Metastasis-associated protein S100A4 induces a network of inflammatory cytokines that activate stromal cells to acquire pro-tumorigenic properties

Cancer Letters

Volumn 344, Issue 1, 2014, Pages 28-39

  Bettum, Ingrid J ^a   Vasiliauskaite, Kotryna ^a   Nygaard, Vigdis ^a   Clancy, Trevor ^a   Pettersen, Solveig J ^a   Tenstad, Ellen ^a,b   Mælandsmo, Gunhild M ^a,c   Prasmickaite, Lina ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Cytokines; Melanoma; Metastasis; S100A4; Tumor stroma interactions

Indexed keywords

CALVASCULIN; CYTOKINE; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; SERUM AMYLOID A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL ACTIVATION; CELL INTERACTION; CELL STIMULATION; CYTOKINE RELEASE; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; INFLAMMATORY CELL; MELANOMA; METASTASIS; MONOCYTE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; STROMA CELL; TUMOR MICROENVIRONMENT; TUMOR PROMOTION;

CYTOKINES; MELANOMA; METASTASIS; S100A4; TUMOR-STROMA INTERACTIONS;

ANIMALS; CELL LINE, TUMOR; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MELANOMA; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR CROSS-TALK; S100 PROTEINS; STROMAL CELLS; TUMOR MICROENVIRONMENT;

EID: 84893671988     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.10.036     Document Type: Article

References (54)

