Skip to main content
Top
Published in: Molecular Cancer 1/2015

Open Access 01-12-2015 | Research

The chemokine receptor CCR6 facilitates the onset of mammary neoplasia in the MMTV-PyMT mouse model via recruitment of tumor-promoting macrophages

Authors: Sarah T. Boyle, Jessica W. Faulkner, Shaun R. McColl, Marina Kochetkova

Published in: Molecular Cancer | Issue 1/2015

Login to get access

Abstract

Background

The expression of the chemokine receptor CCR6 has been previously correlated with higher grades and stages of breast cancer and decreased relapse-free survival. Also, its cognate chemokine ligand CCL20 has been reported to induce proliferation of cultured human breast epithelial cells.

Methods

To establish if CCR6 plays a functional role in mammary tumorigenesis, a bigenic MMTV-PyMT CCR6-null mouse was generated and mammary tumor development was assessed. Levels of tumor-infiltrating immune cells within tumor-bearing mammary glands from MMTV-PyMT Ccr6 WT and Ccr6 −/− mice were also analyzed.

Results

Deletion of CCR6 delayed tumor onset, significantly reduced the extent of initial hyperplastic outgrowth, and decreased tumor incidence in PyMT transgenic mice. CCR6 was then shown to promote the recruitment of pro-tumorigenic macrophages to the tumor site, facilitating the onset of neoplasia.

