Non-tumorigenic epithelial cells secrete MCP-1 and other cytokines that promote cell division in breast cancer cells by activating ERα via PI3K/Akt/mTOR signaling

International Journal of Biochemistry and Cell Biology

Volumn 53, Issue , 2014, Pages 281-294

  Riverso, Maria ^a,c   Kortenkamp, Andreas ^b   Silva, Elisabete ^b  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b BRUNEL UNIVERSITY   (United Kingdom)

^c ISTITUTO TOSCANO TUMORI   (Italy)

Author keywords

Breast cancer; Estrogen receptor; MCP 1; Tumor microenvironment

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BETA ACTIN; BRCA1 PROTEIN; CASPASE 3; CASPASE 7; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR4; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYTOKINE; ESTROGEN RECEPTOR ALPHA; FULVESTRANT; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; MAMMALIAN TARGET OF RAPAMYCIN; MITOMYCIN; MONOCYTE CHEMOTACTIC PROTEIN 1; ONCOSTATIN M; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; TFF1 PROTEIN; UNCLASSIFIED DRUG; CCL2 PROTEIN, HUMAN; ESTROGEN RECEPTOR ALPHA, HUMAN; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; BREAST EPITHELIUM; CANCER CELL; CELL CONTACT; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MCF 7 CELL LINE; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TREATMENT DURATION; TUMOR MICROENVIRONMENT; UPREGULATION; BREAST TUMOR; EPITHELIUM CELL; FEMALE; GENETICS; METABOLISM; PATHOLOGY; SECRETION (PROCESS);

BREAST NEOPLASMS; CELL DIVISION; CHEMOKINE CCL2; EPITHELIAL CELLS; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; MCF-7 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84902456784     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.05.023     Document Type: Article

References (54)

