Cancer-associated fibroblast-secreted CXCL16 attracts monocytes to promote stroma activation in triple-negative breast cancers

Nature Communications

Volumn 7, Issue , 2016, Pages

  Allaoui, Roni ^a   Bergenfelz, Caroline ^a   Mohlin, Sofie ^a   Hagerling, Catharina ^a,b   Salari, Kiarash ^b   Werb, Zena ^b   Anderson, Robin L ^c   Ethier, Stephen P ^d   Jirström, Karin ^e   Påhlman, Sven ^a   Bexell, Daniel ^a   Tahin, Balázs ^f   Johansson, Martin E ^a,f   Larsson, Christer ^a   Leandersson, Karin ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e LUND UNIVERSITY   (Sweden)

^f LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AMPHIREGULIN; CALGRANULIN B; CD123 ANTIGEN; CD16 ANTIGEN; CD163 ANTIGEN; CD19 ANTIGEN; CD3 ANTIGEN; CD56 ANTIGEN; CD7 ANTIGEN; CHLORDANE; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 5; COLLAGEN TYPE 6; CXCL16 CHEMOKINE; ENDOTHELIN 1; GELATINASE B; GLYCOPHORIN A; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 8; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NONFIBRILLAR COLLAGEN; STROMAL CELL DERIVED FACTOR 1; THROMBOCYTE FACTOR 4; TISSUE INHIBITOR OF METALLOPROTEINASE 1; VIMENTIN; CHEMOTACTIC FACTOR; COLLAGEN; CXCL16 PROTEIN, HUMAN;

CANCER; CELLS AND CELL COMPONENTS; CHEMICAL BINDING; DRUG RESISTANCE; GENE EXPRESSION; PHENOTYPE; PHYSIOLOGICAL RESPONSE; SURVIVAL; TUMOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CANCER ASSOCIATED FIBROBLAST; CELL ACTIVATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LUMINAL A BREAST CANCER; MONOCYTE; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; STROMA; STROMA CELL; SUPPRESSOR CELL; TRIPLE NEGATIVE BREAST CANCER; TUMOR MICROENVIRONMENT; ANIMAL; COCULTURE; DRUG EFFECT; DRUG SCREENING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; NUDE MOUSE; PATHOLOGY; SECRETION (PROCESS); SOLUBILITY; TUMOR CELL LINE;

ANIMALS; CANCER-ASSOCIATED FIBROBLASTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CHEMOKINE CXCL16; CHEMOTACTIC FACTORS; COCULTURE TECHNIQUES; COLLAGEN; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOSUPPRESSION; MICE, NUDE; MONOCYTES; MYELOID CELLS; SOLUBILITY; STROMAL CELLS; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84991394206     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13050     Document Type: Article

References (55)

1. Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumour subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869-10874 (2001).
2. Gierach, G. L., Burke, A. & Anderson, W. F. Epidemiology of triple negative breast cancers. Breast Dis. 32, 5-24 (2010).
3. de Kruijf, E. M. et al. Tumor-stroma ratio in the primary tumour is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients. Breast Cancer Res. Treat. 125, 687-696 (2011).
4. Medrek, C., Ponten, F., Jirstrom, K. & Leandersson, K. The presence of tumour associated macrophages in tumour stroma as a prognostic marker for breast cancer patients. BMC Cancer 12, 306 (2012).
5. Moorman, A. M., Vink, R., Heijmans, H. J., van der Palen, J. & Kouwenhoven, E. A. The prognostic value of tumour-stroma ratio in triple-negative breast cancer. Eur. J. Surg. Oncol. 38, 307-313 (2012).
6. Pietras, K. & Ostman, A. Hallmarks of cancer: interactions with the tumour stroma. Exp. Cell Res. 316, 1324-1331 (2010).
7. Conklin, M. W. & Keely, P. J. Why the stroma matters in breast cancer: insights into breast cancer patient outcomes through the examination of stromal biomarkers. Cell Adh. Migr. 6, 249-260 (2012).
8. Anderberg, C. & Pietras, K. On the origin of cancer-associated fibroblasts. Cell Cycle 8, 1461-1462 (2009).
9. Joyce, J. A. & Pollard, J. W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252 (2009).
10. Bergenfelz, C. et al. Systemic monocytic-MDSCs are generated from monocytes and correlate with disease progression in breast cancer patients. PLoS ONE 10, e0127028 (2015).
11. Stromnes, I. M., Greenberg, P. D. & Hingorani, S. R. Molecular pathways: myeloid complicity in cancer. Clin. Cancer Res. 20, 5157-5170 (2014).
12. Leek, R. D. et al. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 56, 4625-4629 (1996).
13. Qian, B. et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS ONE 4, e6562 (2009).
14. Qian, B. Z. & Pollard, J. W. New tricks for metastasis-associated macrophages. Breast Cancer Res. 14, 316 (2012).
15. Gabrilovich, D. I. & Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174 (2009).
16. Ostrand-Rosenberg, S. & Sinha, P. Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 182, 4499-4506 (2009).
17. Pollard, J. W. Macrophages define the invasive microenvironment in breast cancer. J. Leukoc. Biol. 84, 623-630 (2008).
18. Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222-225 (2011).
19. Elkabets, M. et al. Human tumours instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice. J. Clin. Invest. 121, 784-799 (2011).
20. Klemm, F. & Joyce, J. A. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol. 25, 198-213 (2015).
21. Bergenfelz, C. et al. S100A9 expressed in ER(-)PgR(-) breast cancers induces inflammatory cytokines and is associated with an impaired overall survival. Br. J. Cancer 113, 1234-1243 (2015).
22. Tanaka, S. et al. Development of mature and functional human myeloid subsets in hematopoietic stem cell-engrafted NOD/SCID/IL2rgammaKO mice. J. Immunol. 188, 6145-6155 (2012).
23. Mehmeti, M. et al. Expression of functional toll like receptor 4 in estrogen receptor/progesterone receptor-negative breast cancer. Breast Cancer Res. 17, 130 (2015).
24. Ndlovu, M. N. et al. Hyperactivated NF-{kappa}B and AP-1 transcription factors promote highly accessible chromatin and constitutive transcription across the interleukin-6 gene promoter in metastatic breast cancer cells. Mol. Cell. Biol. 29, 5488-5504 (2009).
25. Johnstone, C. N. et al. Functional and molecular characterisation of EO771.LMB tumours, a new C57BL/6-mouse-derived model of spontaneously metastatic mammary cancer. Dis. Model. Mech. 8, 237-251 (2015).
26. Riva, M., He, Z., Kallberg, E., Ivars, F. & Leanderson, T. Human S100A9 protein is stabilized by inflammatory stimuli via the formation of proteolyticallyresistant homodimers. PLoS ONE 8, e61832 (2013).
27. Fang, M., Yuan, J., Peng, C. & Li, Y. Collagen as a double-edged sword in tumour progression. Tumour Biol. 35, 2871-2882 (2014).
28. Schnoor, M. et al. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J. Immunol. 180, 5707-5719 (2008).
29. Chen, P., Cescon, M. & Bonaldo, P. Collagen VI in cancer and its biological mechanisms. Trends Mol. Med. 19, 410-417 (2013).
30. Cathcart, J., Pulkoski-Gross, A. & Cao, J. Targeting matrix metalloproteinases in cancer: bringing new life to old ideas. Genes Dis. 2, 26-34 (2015).
31. Junqueira, L. C., Bignolas, G. & Brentani, R. R. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem. J. 11, 447-455 (1979).
32. Busser, B., Sancey, L., Brambilla, E., Coll, J. L. & Hurbin, A. The multiple roles of amphiregulin in human cancer. Biochim. Biophys. Acta 1816, 119-131 (2011).
33. Wang, J. H. et al. CXCR6 deficiency attenuates pressure overload-induced monocytes migration and cardiac fibrosis through downregulating TNF-alphadependent MMP9 pathway. Int. J. Clin. Exp. Pathol. 7, 6514-6523 (2014).
34. Xia, Y., Entman, M. L. & Wang, Y. Critical role of CXCL16 in hypertensive kidney injury and fibrosis. Hypertension 62, 1129-1137 (2013).
35. Xia, Y., Jin, X., Yan, J., Entman, M. L. & Wang, Y. CXCR6 plays a critical role in angiotensin II-induced renal injury and fibrosis. Arterioscler. Thromb. Vasc. Biol. 34, 1422-1428 (2014).
36. Yamamoto, K., Murphy, G. & Troeberg, L. Extracellular regulation of metalloproteinases. Matrix Biol. 44-46, 255-263 (2015).
37. Zhao, F. et al. S100A9 a new marker for monocytic human myeloid-derived suppressor cells. Immunology 136, 176-183 (2012).
38. Cheng, P. et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J. Exp. Med. 205, 2235-2249 (2008).
39. Hollmen, M., Roudnicky, F., Karaman, S. & Detmar, M. Characterization of macrophage-cancer cell crosstalk in estrogen receptor positive and triple-negative breast cancer. Sci. Rep. 5, 9188 (2015).
40. Su, S. et al. A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell 25, 605-620 (2014).
41. Deguchi, J. O. et al. Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 112, 2708-2715 (2005).
42. Karousou, E. et al. Collagen VI and hyaluronan: the common role in breast cancer. Biomed. Res. Int. 2014, 606458 (2014).
43. Everts, V., Korper, W., Niehof, A., Jansen, I. & Beertsen, W. Type VI collagen is phagocytosed by fibroblasts and digested in the lysosomal apparatus: involvement of collagenase, serine proteinases and lysosomal enzymes. Matrix Biol. 14, 665-676 (1995).
44. Xia, Y., Yan, J., Jin, X., Entman, M. L. & Wang, Y. The chemokine receptor CXCR6 contributes to recruitment of bone marrow-derived fibroblast precursors in renal fibrosis. Kidney Int. 86, 327-337 (2014).
45. Xing, Z., Tremblay, G. M., Sime, P. J. & Gauldie, J. Overexpression of granulocyte-macrophage colony-stimulating factor induces pulmonary granulation tissue formation and fibrosis by induction of transforming growth factor-beta 1 and myofibroblast accumulation. Am. J. Pathol. 150, 59-66 (1997).
46. Wang, Z. & Huang, H. Platelet factor-4 (CXCL4/PF-4): an angiostatic chemokine for cancer therapy. Cancer Lett. 331, 147-153 (2013).
47. Zhang, Y. et al. CXCL4 mediates tumour regrowth after chemotherapy by suppression of antitumor immunity. Cancer Biol. Ther. 16, 1775-1783 (2015).
48. Meyer, T. P. et al. Filter Buffy Coats (FBC): a source of peripheral blood leukocytes recovered from leukocyte depletion filters. J. Immunol. Methods 307, 150-166 (2005).
49. Hashimoto, S., Yamada, M., Motoyoshi, K. & Akagawa, K. S. Enhancement of macrophage colony-stimulating factor-induced growth and differentiation of human monocytes by interleukin-10. Blood 89, 315-321 (1997).
50. Lawson, D. A. et al. Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells. Nature 526, 131-135 (2015).
51. DeRose, Y. S. et al. Tumor grafts derived from women with breast cancer authentically reflect tumour pathology, growth, metastasis and disease outcomes. Nat. Med. 17, 1514-1520 (2011).
52. Gronberg, M., Fjallskog, M. L., Jirstrom, K. & Janson, E. T. Expression of ghrelin is correlated to a favorable outcome in invasive breast cancer. Acta Oncol. 51, 386-393 (2012).
53. Bergenfelz, C. et al. Wnt5a induces a tolerogenic phenotype of macrophages in sepsis and breast cancer patients. J. Immunol. 188, 5448-5458 (2012).
54. Vandesompele, J. et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034 (2002).
55. Parker, J. S. et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol. 27, 1160-1167 (2009).