Conclusions

This study delineated for the first time a role for CCR6 in the development of breast cancer, and demonstrated a critical function for this receptor in maintaining the pro-tumorigenic cancer microenvironment.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Hong CC, Yao S, McCann SE, Dolnick RY, Wallace PK, Gong Z, et al. Pretreatment levels of circulating Th1 and Th2 cytokines, and their ratios, are associated with ER-negative and triple negative breast cancers. Breast Cancer Res Treat. 2013;139:477–88.PubMedCentralPubMedCrossRef Hong CC, Yao S, McCann SE, Dolnick RY, Wallace PK, Gong Z, et al. Pretreatment levels of circulating Th1 and Th2 cytokines, and their ratios, are associated with ER-negative and triple negative breast cancers. Breast Cancer Res Treat. 2013;139:477–88.PubMedCentralPubMedCrossRef
3.
go back to reference Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4:71–8.PubMedCrossRef Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4:71–8.PubMedCrossRef
4.
go back to reference Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010;22:231–7.PubMedCrossRef Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010;22:231–7.PubMedCrossRef
5.
go back to reference Galdiero MR, Garlanda C, Jaillon S, Marone G, Mantovani A. Tumor associated macrophages and neutrophils in tumor progression. J Cell Physiol. 2013;228:1404–12.PubMedCrossRef Galdiero MR, Garlanda C, Jaillon S, Marone G, Mantovani A. Tumor associated macrophages and neutrophils in tumor progression. J Cell Physiol. 2013;228:1404–12.PubMedCrossRef
7.
go back to reference Iwasaki A, Kelsall BL. Localization of distinct Peyer’s patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J Exp Med. 2000;191:1381–94.PubMedCentralPubMedCrossRef Iwasaki A, Kelsall BL. Localization of distinct Peyer’s patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J Exp Med. 2000;191:1381–94.PubMedCentralPubMedCrossRef
8.
go back to reference Greaves DR, Wang W, Dairaghi DJ, Dieu MC, Saint-Vis B, Franz-Bacon K, et al. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J Exp Med. 1997;186:837–44.PubMedCentralPubMedCrossRef Greaves DR, Wang W, Dairaghi DJ, Dieu MC, Saint-Vis B, Franz-Bacon K, et al. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J Exp Med. 1997;186:837–44.PubMedCentralPubMedCrossRef
9.
go back to reference Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol. 2008;181:8391–401.PubMedCentralPubMedCrossRef Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B, et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol. 2008;181:8391–401.PubMedCentralPubMedCrossRef
11.
go back to reference Kleeff J, Kusama T, Rossi DL, Ishiwata T, Maruyama H, Friess H, et al. Detection and localization of Mip-3alpha/LARC/Exodus, a macrophage proinflammatory chemokine, and its CCR6 receptor in human pancreatic cancer. Int J Cancer. 1999;81:650–7.PubMedCrossRef Kleeff J, Kusama T, Rossi DL, Ishiwata T, Maruyama H, Friess H, et al. Detection and localization of Mip-3alpha/LARC/Exodus, a macrophage proinflammatory chemokine, and its CCR6 receptor in human pancreatic cancer. Int J Cancer. 1999;81:650–7.PubMedCrossRef
12.
go back to reference Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003;14:409–26.PubMedCrossRef Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003;14:409–26.PubMedCrossRef
13.
go back to reference Xuan W, Qu Q, Zheng B, Xiong S, Fan GH. The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J Leukoc Biol. 2014;97(1):61–9.PubMedCrossRef Xuan W, Qu Q, Zheng B, Xiong S, Fan GH. The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J Leukoc Biol. 2014;97(1):61–9.PubMedCrossRef
14.
go back to reference Du D, Liu Y, Qian H, Zhang B, Tang X, Zhang T, et al. The effects of the CCR6/CCL20 biological axis on the invasion and metastasis of hepatocellular carcinoma. Int J Mol Sci. 2014;15:6441–52.PubMedCentralPubMedCrossRef Du D, Liu Y, Qian H, Zhang B, Tang X, Zhang T, et al. The effects of the CCR6/CCL20 biological axis on the invasion and metastasis of hepatocellular carcinoma. Int J Mol Sci. 2014;15:6441–52.PubMedCentralPubMedCrossRef
15.
go back to reference Liu F, Lv H, Jia X, Liu G, Li T, Xu Z, et al. CC chemokine receptor 6 expression predicts poor prognosis in hepatocellular carcinoma. J Surg Oncol. 2014;110:151–5.PubMedCrossRef Liu F, Lv H, Jia X, Liu G, Li T, Xu Z, et al. CC chemokine receptor 6 expression predicts poor prognosis in hepatocellular carcinoma. J Surg Oncol. 2014;110:151–5.PubMedCrossRef
16.
go back to reference Liu J, Ke F, Xu Z, Liu Z, Zhang L, Yan S, et al. CCR6 is a prognostic marker for overall survival in patients with colorectal cancer, and its overexpression enhances metastasis in vivo. PLoS One. 2014;9:e101137.PubMedCentralPubMedCrossRef Liu J, Ke F, Xu Z, Liu Z, Zhang L, Yan S, et al. CCR6 is a prognostic marker for overall survival in patients with colorectal cancer, and its overexpression enhances metastasis in vivo. PLoS One. 2014;9:e101137.PubMedCentralPubMedCrossRef