1. J.A. Aka, J. Adjo Aka, and S.X. Lin Comparison of functional proteomic analyses of human breast cancer cell lines T47D and MCF7 PLoS ONE 7 2012 e31532
2. S. Ali, and R.C. Coombes Endocrine-responsive breast cancer and strategies for combating resistance Nat Rev Cancer 2 2002 101 112 (Pubitemid 37328797)
3. M.J. Bissell, and D. Radisky Putting tumours in context Nat Rev Cancer 1 2001 46 54 (Pubitemid 33741880)
4. C. Bolhito, M.A. Hahn, R.C. Baxter, and D.H. Marsh The chemokine CXCL1 induces proliferation in epithelial ovarian cancer cells by transactivation of the epidermal growth factor receptor Enodocr Relat Cancer 17 2010 929 940
5. P.M. Carpenter, A.V. Dao, Z.S. Arain, M.K. Chang, H.P. Nguyen, and S. Arain et al. Motility induction in breast carcinoma by mammary epithelial laminin 332 (laminin 5) Mol Cancer Res 7 2009 462 475
6. K.M. Coleman, and C.L. Smith Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors Front Biosci 6 2001 D1379 D1391
7. L.M. Coussens, and Z. Werb Inflammation and cancer Nature 420 2002 860 867 (Pubitemid 36019639)
8. S. Dawood, and M. Cristofanilli Endocrine resistance in breast cancer: what really matters? Ann Oncol 18 2007 1289 1291 (Pubitemid 47305000)
9. B.J. Deroo, and K.S. Korach Estrogen receptors and human disease J Clin Invest 116 2006 561 570 (Pubitemid 43326860)
10. R.M. Evans, S. Rahte, and A. Kortenkamp Inability to confirm estrogenicity of the heterocyclic amine PhIP in two in vitro assays Toxicol In Vitro 24 2010 1757 1763
11. C. Gabellini, D. Trisciuoglio, M. Desideri, A. Candiloro, Y. Ragazzoni, and A. Orlandi et al. Functional activity of CXCL8 receptors, CXCR1 and CXCR2, on human malignant melanoma progression Eur J Cancer 45 2009 2618 2627
12. A. Gompel, S. Somaï, M. Chaouat, A. Kazem, H.J. Kloosterboer, and I. Beusman et al. Hormonal regulation of apoptosis in breast cells and tissues Steroids 65 2000 593 598
13. I. Gori, C. Pellegrini, D. Staedler, R. Russell, C. Jan, and G.O. Canny Tumor necrosis factor-α activates estrogen signaling pathways in endometrial epithelial cells via estrogen receptor α Mol Cell Endocrinol 345 2011 27 37
14. S. Guo, I. Russo, and J. Russo Difference in gene expression profile in breast epithelial cells from women with different reproductive history Int J Oncol 23 2003 933 941
15. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
16. D.L. Holliday, K.T. Brouilette, A. Markert, L.A. Gordon, and J.L. Jones Novel multicellular organotypic models of normal and malignant breast: tools for dissecting the role of the microenvironment in breast cancer progression Breast Cancer Res 11 2009 R3
17. H. Inadera, T. Sekiya, T. Yoshimura, and K. Matsushima Molecular analysis of the inhibition of monocyte chemoattractant protein-1 gene expression by estrogens and xenoestrogens in MCF-7 cells Endocrinology 141 2000 50 59 (Pubitemid 32260344)
18. P.B. Joel, A.M. Traish, and D.A. Lannigan Estradiol and phorbol ester cause phosphorylation of serine 118 in the human estrogen receptor Mol Endocrinol 9 1995 1041 1052
19. C. Jones, J. Payne, D. Wells, J.D. Delhanty, S.R. Lakhani, and A. Kortenkamp Comparative genomic hybridization reveals extensive variation among different MCF-7 cell stocks Cancer Genet Cytogenet 117 2000 153 158 (Pubitemid 30125818)
20. R. Kalluri, and M. Zeisberg Fibroblasts in cancer Nat Rev Cancer 6 2006 392 401
21. A.E. Karnoub, A.B. Dash, A.P. Vo, A. Sullivan, M.W. Brooks, and G.W. Bell et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis Nature 449 2007 557 563 (Pubitemid 47525152)
22. G. Lazennec, and A. Richmond Chemokines and chemokine receptors: new insights into cancer-related inflammation Trends Mol Med 16 2010 133 144
23. M.A. Le Bitoux, and I. Stamenkovic Tumor-host interactions: the role of inflammation Histochem Cell Biol 130 2008 1079 1090
24. V.S. Likhite, F. Stossi, K. Kim, B.S. Katzenellenbogen, and J.A. Katzenellenbogen Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity Mol Endocrinol 20 2006 3120 3132 (Pubitemid 44833560)
25. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408 (Pubitemid 34164012)
26. R.D. Loberg, L.L. Day, J. Harwood, C. Ying, L.N. St John, and R. Giles et al. CCL2 is a potent regulator of prostate cancer cell migration and proliferation Neoplasia 8 2006 578 586 (Pubitemid 44061313)
27. Z. Lu, G. Jiang, P. Blume-Jensen, and T. Hunter Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase Mol Cell Biol 21 2001 4016 4031 (Pubitemid 32476463)
28. S. Marchese, and E. Silva Disruption of 3D MCF-12A breast cell cultures by estrogens - an in vitro model for ER-mediated changes indicative of hormonal carcinogenesis PLoS ONE 7 2012 e45767
29. M. Mestdagt, M. Polette, G. Buttice, A. Noël, A. Ueda, and J.M. Foidart et al. Transactivation of MCP-1/CCL2 by beta-catenin/TCF-4 in human breast cancer cells Int J Cancer 118 2006 35 42 (Pubitemid 41681578)
30. M.M. Mueller, and N.E. Fusenig Friends or foes - bipolar effects of the tumour stroma in cancer Nat Rev Cancer 4 2004 839 849 (Pubitemid 39472951)
31. E.A. Musgrove, and R.L. Sutherland Biological determinants of endocrine resistance in breast cancer Nat Rev Cancer 9 2009 631 643