1. Sleeman J., Steeg P.S. Cancer metastasis as a therapeutic target. Eur. J. Cancer 2010, 46:1177-1180.
2. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 2009, 9:239-252.
3. O'Connell J.T., Sugimoto H., Cooke V.G., Macdonald B.A., Mehta A.I., Lebleu V.S., Dewar R., Rocha R.M., Brentani R.R., Resnick M.B., Neilson E.G., Zeisberg M., Kalluri R. VEGF-A and Tenascin-C produced by S100A4+ stromal cells are important for metastatic colonization. Proc. Natl. Acad. Sci. USA 2011, 108:16002-16007.
4. Peinado H., Aleckovic M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno G., Hergueta-Redondo M., Williams C., Garcia-Santos G., Ghajar C., Nitadori-Hoshino A., Hoffman C., Badal K., Garcia B.A., Callahan M.K., Yuan J., Martins V.R., Skog J., Kaplan R.N., Brady M.S., Wolchok J.D., Chapman P.B., Kang Y., Bromberg J., Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 2012, 18:883-891.
5. Acharyya S., Oskarsson T., Vanharanta S., Malladi S., Kim J., Morris P.G., Manova-Todorova K., Leversha M., Hogg N., Seshan V.E., Norton L., Brogi E., Massague J. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150:165-178.
6. Seike T., Fujita K., Yamakawa Y., Kido M.A., Takiguchi S., Teramoto N., Iguchi H., Noda M. Interaction between lung cancer cells and astrocytes via specific inflammatory cytokines in the microenvironment of brain metastasis. Clin. Exp. Metastasis 2011, 28:13-25.
7. Hiratsuka S., Watanabe A., Sakurai Y., Akashi-Takamura S., Ishibashi S., Miyake K., Shibuya M., Akira S., Aburatani H., Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat. Cell Biol. 2008, 10:1349-1355.
8. Salama I., Malone P.S., Mihaimeed F., Jones J.L. A review of the S100 proteins in cancer. Eur. J. Surg. Oncol. 2008, 34:357-364.
9. Marenholz I., Heizmann C.W., Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 2004, 322:1111-1122.
10. Lukanidin E., Sleeman J.P. Building the niche: the role of the S100 proteins in metastatic growth. Semin. Cancer Biol. 2012, 22:216-225.
11. Andersen K., Nesland J.M., Holm R., Florenes V.A., Fodstad O., Maelandsmo G.M. Expression of S100A4 combined with reduced E-cadherin expression predicts patient outcome in malignant melanoma. Mod. Pathol. 2004, 17:990-997.
12. Rudland P.S., Platt-Higgins A., Renshaw C., West C.R., Winstanley J.H., Robertson L., Barraclough R. Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res. 2000, 60:1595-1603.
13. Boye K., Maelandsmo G.M. S100A4 and metastasis: a small actor playing many roles. Am. J. Pathol. 2009, 176:528-535.
14. Grigorian M., Ambartsumian N., Lukanidin E. Metastasis-inducing S100A4 protein: implication in non-malignant human pathologies. Curr. Mol. Med. 2008, 8:492-496.
15. Andres Cerezo L., Kuncova K., Mann H., Tomcik M., Zamecnik J., Lukanidin E., Neidhart M., Gay S., Grigorian M., Vencovsky J., Senolt L. The metastasis promoting protein S100A4 is increased in idiopathic inflammatory myopathies. Rheumatol. (Oxford) 2011, 50:1766-1772.
16. Cabezon T., Celis J.E., Skibshoj I., Klingelhofer J., Grigorian M., Gromov P., Rank F., Myklebust J.H., Maelandsmo G.M., Lukanidin E., Ambartsumian N. Expression of S100A4 by a variety of cell types present in the tumor microenvironment of human breast cancer. Int. J. Cancer 2007, 121:1433-1444.
17. Grum-Schwensen B., Klingelhofer J., Berg C.H., El-Naaman C., Grigorian M., Lukanidin E., Ambartsumian N. Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res. 2005, 65:3772-3780.
18. Schmidt-Hansen B., Ornas D., Grigorian M., Klingelhofer J., Tulchinsky E., Lukanidin E., Ambartsumian N. Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 2004, 23:5487-5495.
19. Ambartsumian N., Klingelhofer J., Grigorian M., Christensen C., Kriajevska M., Tulchinsky E., Georgiev G., Berezin V., Bock E., Rygaard J., Cao R., Cao Y., Lukanidin E. The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 2001, 20:4685-4695.
20. Grum-Schwensen B., Klingelhofer J., Grigorian M., Almholt K., Nielsen B.S., Lukanidin E., Ambartsumian N. Lung metastasis fails in MMTV-PyMT oncomice lacking S100A4 due to a T-cell deficiency in primary tumors. Cancer Res. 2010, 70:936-947.
21. Klingelhofer J., Grum-Schwensen B., Beck M.K., Knudsen R.S., Grigorian M., Lukanidin E., Ambartsumian N. Anti-S100A4 antibody suppresses metastasis formation by blocking stroma cell invasion. Neoplasia 2012, 14:1260-1268.
22. Fang Z., Forslund N., Takenaga K., Lukanidin E., Kozlova E.N. Sensory neurite outgrowth on white matter astrocytes is influenced by intracellular and extracellular S100A4 protein. J. Neurosci. Res. 2006, 83:619-626.
23. Fodstad O., Kjonniksen I., Aamdal S., Nesland J.M., Boyd M.R., Pihl A. Extrapulmonary, tissue-specific metastasis formation in nude mice injected with FEMX-I human melanoma cells. Cancer Res. 1988, 48:4382-4388.
24. Prasmickaite L., Skrbo N., Hoifodt H.K., Suo Z., Engebraten O., Gullestad H.P., Aamdal S., Fodstad O., Maelandsmo G.M. Human malignant melanoma harbours a large fraction of highly clonogenic cells that do not express markers associated with cancer stem cells. Pigment Cell Melanoma Res. 2010, 23:449-451.
25. Day C.P., Carter J., Bonomi C., Esposito D., Crise B., Ortiz-Conde B., Hollingshead M., Merlino G. Lentivirus-mediated bifunctional cell labeling for in vivo melanoma study. Pigment Cell Melanoma Res. 2009, 22:283-295.
26. Berge G., Pettersen S., Grotterod I., Bettum I.J., Boye K., Maelandsmo G.M. Osteopontin - an important downstream effector of S100A4-mediated invasion and metastasis. Int. J. Cancer 2011, 129:780-790.
27. Boye K., Grotterod I., Aasheim H.C., Hovig E., Maelandsmo G.M. Activation of NF-kappaB by extracellular S100A4: analysis of signal transduction mechanisms and identification of target genes. Int. J. Cancer 2008, 123:1301-1310.
28. Razick S., Magklaras G., Donaldson I.M. iRefIndex: a consolidated protein interaction database with provenance. BMC Bioinformatics 2008, 405.
29. Smoot M.E., Ono K., Ruscheinski J., Wang P.-L., Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 431-432.
30. Evensen L., Micklem D.R., Blois A., Berge S.V., Aarsæther N., Littlewood-Evans A., Wood J., Lorens J.B. Mural cell associated VEGF is required for organotypic vessel formation. PLoS ONE 2009, 4:e5798.
31. Vinci M., Box C., Zimmermann M., Eccles S.A. Tumor spheroid-based migration assays for evaluation of therapeutic agents. Methods Mol. Biol. 2013, 986:253-266.
32. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr. Mol. Med. 2007, 7:711-724.
33. Fiedler U., Augustin H.G. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 2006, 27:552-558.
34. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
35. Mas-Moruno C., Rechenmacher F., Kessler H. Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer Agents Med. Chem. 2010, 10:753-768.
36. Singh S., Singh A.P., Sharma B., Owen L.B., Singh R.K. CXCL8 and its cognate receptors in melanoma progression and metastasis. Future Oncol. 2010, 6:111-116.
37. Zhang J., Patel L., Pienta K.J. Targeting chemokine (C-C motif) ligand 2 (CCL2) as an example of translation of cancer molecular biology to the clinic. Prog. Mol. Biol. Transl. Sci. 2010, 95:31-53.
38. Rasanen K., Sriswasdi S., Valiga A., Tang H.Y., Zhang G., Perego M., Somasundaram R., Li L., Speicher K., Klein-Szanto A., Basu D., Rustgi A.K., Speicher D.W., Herlyn M. Comparative secretome analysis of epithelial and mesenchymal subpopulations of head and neck squamous cell carcinoma identifies S100A4 as a potential therapeutic target. Mol. Cell Proteomics 2013.
39. Hernandez J.L., Padilla L., Dakhel S., Coll T., Hervas R., Adan J., Masa M., Mitjans F., Martinez J.M., Coma S., Rodriguez L., Noe V., Ciudad C.J., Blasco F., Messeguer R. Therapeutic targeting of tumor growth and angiogenesis with a novel anti-S100A4 monoclonal antibody. PLoS One 2013, 8:e72480.
40. Dmytriyeva O., Pankratova S., Owczarek S., Sonn K., Soroka V., Ridley C.M., Marsolais A., Lopez-Hoyos M., Ambartsumian N., Lukanidin E., Bock E., Berezin V., Kiryushko D. The metastasis-promoting S100A4 protein confers neuroprotection in brain injury. Nat. Commun. 2012, 3:1197.
41. Cedervall J., Jamil S., Prasmickaite L., Cheng Y., Eskandarpour M., Hansson J., Maelandsmo G.M., Ringborg U., Gulyas M., Suo Z., Kanter L., Ahrlund-Richter L. Species-specific in vivo engraftment of the human BL melanoma cell line results in an invasive dedifferentiated phenotype not present in xenografts. Cancer Res. 2009, 69:3746-3754.
42. Forst B., Hansen M.T., Klingelhofer J., Moller H.D., Nielsen G.H., Grum-Schwensen B., Ambartsumian N., Lukanidin E., Grigorian M. Metastasis-inducing S100A4 and RANTES cooperate in promoting tumor progression in mice. PLoS ONE 2010, 5:e10374.
43. Huang Y., Song N., Ding Y., Yuan S., Li X., Cai H., Shi H., Luo Y. Pulmonary vascular destabilization in the premetastatic phase facilitates lung metastasis. Cancer Res. 2009, 69:7529-7537.
44. Wolf M.J., Hoos A., Bauer J., Boettcher S., Knust M., Weber A., Simonavicius N., Schneider C., Lang M., Sturzl M., Croner R.S., Konrad A., Manz M.G., Moch H., Aguzzi A., van Loo G., Pasparakis M., Prinz M., Borsig L., Heikenwalder M. Endothelial CCR2 signaling induced by colon carcinoma cells enables extravasation via the JAK2-Stat5 and p38MAPK pathway. Cancer Cell 2012, 22:91-105.
45. Peinado H., Lavotshkin S., Lyden D. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin. Cancer Biol. 2011, 21:139-146.
46. Carbonell W.S., Ansorge O., Sibson N., Muschel R. The vascular basement membrane as "soil" in brain metastasis. PLoS One 2009, 4:e5857.
47. Ghajar C.M., Peinado H., Mori H., Matei I.R., Evason K.J., Brazier H., Almeida D., Koller A., Hajjar K.A., Stainier D.Y., Chen E.I., Lyden D., Bissell M.J. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 2013, 15:807-817.
48. Waugh D.J., Wilson C. The interleukin-8 pathway in cancer. Clin. Cancer Res. 2008, 14:6735-6741.
49. Bar-Eli M. Role of interleukin-8 in tumor growth and metastasis of human melanoma. Pathobiology 1999, 67:12-18.
50. Huh S.J., Liang S., Sharma A., Dong C., Robertson G.P. Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res. 2010, 70:6071-6082.
51. DeNardo D.G.B., Rexhepaj D.J., Ruffell E., Shiao B., Madden S., Gallagher S.F., Wadhwani W.M., Keil N., Junaid S.D., Rugo S.A., Hwang H.S., Jirstrom E.S., West K., Coussens B.L. Leukocyte complexicity predicts breast cancer survival and fucntionallity regulates responses to chemotherapy. Cancer, Discovery 2011, 1:OF53-OF65.
52. Qian B.Z., Li J., Zhang H., Kitamura T., Zhang J., Campion L.R., Kaiser E.A., Snyder L.A., Pollard J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011, 475:222-225.
53. Lu X., Kang Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J. Biol. Chem. 2009, 284:29087-29096.
54. Wang T., Ge Y., Xiao M., Lopez-Coral A., Azuma R., Somasundaram R., Zhang G., Wei Z., Xu X., Rauscher F.J., Herlyn M., Kaufman R.E. Melanoma-derived conditioned media efficiently induce the differentiation of monocytes to macrophages that display a highly invasive gene signature. Pigment Cell Melanoma Res. 2012, 25:493-505.