17.
go back to reference Nandi B, Pai C, Huang Q, Prabhala RH, Munshi NC, Gold JS. CCR6, the sole receptor for the chemokine CCL20, promotes spontaneous intestinal tumorigenesis. PLoS One. 2014;9:e97566.PubMedCentralPubMedCrossRef Nandi B, Pai C, Huang Q, Prabhala RH, Munshi NC, Gold JS. CCR6, the sole receptor for the chemokine CCL20, promotes spontaneous intestinal tumorigenesis. PLoS One. 2014;9:e97566.PubMedCentralPubMedCrossRef
18.
go back to reference Cheng XS, Li YF, Tan J, Sun B, Xiao YC, Fang XB, et al. CCL20 and CXCL8 synergize to promote progression and poor survival outcome in patients with colorectal cancer by collaborative induction of the epithelial-mesenchymal transition. Cancer Lett. 2014;348:77–87.PubMedCrossRef Cheng XS, Li YF, Tan J, Sun B, Xiao YC, Fang XB, et al. CCL20 and CXCL8 synergize to promote progression and poor survival outcome in patients with colorectal cancer by collaborative induction of the epithelial-mesenchymal transition. Cancer Lett. 2014;348:77–87.PubMedCrossRef
19.
go back to reference Wang L, Qin H, Li L, Zhang Y, Tu Y, Feng F, et al. Overexpression of CCL20 and its receptor CCR6 predicts poor clinical prognosis in human gliomas. Med Oncol. 2012;29:3491–7.PubMedCrossRef Wang L, Qin H, Li L, Zhang Y, Tu Y, Feng F, et al. Overexpression of CCL20 and its receptor CCR6 predicts poor clinical prognosis in human gliomas. Med Oncol. 2012;29:3491–7.PubMedCrossRef
20.
go back to reference Kirshberg S, Izhar U, Amir G, Demma J, Vernea F, Beider K, et al. Involvement of CCR6/CCL20/IL-17 axis in NSCLC disease progression. PLoS One. 2011;6:e24856.PubMedCentralPubMedCrossRef Kirshberg S, Izhar U, Amir G, Demma J, Vernea F, Beider K, et al. Involvement of CCR6/CCL20/IL-17 axis in NSCLC disease progression. PLoS One. 2011;6:e24856.PubMedCentralPubMedCrossRef
21.
go back to reference Ito M, Teshima K, Ikeda S, Kitadate A, Watanabe A, Nara M, et al. MicroRNA-150 inhibits tumor invasion and metastasis by targeting the chemokine receptor CCR6, in advanced cutaneous T-cell lymphoma. Blood. 2014;123:1499–511.PubMedCrossRef Ito M, Teshima K, Ikeda S, Kitadate A, Watanabe A, Nara M, et al. MicroRNA-150 inhibits tumor invasion and metastasis by targeting the chemokine receptor CCR6, in advanced cutaneous T-cell lymphoma. Blood. 2014;123:1499–511.PubMedCrossRef
22.
go back to reference Zeng W, Chang H, Ma M, Li Y. CCL20/CCR6 promotes the invasion and migration of thyroid cancer cells via NF-kappa B signaling-induced MMP-3 production. Exp Mol Pathol. 2014;97:184–90.PubMedCrossRef Zeng W, Chang H, Ma M, Li Y. CCL20/CCR6 promotes the invasion and migration of thyroid cancer cells via NF-kappa B signaling-induced MMP-3 production. Exp Mol Pathol. 2014;97:184–90.PubMedCrossRef
23.
go back to reference Cassier PA, Treilleux I, Bachelot T, Ray-Coquard I, Bendriss-Vermare N, Menetrier-Caux C, et al. Prognostic value of the expression of C-Chemokine Receptor 6 and 7 and their ligands in non-metastatic breast cancer. BMC Cancer. 2011;11:213.PubMedCentralPubMedCrossRef Cassier PA, Treilleux I, Bachelot T, Ray-Coquard I, Bendriss-Vermare N, Menetrier-Caux C, et al. Prognostic value of the expression of C-Chemokine Receptor 6 and 7 and their ligands in non-metastatic breast cancer. BMC Cancer. 2011;11:213.PubMedCentralPubMedCrossRef
24.
go back to reference Andre F, Cabioglu N, Assi H, Sabourin JC, Delaloge S, Sahin A, et al. Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer. Ann Oncol. 2006;17:945–51.PubMedCrossRef Andre F, Cabioglu N, Assi H, Sabourin JC, Delaloge S, Sahin A, et al. Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer. Ann Oncol. 2006;17:945–51.PubMedCrossRef
25.
go back to reference Marsigliante S, Vetrugno C, Muscella A. CCL20 induces migration and proliferation on breast epithelial cells. J Cell Physiol. 2013;228:1873–83.PubMedCrossRef Marsigliante S, Vetrugno C, Muscella A. CCL20 induces migration and proliferation on breast epithelial cells. J Cell Physiol. 2013;228:1873–83.PubMedCrossRef
26.
go back to reference Roberti MP, Arriaga JM, Bianchini M, Quinta HR, Bravo AI, Levy EM, et al. Protein expression changes during human triple negative breast cancer cell line progression to lymph node metastasis in a xenografted model in nude mice. Cancer Biol Ther. 2012;13:1123–40.PubMedCentralPubMedCrossRef Roberti MP, Arriaga JM, Bianchini M, Quinta HR, Bravo AI, Levy EM, et al. Protein expression changes during human triple negative breast cancer cell line progression to lymph node metastasis in a xenografted model in nude mice. Cancer Biol Ther. 2012;13:1123–40.PubMedCentralPubMedCrossRef
27.
go back to reference Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992;12:954–61.PubMedCentralPubMed Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992;12:954–61.PubMedCentralPubMed