32. R. O'Lone, M.C. Frith, E.K. Karlsson, and U. Hansen Genomic targets of nuclear estrogen receptors Mol Endocrinol 18 2004 1859 1875 (Pubitemid 39022608)
33. M. Ohta, Y. Kitadai, S. Tanaka, M. Yoshihara, W. Yasui, and N. Mukaida et al. Monocyte chemoattractant protein-1 expression correlates with macrophage infiltration and tumor vascularity in human esophageal squamous cell carcinomas Int J Cancer 102 2002 220 224 (Pubitemid 35222287)
34. C.K. Osborne, and R. Schiff Mechanisms of endocrine resistance in breast cancer Annu Rev Med 62 2011 233 247
35. J.M. Poczobutt, J. Tentler, X. Lu, P.J. Schedin, and A. Gutierrez-Hartmann Benign mammary epithelial cells enhance the transformed phenotype of human breast cancer cells BMC Cancer 10 2010 373
36. L.V. Rhodes, J. Antoon, E. Muir, S. Elliott, B.S. Beckman, and M. Burrow Effects of human mesenchymal stem cells on ER-positive human breast carcinoma cells mediated through ER-SDF-1/CXCR4 crosstalk Mol Cancer 9 2010 295
37. L.V. Rhodes, S.P. Short, N.F. Neel, V.A. Salvo, Y. Zhu, and S. Elliott et al. Cytokine receptor CXCR4 mediates estrogen-independent tumorigenesis, metastasis, and resistance to endocrine therapy in human breast cancer Cancer Res 71 2011 603 613
38. R. Riggins, R. Schrecengost, M. Guerrero, and A. Bouton Pathways to tamoxifen resistance Cancer Lett 256 2007 1 24 (Pubitemid 47333324)
39. H. Saji, M. Koike, T. Yamori, S. Saji, M. Seiki, and K. Matsushima et al. Significant correlation of monocyte chemoattractant protein-1 expression with neovascularization and progression of breast carcinoma Cancer 92 2001 1085 1091 (Pubitemid 32861655)
40. K. Sauvé, J. Lepage, M. Sanchez, N. Heveker, and A. Tremblay Positive feedback activation of estrogen receptors by the CXCL12-CXCR4 pathway Cancer Res 69 2009 5793 5800
41. R. Schiff, S.A. Massarweh, J. Shou, L. Bharwani, G. Arpino, and M. Rimawi et al. Advanced concepts in estrogen receptor biology and breast cancer endocrine resistance: implicated role of growth factor signaling and estrogen receptor coregulators Cancer Chemother Pharmacol 56 Suppl. 1 2005 10 20
42. R. Schiff, S.A. Massarweh, J. Shou, L. Bharwani, S.K. Mohsin, and C.K. Osborne Cross-talk between estrogen receptor and growth factor pathways as a molecular target for overcoming endocrine resistance Clin Cancer Res 10 2004 331S 336S (Pubitemid 38116639)
43. Y.M. Shah, and B.G. Rowan The Src kinase pathway promotes tamoxifen agonist action in Ishikawa endometrial cells through phosphorylation-dependent stabilization of estrogen receptor (alpha) promoter interaction and elevated steroid receptor coactivator 1 activity Mol Endocrinol 19 2005 732 748 (Pubitemid 40349444)
44. E. Silva, M.J. Lopez-Espinosa, J.M. Molina-Molina, M. Fernández, N. Olea, and A. Kortenkamp Lack of activity of cadmium in in vitro estrogenicity assays Toxicol Appl Pharmacol 216 2006 20 28 (Pubitemid 44402630)
45. E. Silva, M. Scholze, and A. Kortenkamp Activity of xenoestrogens at nanomolar concentrations in the E-Screen assay Environ Health Perspect 115 Suppl. 1 2007 91 97
46. G. Soria, M. Ofri-Shahak, I. Haas, N. Yaal-Hahoshen, L. Leider-Trejo, and T. Leibovich-Rivkin et al. Inflammatory mediators in breast cancer: coordinated expression of TNFα & IL-1β with CCL2 & CCL5 and effects on epithelial-to-mesenchymal transition BMC Cancer 11 2011 130
47. B.C. Spink, R.W. Cole, B.H. Katz, J.F. Gierthy, L.M. Bradley, and D.C. Spink Inhibition of MCF-7 breast cancer cell proliferation by MCF-10A breast epithelial cells in coculture Cell Biol Int 30 2006 227 238 (Pubitemid 43276448)
48. R.A. Toillon, V. Chopin, N. Jouy, W. Fauquette, B. Boilly, and X. le Bourhis Normal breast epithelial cells induce p53-dependent apoptosis and p53-independent cell cycle arrest of breast cancer cells Breast Cancer Res Treat 71 2002 269 280 (Pubitemid 34263990)
49. A. Tsuyada, A. Chow, J. Wu, G. Somlo, P. Chu, and S. Loera et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells Cancer Res 72 2012 2768 2779
50. K. Vanderkerken, I. Vande Broek, D.L. Eizirik, E. Van Valckenborgh, K. Asosingh, and I. Van Riet et al. Monocyte chemoattractant protein-1 (MCP-1), secreted by bone marrow endothelial cells, induces chemoattraction of 5T multiple myeloma cells Clin Exp Metastasis 19 2002 87 90 (Pubitemid 34208358)
51. M. Villalobos, N. Olea, J.A. Brotons, M.F. Olea-Serrano, J.M. Ruiz de Almodovar, and V. Pedraza The E-screen assay: a comparison of different MCF7 cell stocks Environ Health Perspect 103 1995 844 850
52. D.J. Waugh, and C. Wilson The inteleukin-8 pathway in cancer Clin Cancer Res 34 2008 55 58
53. V.S. Wilson, K. Bobseine, and L.E. Gray Development and characterization of a cell line that stably expresses an estrogen-responsive luciferase reporter for the detection of estrogen receptor agonist and antagonists Toxicol Sci 81 2004 69 77 (Pubitemid 39199865)
54. M. Zilli, A. Grassadonia, N. Tinari, A. di Giacobbe, S. Gildetti, and J. Giampietro et al. Molecular mechanisms of endocrine resistance and their implication in the therapy of breast cancer Biochim Biophys Acta 1795 2009 62 81