Lung metastasis fails in MMTV-PyMT oncomice lacking S100A4 due to a T-cell deficiency in primary tumors

Cancer Research

Volumn 70, Issue 3, 2010, Pages 936-947

  Grum Schwensen, Birgitte ^a   Klingelhöfer, Jörg ^a   Grigorian, Mariam ^b   Almholt, Kasper ^b,c   Nielsen, Boye Schnack ^a,d   Lukanidin, Eugene ^a   Ambartsumian, Noona ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b FINSEN LABORATORY   (Denmark)

^c NOVO NORDISK A S   (Denmark)

^d Exiqon AS   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CALVASCULIN; EOTAXIN 2; GRANULOCYTE COLONY STIMULATING FACTOR; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL INFILTRATION; CELL INTERACTION; CELL INVASION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FIBROBLAST; INFLAMMATION; KNOCKOUT GENE; LEUKOCYTE; LUNG METASTASIS; MALIGNANT TRANSFORMATION; MICROENVIRONMENT; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; STROMA CELL; T LYMPHOCYTE; TUMOR GROWTH;

ANIMALS; BLOTTING, WESTERN; CHEMOKINE CCL24; CYTOKINES; FEMALE; FIBROBLASTS; GRANULOCYTE COLONY-STIMULATING FACTOR; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, KNOCKOUT; RETROVIRIDAE INFECTIONS; S100 PROTEINS; T-LYMPHOCYTES; TUMOR VIRUS INFECTIONS;

EID: 76249122307     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-3220     Document Type: Article

References (46)