28.
go back to reference Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol. 2003;163:2113–26.PubMedCentralPubMedCrossRef Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol. 2003;163:2113–26.PubMedCentralPubMedCrossRef
29.
go back to reference Boyle ST, Ingman WV, Poltavets V, Faulkner JW, Whitfield RJ, McColl SR, et al. The chemokine receptor CCR7 promotes mammary tumorigenesis through amplification of stem-like cells. Oncogene. 2015. doi:10.1038/onc.2015.66. Boyle ST, Ingman WV, Poltavets V, Faulkner JW, Whitfield RJ, McColl SR, et al. The chemokine receptor CCR7 promotes mammary tumorigenesis through amplification of stem-like cells. Oncogene. 2015. doi:10.​1038/​onc.​2015.​66.
30.
go back to reference Visvader JE, Smith GH. Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harb Perspect Biol. 2010;3(2):a004879. Visvader JE, Smith GH. Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harb Perspect Biol. 2010;3(2):a004879.
31.
go back to reference Boyle ST, Kochetkova M. Breast cancer stem cells and the immune system: promotion, evasion and therapy. J Mammary Gland Biol Neoplasia. 2014;19:203–11.PubMedCrossRef Boyle ST, Kochetkova M. Breast cancer stem cells and the immune system: promotion, evasion and therapy. J Mammary Gland Biol Neoplasia. 2014;19:203–11.PubMedCrossRef
33.
go back to reference Ma J, Lanza DG, Guest I, Uk-Lim C, Glinskii A, Glinsky G, et al. Characterization of mammary cancer stem cells in the MMTV-PyMT mouse model. Tumour Biol. 2012;33:1983–96.PubMedCrossRef Ma J, Lanza DG, Guest I, Uk-Lim C, Glinskii A, Glinsky G, et al. Characterization of mammary cancer stem cells in the MMTV-PyMT mouse model. Tumour Biol. 2012;33:1983–96.PubMedCrossRef
34.
go back to reference Schwab LP, Peacock DL, Majumdar D, Ingels JF, Jensen LC, Smith KD, et al. Hypoxia-inducible factor 1alpha promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res. 2012;14:R6.PubMedCentralPubMedCrossRef Schwab LP, Peacock DL, Majumdar D, Ingels JF, Jensen LC, Smith KD, et al. Hypoxia-inducible factor 1alpha promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res. 2012;14:R6.PubMedCentralPubMedCrossRef
35.
go back to reference Zhang M, Behbod F, Atkinson RL, Landis MD, Kittrell F, Edwards D, et al. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 2008;68:4674–82.PubMedCentralPubMedCrossRef Zhang M, Behbod F, Atkinson RL, Landis MD, Kittrell F, Edwards D, et al. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 2008;68:4674–82.PubMedCentralPubMedCrossRef
36.
go back to reference Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439:84–8.PubMedCrossRef Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439:84–8.PubMedCrossRef
37.
go back to reference Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17:1253–70.PubMedCentralPubMedCrossRef Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17:1253–70.PubMedCentralPubMedCrossRef
38.
go back to reference Laoui D, Movahedi K, Van Overmeire E, Van den Bossche J, Schouppe E, Mommer C, et al. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol. 2011;55:861–7.PubMedCrossRef Laoui D, Movahedi K, Van Overmeire E, Van den Bossche J, Schouppe E, Mommer C, et al. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int J Dev Biol. 2011;55:861–7.PubMedCrossRef
40.
go back to reference Laoui D, Van Overmeire E, Di Conza G, Aldeni C, Keirsse J, Morias Y, et al. Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population. Cancer Res. 2014;74:24–30.PubMedCrossRef Laoui D, Van Overmeire E, Di Conza G, Aldeni C, Keirsse J, Morias Y, et al. Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population. Cancer Res. 2014;74:24–30.PubMedCrossRef
41.
go back to reference Xiao X, Gaffar I, Guo P, Wiersch J, Fischbach S, Peirish L, et al. M2 macrophages promote beta-cell proliferation by up-regulation of SMAD7. Proc Natl Acad Sci U S A. 2014;111:E1211–20.PubMedCentralPubMedCrossRef Xiao X, Gaffar I, Guo P, Wiersch J, Fischbach S, Peirish L, et al. M2 macrophages promote beta-cell proliferation by up-regulation of SMAD7. Proc Natl Acad Sci U S A. 2014;111:E1211–20.PubMedCentralPubMedCrossRef
42.
go back to reference Ford AQ, Dasgupta P, Mikhailenko I, Smith EM, Noben-Trauth N, Keegan AD. Adoptive transfer of IL-4Ralpha + macrophages is sufficient to enhance eosinophilic inflammation in a mouse model of allergic lung inflammation. BMC Immunol. 2012;13:6.PubMedCentralPubMedCrossRef Ford AQ, Dasgupta P, Mikhailenko I, Smith EM, Noben-Trauth N, Keegan AD. Adoptive transfer of IL-4Ralpha + macrophages is sufficient to enhance eosinophilic inflammation in a mouse model of allergic lung inflammation. BMC Immunol. 2012;13:6.PubMedCentralPubMedCrossRef
43.
