p53 in alpha4beta1 integrin-mediated resistance of B-CLL cells to fludarabine. Biochem Biophys Res Commun 2003, 311:708-712.
70. Hazlehurst L.A., Argilagos R.F., Dalton W.S. Beta1 integrin mediated adhesion increases Bim protein degradation and contributes to drug resistance in leukaemia cells. Br J Haematol 2007, 136:269-275.
71. Hodkinson P.S., Mackinnon A.C., Sethi T. Extracellular matrix regulation of drug resistance in small-cell lung cancer. Int J Radiat Biol 2007, 83:733-741.
72. Fu Y., Fang Z., Liang Y., Zhu X., Prins P., Li Z., et al. Overexpression of integrin beta1 inhibits proliferation of hepatocellular carcinoma cell SMMC-7721 through preventing Skp2-dependent degradation of p27 via PI3K pathway. J Cell Biochem 2007, 102:704-718.
73. Cordes N., Seidler J., Durzok R., Geinitz H., Brakebusch C. Beta1-integrin-mediated signaling essentially contributes to cell survival after radiation-induced genotoxic injury. Oncogene 2006, 25:1378-1390.
74. Schrader J., Gordon-Walker T.T., Aucott R.L., van Deemter M., Quaas A., Walsh S., et al. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 2011, 53:1192-1205.
75. Eberle K.E., Sansing H.A., Szaniszlo P., Resto V.A., Berrier A.L. Carcinoma matrix controls resistance to cisplatin through talin regulation of NF-kB. PLoS ONE 2011, 6:e21496.
76. Margadant C., Monsuur H.N., Norman J.C., Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol 2011, 23:607-614.
77. Matsunaga T., Fukai F., Miura S., Nakane Y., Owaki T., Kodama H., et al. Combination therapy of an anticancer drug with the FNIII14 peptide of fibronectin effectively overcomes cell adhesion-mediated drug resistance of acute myelogenous leukemia. Leukemia 2008, 22:353-360.
78. Landowski T.H., Olashaw N.E., Agrawal D., Dalton W.S. Cell adhesion-mediated drug resistance (CAM-DR) is associated with activation of NF-kappa B (RelB/p50) in myeloma cells. Oncogene 2003, 22:2417-2421.
79. Oida K., Matsuda A., Jung K., Xia Y., Jang H., Amagai Y., et al. Nuclear factor-kB plays a critical role in both intrinsic and acquired resistance against endocrine therapy in human breast cancer cells. Sci Rep 2014, 4:4057.
80. Chen Y.J., Yeh M.H., Yu M.C., Wei Y.L., Chen W.S., Chen J.Y., et al. Lapatinib - induced NF-kappaB activation sensitizes triple-negative breast cancer cells to proteasome inhibitors. Breast Cancer Res 2013, 15:R108.
81. Hazlehurst L.A., Damiano J.S., Buyuksal I., Pledger W.J., Dalton W.S. Adhesion to fibronectin via beta1 integrins regulates p27kip1 levels and contributes to cell adhesion mediated drug resistance (CAM-DR). Oncogene 2000, 19:4319-4327.
82. Folgiero V., Avetrani P., Bon G., Di Carlo S.E., Fabi A., Nistico C., et al. Induction of ErbB-3 expression by alpha6beta4 integrin contributes to tamoxifen resistance in ERbeta1-negative breast carcinomas. PLoS ONE 2008, 3:e1592.
83. Maubant S., Cruet-Hennequart S., Poulain L., Carreiras F., Sichel F., Luis J., et al. Altered adhesion properties and alphav integrin expression in a cisplatin-resistant human ovarian carcinoma cell line. Int J Cancer 2002, 97:186-194.
84. Uhm J.H., Dooley N.P., Kyritsis A.P., Rao J.S., Gladson C.L. Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells from apoptotic death. Clin Cancer Res 1999, 5:1587-1594.
85. Schafer H., Dieckmann C., Korniienko O., Moldenhauer G., Kiefel H., Salnikov A., et al. Combined treatment of L1CAM antibodies and cytostatic drugs improve the therapeutic response of pancreatic and ovarian carcinoma. Cancer Lett 2012, 319:66-82.
86. Goel S., Duda D.G., Xu L., Munn L.L., Boucher Y., Fukumura D., et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011, 91:1071-1121.
87. Olive K.P., Jacobetz M.A., Davidson C.J., Gopinathan A., McIntyre D., Honess D., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009, 324:1457-1461.
88. Jain R.K. Normalizing tumor microenvironment to treat cancer: bench to bedside to biomarkers. J Clin Oncol 2013, 31:2205-2218.
89. Hall C.N., Reynell C., Gesslein B., Hamilton N.B., Mishra A., Sutherland B.A., et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014, 508(7494):55-60.
90. Rolny C., Mazzone M., Tugues S., Laoui D., Johansson I., Coulon C., et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 2011, 19:31-44.
91. Farmer P., Bonnefoi H., Anderle P., Cameron D., Wirapati P., Becette V., et al. A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med 2009, 15:68-74.
92. Mao Y., Keller E.T., Garfield D.H., Shen K., Wang J. Stromal cells in tumor microenvironment and breast cancer. Cancer Metastasis Rev 2013, 32:303-315.
93. Meckes D.G., Raab-Traub N. Microvesicles and viral infection. J Virol 2011, 85:12844-12854.
94. Muralidharan-Chari V., Clancy J.W., Sedgwick A., D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 2010, 123:1603-1611.
95. Rafii A., Mirshahi P., Poupot M., Faussat A.M., Simon A., Ducros E., et al. Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumours. PLoS ONE 2008, 3:e3894.
96. Polanska U.M., Orimo A. Carcinoma-associated fibroblasts: non-neoplastic tumour-promoting mesenchymal cells. J Cell Physiol 2013, 228:1651-1657.
97. Biswas S.K., Allavena P., Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol 2013, 35:585-600.
98. Cook J., Hagemann T. Tumour-associated macrophages and cancer. Curr Opin Pharmacol 2013, 13:595-601.
99. Cuiffo B.G., Karnoub A.E. Mesenchymal stem cells in tumor development: emerging roles and concepts. Cell Adh Migr 2012, 6:220-230.
100. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:232-309.
101. Dittmer J., Oerlecke I., Leyh B. Involvement of mesenchymal stem cells in breast cancer progression. Breast Cancer-Focusing Tumor Microenvironment, Stem Cells and Metastasis 2011, 247-272. INTECH Open Access Publisher, Rijeka, Croatia. M. Gunduz, E. Gunduz (Eds.).
102. Paraiso K.H., Smalley K.S. Fibroblast-mediated drug resistance in cancer. Biochem Pharmacol 2013, 85:1033-1041.
103. Tchou J., Conejo-Garcia J. Targeting the tumor stroma as a novel treatment strategy for breast cancer: shifting from the neoplastic cell-centric to a stroma-centric paradigm. Adv Pharmacol 2012, 65:45-61.
104. Shekhar M.P., Santner S., Carolin K.A., Tait L. Direct involvement of breast tumor fibroblasts in the modulation of tamoxifen sensitivity. Am J Pathol 2007, 170:1546-1560.
105. Martinez-Outschoorn U.E., Goldberg A., Lin Z., Ko Y.H., Flomenberg N., Wang C., et al. Anti-estrogen resistance in breast cancer is induced by the tumor microenvironment and can be overcome by inhibiting mitochondrial function in epithelial cancer cells. Cancer Biol Ther 2011, 12:924-938.
106. Sotgia F., Martinez-Outschoorn U.E., Howell A., Pestell R.G., Pavlides S., Lisanti M.P. Caveolin-1 and cancer metabolism in the tumor microenvironment: markers, models, and mechanisms. Annu Rev Pathol 2012, 7:423-467.
107. Luo H., Yang G., Yu T., Luo S., Wu C., Sun Y., et al. GPER-mediated proliferation and estradiol production in breast cancer-associated fibroblasts. Endocr Relat Cancer 2014, 21:355-369.
108. Busch S., Ryden L., Stal O., Jirstrom K., Landberg G. Low ERK phosphorylation in cancer-associated fibroblasts is associated with tamoxifen resistance in pre-menopausal breast cancer. PLoS ONE 2012, 7:e45669.
109. Sun Y., Campisi J., Higano C., Beer T.M., Porter P., Coleman I., et al. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 2012, 18:1359-1568.
110. Lafkas D., Trimis G., Papavassiliou A.G., Kiaris H. P53 mutations in stromal fibroblasts sensitize tumors against chemotherapy. Int J Cancer 2008, 123:967-971.
111. Burdelya L.G., Komarova E.A., Hill J.E., Browder T., Tararova N.D., Mavrakis L., et al. Inhibition of p53 response in tumor stroma improves efficacy of anticancer treatment by increasing antiangiogenic effects of chemotherapy and radiotherapy in mice. Cancer Res 2006, 66:9356-9361.
112. West R.B., Nuyten D.S., Subramanian S., Nielsen T.O., Corless C.L., Rubin B.P., et al. Determination of stromal signatures in breast carcinoma. PLoS Biol 2005, 3:e187.
113. Chen S., Lewallen M., Xie T. Adhesion in the stem cell niche: biological roles and regulation. Development 2013, 140:255-265.
114. Dittmer A., Fuchs A., Oerlecke I., Leyh B., Kaiser S., Martens J.W., et al. Mesenchymal stem cells and carcinoma-associated fibroblasts sensitize breast cancer cells in 3D cultures to kinase inhibitors. Int J Oncol 2011, 39:689-696.
115. Heidorn S.J., Milagre C., Whittaker S., Nourry A., Niculescu-Duvas I., Dhomen N., et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010, 140:209-221.
116. Hiscox S., Jordan N.J., Jiang W., Harper M., McClelland R., Smith C., et al. Chronic exposure to fulvestrant promotes overexpression of the c-Met receptor in breast cancer cells: implications for tumour-stroma interactions. Endocr Relat Cancer 2006, 13:1085-1099.
117. Wilson T.R., Fridlyand J., Yan Y., Penuel E., Burton L., Chan E., et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012, 487:505-509.
118. Mueller K.L., Madden J.M., Zoratti G.L., Kuperwasser C., List K., Boerner J.L. Fibroblast-secreted hepatocyte growth factor mediates epidermal growth factor receptor tyrosine kinase inhibitor resistance in triple-negative breast cancers through paracrine activation of Met. Breast Cancer Res 2012, 14:R104.
119. Aesoy R., Sanchez B.C., Norum J.H., Lewensohn R., Viktorsson K., Linderholm B. An autocrine VEGF/VEGFR2 and p38 signaling loop confers resistance to 4-hydroxytamoxifen in MCF-7 breast cancer cells. Mol Cancer Res 2008, 6:1630-1638.
120. Liang Y., Brekken R.A., Hyder S.M. Vascular endothelial growth factor induces proliferation of breast cancer cells and inhibits the anti-proliferative activity of anti-hormones. Endocr Relat Cancer 2006, 13:905-919.
121. Shah N., Jin K., Cruz L.A., Park S., Sadik H., Cho S., et al. HOXB13 mediates tamoxifen resistance and invasiveness in human breast cancer by suppressing ERalpha and inducing IL-6 expression. Cancer Res 2013, 73:5449-5458.
122. Shi Z., Yang W.M., Chen L.P., Yang D.H., Zhou Q., Zhu J., et al. Enhanced chemosensitization in multidrug-resistant human breast cancer cells by inhibition of IL-6 and IL-8 production. Breast Cancer Res Treat 2012, 135:737-747.
123. Ohbayashi M., Yasuda M., Kawakami I., Kohyama N., Kobayashi Y., Yamamoto T. Effect of interleukins response to ECM-induced acquisition of drug resistance in MCF-7 cells. Exp Oncol 2008, 30:276-282.
124. Conze D., Weiss L., Regen P.S., Bhushan A., Weaver D., Johnson P., et al. Autocrine production of interleukin 6 causes multidrug resistance in breast cancer cells. Cancer Res 2001, 61:8851-8858.
125. Sullivan N.J., Sasser A.K., Axel A.E., Vesuna F., Raman V., Ramirez N., et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009, 28:2940-2947.
126. Xie G., Yao Q., Liu Y., Du S., Liu A., Guo Z., et al. IL-6-induced epithelial-mesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int J Oncol 2012, 40:1171-1179.
127. 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.
128. 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.
129. Britschgi A., Andraos R., Brinkhaus H., Klebba I., Romanet V., Muller U., et al. JAK2/STAT5 inhibition circumvents resistance to PI3K/mTOR blockade: a rationale for cotargeting these pathways in metastatic breast cancer. Cancer Cell 2012, 22:796-811.
130. Shao N., Chen L.H., Ye R.Y., Lin Y., Wang S.M. The depletion of interleukin-8 causes cell cycle arrest and increases the efficacy of docetaxel in breast cancer cells. Biochem Biophys Res Commun 2013, 431:535-541.
131. Rhodes L.V., Muir S.E., Elliott S., Guillot L.M., Antoon J.W., Penfornis P., et al. Adult human mesenchymal stem cells enhance breast tumorigenesis and promote hormone independence. Breast Cancer Res Treat 2010, 121:293-300.
132. Rhodes L.V., Short S.P., Neel N.F., Salvo V.A., Zhu Y., Elliott S., et al. Cytokine receptor CXCR4 mediates estrogen-independent tumorigenesis, metastasis, and resistance to endocrine therapy in human breast cancer. Cancer Res 2011, 71:603-613.
133. Shi X.P., Miao S., Wu Y., Zhang W., Zhang X.F., Ma H.Z., et al. Resveratrol sensitizes tamoxifen in antiestrogen-resistant breast cancer cells with epithelial-mesenchymal transition features. Int J Mol Sci 2013, 14:15655-15668.
134. Yu Y., Xiao C.H., Tan L.D., Wang Q.S., Li X.Q., Feng Y.M. Cancer-associated fibroblasts induce epithelial-mesenchymal transition of breast cancer cells through paracrine TGF-beta signalling. Br J Cancer 2014, 110:724-732.
135. Saxena M., Stephens M.A., Pathak H., Rangarajan A. Transcription factors that mediate epithelial-mesenchymal transition lead to multidrug resistance by upregulating ABC transporters. Cell Death Dis 2011, 2:e179.
136. Hombauer H., Minguell J.J. Selective interactions between epithelial tumour cells and bone marrow mesenchymal stem cells. Br J Cancer 2000, 82:1290-1296.
137. Martin F.T., Dwyer R.M., Kelly J., Khan S., Murphy J.M., Curran C., et al. Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT). Breast Cancer Res Treat 2010, 124:317-326.
138. El-Haibi C.P., Bell G.W., Zhang J., Collmann A.Y., Wood D., Scherber C.M., et al. Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy. Proc Natl Acad Sci USA 2012, 109:17460-17465.
139. Shree T., Olson O.C., Elie B.T., Kester J.C., Garfall A.L., Simpson K., et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev 2011, 25:2465-2479.
140. Straussman R., Morikawa T., Shee K., Barzily-Rokni M., Qian Z.R., Du J., et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012, 487:500-504.
141. Maroun C.R., Rowlands T. The Met receptor tyrosine kinase: a key player in oncogenesis and drug resistance. Pharmacol Ther 2014, 142(3):316-338.
142. Ponzo M.G., Park M. The Met receptor tyrosine kinase and basal breast cancer. Cell Cycle 2010, 9:1043-1050.
143. Crawford Y., Kasman I., Yu L., Zhong C., Wu X., Modrusan Z., et al. PDGF-C mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment. Cancer Cell 2009, 15:21-34.
144. Massague J. TGFbeta in cancer. Cell 2008, 134:215-230.
145. Ikushima H., Miyazono K. TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 2010, 10:415-424.
146. Sabbah M., Emami S., Redeuilh G., Julien S., Prevost G., Zimber A., et al. Molecular signature and therapeutic perspective of the epithelial-to-mesenchymal transitions in epithelial cancers. Drug Resist Updat 2008, 11:123-151.
147. Mallini P., Lennard T., Kirby J., Meeson A. Epithelial-to-mesenchymal transition: what is the impact on breast cancer stem cells and drug resistance. Cancer Treat Rev 2014, 40:341-348.
148. Polyak K., Weinberg R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9:265-273.
149. Shipitsin M., Campbell L.L., Argani P., Weremowicz S., Bloushtain-Qimron N., Yao J., et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007, 11:259-273.
150. 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 USA 2009, 106:13805-13820.
151. Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
152. Park J., Schwarzbauer J.E. Mammary epithelial cell interactions with fibronectin stimulate epithelial-mesenchymal transition. Oncogene 2014, 33:1649-1657.
153. Yao Z., Fenoglio S., Gao D.C., Camiolo M., Stiles B., Lindsted T., et al. TGF-beta IL-6 axis mediates selective and adaptive mechanisms of resistance to molecular targeted therapy in lung cancer. Proc Natl Acad Sci USA 2010, 107:15535-15540.
154. Yamada D., Kobayashi S., Wada H., Kawamoto K., Marubashi S., Eguchi H., et al. Role of crosstalk between interleukin-6 and transforming growth factor-beta 1 in epithelial-mesenchymal transition and chemoresistance in biliary tract cancer. Eur J Cancer 2013, 49:1725-1740.
155. Yadav A., Kumar B., Datta J., Teknos T.N., Kumar P. IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 2011, 9:1658-1667.
156. Huang C., Yang G., Jiang T., Zhu G., Li H., Qiu Z. The effects and mechanisms of blockage of STAT3 signaling pathway on IL-6 inducing EMT in human pancreatic cancer cells in vitro. Neoplasma 2011, 58:396-405.
157. Bruna A., Greenwood W., Le Quesne J., Teschendorff A., Miranda-Saavedra D., Rueda O.M., et al. TGFbeta induces the formation of tumour-initiating cells in claudinlow breast cancer. Nat Commun 2012, 3.
158. Smith P.G., Tanaka H., Chantry A. A novel co-operative mechanism linking TGFbeta and Lyn kinase activation to imatinib resistance in chronic myeloid leukaemia cells. Oncotarget 2012, 3:518-524.
159. Pickup M., Novitskiy S., Moses H.L. The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 2013, 13:788-799.
160. Bhowmick N.A., Chytil A., Plieth D., Gorska A.E., Dumont N., Shappell S., et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004, 303:848-851.
161. Soon P.S., Kim E., Pon C.K., Gill A.J., Moore K., Spillane A.J., et al. Breast cancer-associated fibroblasts induce epithelial-to-mesenchymal transition in breast cancer cells. Endocr Relat Cancer 2013, 20:1-12.
162. Orimo A., Gupta P.B., Sgroi D.C., Arenzana-Seisdedos F., Delaunay T., Naeem R., et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
163. Hartmann T.N., Burger J.A., Glodek A., Fujii N., Burger M. CXCR4 chemokine receptor and integrin signaling co-operate in mediating adhesion and chemoresistance in small cell lung cancer (SCLC) cells. Oncogene 2005, 24:4462-4471.
164. Muerkoster S., Wegehenkel K., Arlt A., Witt M., Sipos B., Kruse M.L., et al. Tumor stroma interactions induce chemoresistance in pancreatic ductal carcinoma cells involving increased secretion and paracrine effects of nitric oxide and interleukin-1beta. Cancer Res 2004, 64:1331-1337.
165. Johansson A.C., Ansell A., Jerhammar F., Lindh M.B., Grenman R., Munck-Wikland E., et al. Cancer-associated fibroblasts induce matrix metalloproteinase-mediated cetuximab resistance in head and neck squamous cell carcinoma cells. Mol Cancer Res 2012, 10:1158-1168.
166. Bluguermann C., Wu L., Petrigliano F., McAllister D., Miriuka S., Evseenko D.A. Novel aspects of parenchymal-mesenchymal interactions: from cell types to molecules and beyond. Cell Biochem Funct 2013, 31:271-280.
167. Frenette P.S., Pinho S., Lucas D., Scheiermann C. Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu Rev Immunol 2013, 31:285-316.
168. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
169. Houthuijzen J.M., Daenen L.G., Roodhart J.M., Voest E.E. The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression. Br J Cancer 2012, 106:1901-1906.
170. Matsunaga T., Takemoto N., Sato T., Takimoto R., Tanaka I., Fujimi A., et al. Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med 2003, 9:1158-1165.
171. McMillin D.W., Delmore J., Weisberg E., Negri J.M., Geer D.C., Klippel S., et al. Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity. Nat Med 2010, 16:483-489.
172. Scherzed A., Hackenberg S., Froelich K., Kessler M., Koehler C., Hagen R., et al. BMSC enhance the survival of paclitaxel treated squamous cell carcinoma cells in vitro. Cancer Biol Ther 2011, 11:349-357.
173. Kucerova L., Skolekova S., Matuskova M., Bohac M., Kozovska Z. Altered features and increased chemosensitivity of human breast cancer cells mediated by adipose tissue-derived mesenchymal stromal cells. BMC Cancer 2013, 13:535.
174. Nefedova Y., Cheng P., Alsina M., Dalton W.S., Gabrilovich D.I. Involvement of Notch-1 signaling in bone marrow stroma-mediated de novo drug resistance of myeloma and other malignant lymphoid cell lines. Blood 2004, 103:3503-3510.
175. Lwin T., Hazlehurst L.A., Dessureault S., Lai R., Bai W., Sotomayor E., et al. Cell adhesion induces p27Kip1-associated cell-cycle arrest through down-regulation of the SCFSkp2 ubiquitin ligase pathway in mantle-cell and other non-Hodgkin B-cell lymphomas. Blood 2007, 110:1631-1638.
176. Nefedova Y., Landowski T.H., Dalton W.S. Bone marrow stromal-derived soluble factors and direct cell contact contribute to de novo drug resistance of myeloma cells by distinct mechanisms. Leukemia 2003, 17:1175-1182.
177. Hao M., Zhang L., An G., Meng H., Han Y., Xie Z., et al. Bone marrow stromal cells protect myeloma cells from bortezomib induced apoptosis by suppressing microRNA-15a expression. Leuk Lymphoma 2011, 52:1787-1794.
178. Xu Y., Tabe Y., Jin L., Watt J., McQueen T., Ohsaka A., et al. TGF-beta receptor kinase inhibitor LY2109761 reverses the anti-apoptotic effects of TGF-beta1 in myelo-monocytic leukaemic cells co-cultured with stromal cells. Br J Haematol 2008, 142:192-201.
179. Zimmerlin L., Park T.S., Zambidis E.T., Donnenberg V.S., Donnenberg A.D. Mesenchymal stem cell secretome and regenerative therapy after cancer. Biochimie 2013, 95:2235-2245.
180. Sasser A.K., Sullivan N.J., Studebaker A.W., Hendey L.F., Axel A.E., Hall B.M. Interleukin-6 is a potent growth factor for ER-alpha-positive human breast cancer. FASEB J 2007, 21:3763-3770.
181. Zeng Z., Shi Y.X., Samudio I.J., Wang R.Y., Ling X., Frolova O., et al. Targeting the leukemia microenvironment by CXCR4 inhibition overcomes resistance to kinase inhibitors and chemotherapy in AML. Blood 2009, 113:6215-6224.
182. Vianello F., Villanova F., Tisato V., Lymperi S., Ho K.K., Gomes A.R., et al. Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis. Haematologica 2010, 95:1081-1089.
183. Lis R., Touboul C., Mirshahi P., Ali F., Mathew S., Nolan D.J., et al. Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int J Cancer 2011, 128:715-725.
184. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1408-1420.
185. Klopp A.H., Lacerda L., Gupta A., Debeb B.G., Solley T., Li L., et al. Mesenchymal stem cells promote mammosphere formation and decrease E-cadherin in normal and malignant breast cells. PLoS ONE 2010, 5:e12180.
186. Dittmer A., Hohlfeld K., Lutzkendorf J., Muller L.P., Dittmer J. Human mesenchymal stem cells induce E-cadherin degradation in breast carcinoma spheroids by activating ADAM10. Cell Mol Life Sci 2009, 66:3053-3065.
187. Bohrer L.R., Chuntova P., Bade L.K., Beadnell T.C., Leon R.P., Brady N.J., et al. Activation of the FGFR-STAT3 pathway in breast cancer cells induces a hyaluronan-rich microenvironment that licenses tumor formation. Cancer Res 2014, 74:374-386.
188. Ng M.R., Brugge J.S. A stiff blow from the stroma: collagen crosslinking drives tumor progression. Cancer Cell 2009, 16:455-457.
189. Roodhart J.M., Daenen L.G., Stigter E.C., Prins H.J., Gerrits J., Houthuijzen J.M., et al. Mesenchymal stem cells induce resistance to chemotherapy through the release of platinum-induced fatty acids. Cancer Cell 2011, 20:370-383.
190. Borghese C., Cattaruzza L., Pivetta E., Normanno N., De Luca A., Mazzucato M., et al. Gefitinib inhibits the cross-talk between mesenchymal stem cells and prostate cancer cells leading to tumor cell proliferation and inhibition of docetaxel activity. J Cell Biochem 2013, 114:1135-1144.
191. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007, 449:557-563.
192. Waterman R.S., Tomchuck S.L., Henkle S.L., Betancourt A.M. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. PLoS ONE 2010, 5:e10088.
193. Waterman R.S., Henkle S.L., Betancourt A.M. Mesenchymal stem cell 1 (MSC1)-based therapy attenuates tumor growth whereas MSC2-treatment promotes tumor growth and metastasis. PLoS ONE 2012, 7:e45590.
194. Ribeiro A., Laranjeira P., Mendes S., Velada I., Leite C., Andrade P., et al. Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells. Stem Cell Res Ther 2013, 4:125.
195. Subramanian A., Shu-Uin G., Kae-Siang N., Gauthaman K., Biswas A., Choolani M., et al. Human umbilical cord Wharton's jelly mesenchymal stem cells do not transform to tumor-associated fibroblasts in the presence of breast and ovarian cancer cells unlike bone marrow mesenchymal stem cells. J Cell Biochem 2012, 113:1886-1895.
196. Ehninger A., Trumpp A. The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J Exp Med 2011, 208:421-428.
197. Jin L., Tabe Y., Konoplev S., Xu Y., Leysath C.E., Lu H., et al. CXCR4 up-regulation by imatinib induces chronic myelogenous leukemia (CML) cell migration to bone marrow stroma and promotes survival of quiescent CML cells. Mol Cancer Ther 2008, 7:48-58.
198. Saki N., Abroun S., Hagh M.F., Asgharei F. Neoplastic bone marrow niche: hematopoietic and mesenchymal stem cells. Cell J 2011, 13:131-136.
199. Cabarcas S.M., Mathews L.A., Farrar W.L. The cancer stem cell niche - there goes the neighborhood. Int J Cancer 2011, 129:2315-2327.
200. Martinez F.O., Gordon S., Locati M., Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 2006, 177:7303-7311.
201. Mantovani A., Sica A., Locati M. Macrophage polarization comes of age. Immunity 2005, 23:344-346.
202. Sica A., Schioppa T., Mantovani A., Allavena P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 2006, 42:717-727.
203. Beatty G.L., Chiorean E.G., Fishman M.P., Saboury B., Teitelbaum U.R., Sun W., et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011, 331:1612-1616.
204. DeNardo D.G., Brennan D.J., Rexhepaj E., Ruffell B., Shiao S.L., Madden S.F., et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011, 1:54-67.
205. Paulus P., Stanley E.R., Schafer R., Abraham D., Aharinejad S. Colony-stimulating factor-1 antibody reverses chemoresistance in human MCF-7 breast cancer xenografts. Cancer Res 2006, 66:4349-4356.
206. Chung F.T., Lee K.Y., Wang C.W., Heh C.C., Chan Y.F., Chen H.W., et al. Tumor-associated macrophages correlate with response to epidermal growth factor receptor-tyrosine kinase inhibitors in advanced non-small cell lung cancer. Int J Cancer 2012, 131:E227-E235.
207. Obermajer N., Jevnikar Z., Doljak B., Kos J. Role of cysteine cathepsins in matrix degradation and cell signalling. Connect Tissue Res 2008, 49:193-196.
208. Zheng X., Chu F., Chou P.M., Gallati C., Dier U., Mirkin B.L., et al. Cathepsin L inhibition suppresses drug resistance in vitro and in vivo: a putative mechanism. Am J Physiol Cell Physiol 2009, 296:C65-C74.
209. Courtney K.D., Corcoran R.B., Engelman J.A. The PI3K pathway as drug target in human cancer. J Clin Oncol 2010, 28:1075-1083.
210. Fuchs D., Daniel V., Sadeghi M., Opelz G., Naujokat C. Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 2010, 394:1098-1104.
211. 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 USA 2011, 108:13253-13257.
212. Mertins S.D. Cancer stem cells: a systems biology view of their role in prognosis and therapy. Anticancer Drugs 2014, 25:353-367.
213. Quail D.F., Joyce J.A. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013, 19:1423-1437.
214. Droujinine I.A., Eckert M.A., Zhao W. To grab the stroma by the horns: from biology to cancer therapy with mesenchymal stem cells. Oncotarget 2013, 4:651-664.