1. DeNardo DG, Johansson M, Coussens LM. Immune cells as mediators of solid tumor metastasis. Cancer Metastasis Rev 2008;27: 11-8.
2. Lin EY, Li JF, Gnatovskiy L, et al. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006; 66:11238-46.
3. Kim S, Takahashi H, Lin WW, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009;457:102-6.
4. DeNardo DG, Coussens LM. Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression. Breast Cancer Res 2007;9:212.
5. + T cells secreting interleukin-10 and transforming growth factor-β1 mediates suppression in the tumor microenvironment. Clin Cancer Res 2007; 13:4345-54.
6. DeNardo DG, Barreto JB, Andreu P, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009;16: 91-102.
7. 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.
8. Lin EY, Jones JG, Li P, 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.
9. Garrett SC, Varney KM, Weber DJ, Bresnick AR. S100A4, a mediator of metastasis. J Biol Chem 2006;281:677-80.
10. Yao R, Davidson DD, Lopez-Beltran A, Maclennan GT, Montironi R, Cheng L. The S100 proteins for screening and prognostic grading of bladder cancer. Histol Histopathol 2007;22:1025-32.
11. Cabezon T, Celis JE, Skibshoj I, et al. Expression of S100A4 by a variety of cell types present in the tumor microenvironment of human breast cancer. Int J Cancer 2007;121:1433-44.
12. Schmidt-Hansen B, Klingelhofer J, Grum-Schwensen B, et al. Functional significance of metastasis-inducing S100A4(Mts1) in tumorstroma interplay. J Biol Chem 2004;279:24498-504.
13. Ambartsumian N, Klingelhofer J, Grigorian M, et al. The metastasisassociated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 2001;20:4685-95.
14. Novitskaya V, Grigorian M, Kriajevska M, et al. Oligomeric forms of the metastasis-related Mts1 (S100A4) protein stimulate neuronal differentiation in cultures of rat hippocampal neurons. J Biol Chem 2000;275:41278-86.
15. Belot N, Pochet R, Heizmann CW, Kiss R, Decaestecker C. Extracellular S100A4 stimulates the migration rate of astrocytic tumor cells by modifying the organization of their actin cytoskeleton. Biochim Biophys Acta 2002;1600:74-83.
16. Pedersen KB, Andersen K, Fodstad O, Maelandsmo GM. Sensitization of interferon-γ induced apoptosis in human osteosarcoma cells by extracellular S100A4. BMC Cancer 2004;4:52.
17. Schmidt-Hansen B, Ornas D, Grigorian M, et al. Extracellular S100A4 (mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 2004;23:5487-95.
18. Boye K, Grotterod I, Aasheim HC, Hovig E, Maelandsmo GM. Activation of NF-κB by extracellular S100A4: analysis of signal transduction mechanisms and identification of target genes. Int J Cancer 2008;123:1301-10.
19. Klingelhofer J, Moller HD, Sumer EU, et al. Epidermal growth factor receptor ligands as new extracellular targets for the metastasispromoting S100A4 protein. FEBS J 2009;276:5936-48.
20. Grum-Schwensen B, Klingelhofer J, Berg CH, et al. Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 2005;65:3772-80.
21. Grigorian M, Ambartsumian N, Lukanidin E. Metastasis-inducing S100A4 protein: implication in non-malignant human pathologies. Curr Mol Med 2008;8:492-6.
22. Ambartsumian NS, Grigorian MS, Larsen IF, et al. Metastasis of mammary carcinomas in GRS/A hybrid mice transgenic for the mts1 gene. Oncogene 1996;13:1621-30.
23. Celis JE, Gromov P, Cabezon T, et al. Proteomic characterization of the interstitial fluid perfusing the breast tumor microenvironment: a novel resource for biomarker and therapeutic target discovery. Mol Cell Proteomics 2004;3:327-44.
24. Yanagawa Y, Iwabuchi K, Onoe K. Enhancement of stromal cellderived factor-1α-induced chemotaxis for CD4/8 double-positive thymocytes by fibronectin and laminin in mice. Immunology 2001; 104:43-9.
25. Stam JC, Michiels F, van der Kammen RA, Moolenaar WH, Collard JG. Invasion of T-lymphoma cells: cooperation between Rho family GTPases and lysophospholipid receptor signaling. EMBO J 1998;17: 4066-74.
26. Baus E, Van LF, Andris F, Rolin S, Urbain J, Leo O. Dexamethasone increases intracellular cyclic AMP concentration in murine T lymphocyte cell lines. Steroids 2001;66:39-47.
27. Lee WY, Su WC, Lin PW, Guo HR, Chang TW, Chen HH. Expression of S100A4 and Met: potential predictors for metastasis and survival in early-stage breast cancer. Oncology 2004;66:429-38.
28. Xue C, Plieth D, Venkov C, Xu C, Neilson EG. The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res 2003;63:3386-94.
29. Ben-Baruch A. Host microenvironment in breast cancer development: inflammatory cells, cytokines and chemokines in breast cancer progression: reciprocal tumor-microenvironment interactions. Breast Cancer Res 2003;5:31-6.
30. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006;124: 263-6.
31. Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008;27:5904-12.
32. Husemann Y, Geigl JB, Schubert F, et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008;13:58-68.
33. Soria G, Ben-Baruch A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett 2008;267:271-85.
34. Lotfi R, Lee JJ, Lotze MT. Eosinophilic granulocytes and damageassociated molecular pattern molecules (DAMPs): role in the inflammatory response within tumors. J Immunother 2007;30:16-28.
35. Lampinen M, Carlson M, Hakansson LD, Venge P. Cytokineregulated accumulation of eosinophils in inflammatory disease. Allergy 2004;59:793-805.
36. Cheadle EJ, Riyad K, Subar D, et al. Eotaxin-2 and colorectal cancer: a potential target for immune therapy. Clin Cancer Res 2007;13: 5719-28.
37. Hunter MG, Jacob A, O'donnell LC, et al. Loss of SHIP and CIS recruitment to the granulocyte colony-stimulating factor receptor contribute to hyperproliferative responses in severe congenital neutropenia/ acute myelogenous leukemia. J Immunol 2004;173:5036-45.
38. Smith TJ, Khatcheressian J, Lyman GH, et al. 2006 update of recommendations for the use of white blood cell growth factors: an evidence-based clinical practice guideline. J Clin Oncol 2006;24: 3187-205.
39. Mueller MM. Inflammation in epithelial skin tumours: old stories and new ideas. Eur J Cancer 2006;42:735-44.
40. Obermueller E, Vosseler S, Fusenig NE, Mueller MM. Cooperative autocrine and paracrine functions of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor in the progression of skin carcinoma cells. Cancer Res 2004;64: 7801-12.
41. Hirbe AC, Uluckan O, Morgan EA, et al. Granulocyte colony-stimulating factor enhances bone tumor growth in mice in an osteoclastdependent manner. Blood 2007;109:3424-31.
42. Piscaglia AC, Shupe TD, Pani G, Tesori V, Gasbarrini A, Petersen BE. Establishment of cancer cell lines from rat hepatocholangiocarcinoma and assessment of the role of granulocyte-colony stimulating factor and hepatocyte growth factor in their growth, motility and survival. J Hepatol 2009;51:77-92.
43. Shojaei F, Wu X, Qu X, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci U S A 2009;106: 6742-7.
44. + myeloid cells that promote metastasis. Cancer Cell 2008;13:23-35.
45. Alison MR, Lim S, Houghton JM. Bone marrow-derived cells and epithelial tumours: more than just an inflammatory relationship. Curr Opin Oncol 2009;21:77-82.
46. Peinado H, Rafii S, Lyden D. Inflammation joins the "niche". Cancer Cell 2008;14:347-9.