go back to reference Strachan DC, Ruffell B, Oei Y, Bissell MJ, Coussens LM, Pryer N, et al. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8 T cells. Oncoimmunology. 2013;2:e26968.PubMedCentralPubMedCrossRef Strachan DC, Ruffell B, Oei Y, Bissell MJ, Coussens LM, Pryer N, et al. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8 T cells. Oncoimmunology. 2013;2:e26968.PubMedCentralPubMedCrossRef
44.
go back to reference Varona R, Villares R, Carramolino L, Goya I, Zaballos A, Gutierrez J, et al. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J Clin Invest. 2001;107:R37–45.PubMedCentralPubMedCrossRef Varona R, Villares R, Carramolino L, Goya I, Zaballos A, Gutierrez J, et al. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J Clin Invest. 2001;107:R37–45.PubMedCentralPubMedCrossRef
45.
go back to reference Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ, et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity. 2000;12:495–503.PubMedCrossRef Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ, et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity. 2000;12:495–503.PubMedCrossRef
46.
go back to reference Xu L, Xu W, Qiu S, Xiong S. Enrichment of CCR6 + Foxp3+ regulatory T cells in the tumor mass correlates with impaired CD8+ T cell function and poor prognosis of breast cancer. Clin Immunol. 2010;135:466–75.PubMedCrossRef Xu L, Xu W, Qiu S, Xiong S. Enrichment of CCR6 + Foxp3+ regulatory T cells in the tumor mass correlates with impaired CD8+ T cell function and poor prognosis of breast cancer. Clin Immunol. 2010;135:466–75.PubMedCrossRef
47.
go back to reference O’Brien J, Martinson H, Durand-Rougely C, Schedin P. Macrophages are crucial for epithelial cell death and adipocyte repopulation during mammary gland involution. Development. 2012;139:269–75.PubMedCrossRef O’Brien J, Martinson H, Durand-Rougely C, Schedin P. Macrophages are crucial for epithelial cell death and adipocyte repopulation during mammary gland involution. Development. 2012;139:269–75.PubMedCrossRef
48.
go back to reference Ojalvo LS, King W, Cox D, Pollard JW. High-density gene expression analysis of tumor-associated macrophages from mouse mammary tumors. Am J Pathol. 2009;174:1048–64.PubMedCentralPubMedCrossRef Ojalvo LS, King W, Cox D, Pollard JW. High-density gene expression analysis of tumor-associated macrophages from mouse mammary tumors. Am J Pathol. 2009;174:1048–64.PubMedCentralPubMedCrossRef
49.
go back to reference Chen J, Yao Y, Gong C, Yu F, Su S, Chen J, et al. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell. 2011;19:541–55.PubMedCentralPubMedCrossRef Chen J, Yao Y, Gong C, Yu F, Su S, Chen J, et al. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell. 2011;19:541–55.PubMedCentralPubMedCrossRef
50.
go back to reference Lu H, Clauser KR, Tam WL, Frose J, Ye X, Eaton EN, et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol. 2014;16:1105–17.PubMedCentralPubMedCrossRef Lu H, Clauser KR, Tam WL, Frose J, Ye X, Eaton EN, et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol. 2014;16:1105–17.PubMedCentralPubMedCrossRef
51.
go back to reference Liu J, Zhang N, Li Q, Zhang W, Ke F, Leng Q, et al. Tumor-associated macrophages recruit CCR6+ regulatory T cells and promote the development of colorectal cancer via enhancing CCL20 production in mice. PLoS One. 2011;6:e19495.PubMedCentralPubMedCrossRef Liu J, Zhang N, Li Q, Zhang W, Ke F, Leng Q, et al. Tumor-associated macrophages recruit CCR6+ regulatory T cells and promote the development of colorectal cancer via enhancing CCL20 production in mice. PLoS One. 2011;6:e19495.PubMedCentralPubMedCrossRef
52.
go back to reference Karthaus N, Torensma R, Tel J. Deciphering the message broadcast by tumor-infiltrating dendritic cells. Am J Pathol. 2012;181:733–42.PubMedCrossRef Karthaus N, Torensma R, Tel J. Deciphering the message broadcast by tumor-infiltrating dendritic cells. Am J Pathol. 2012;181:733–42.PubMedCrossRef
53.
go back to reference Chan CW, Housseau F. The ‘kiss of death’ by dendritic cells to cancer cells. Cell Death Differ. 2008;15:58–69.PubMedCrossRef Chan CW, Housseau F. The ‘kiss of death’ by dendritic cells to cancer cells. Cell Death Differ. 2008;15:58–69.PubMedCrossRef
54.
go back to reference Gabrilovich DI, Corak J, Ciernik IF, Kavanaugh D, Carbone DP. Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin Cancer Res. 1997;3:483–90.PubMed Gabrilovich DI, Corak J, Ciernik IF, Kavanaugh D, Carbone DP. Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin Cancer Res. 1997;3:483–90.PubMed
Metadata
Title
The chemokine receptor CCR6 facilitates the onset of mammary neoplasia in the MMTV-PyMT mouse model via recruitment of tumor-promoting macrophages
Authors
Sarah T. Boyle
Jessica W. Faulkner
Shaun R. McColl
Marina Kochetkova
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2015
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-015-0394-1

Other articles of this Issue 1/2015

Molecular Cancer 1/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine