Interleukin-34 promotes tumor progression and metastatic process in osteosarcoma through induction of angiogenesis and macrophage recruitment

International Journal of Cancer

Volumn 137, Issue 1, 2015, Pages 73-85

  Ségaliny, Aude I ^a,b   Mohamadi, Amel ^a,c   Dizier, Blandine ^a,c   Lokajczyk, Anna ^a,c   Brion, Régis ^a,b,d   Lanel, Rachel ^a,b   Amiaud, Jérôme ^a,b   Charrier, Céline ^a,b   Boisson Vidal, Catherine ^a,c   Heymann, Dominique ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

angiogenesis; cell adhesion; endothelial cells; interleukin 34; M CSF; osteosarcoma; tumor associated macrophages

Indexed keywords

CD34 ANTIGEN; COLONY STIMULATING FACTOR 1; HEPARIN LYASE; INTERLEUKIN 1BETA; INTERLEUKIN 34; N ACETYLGALACTOSAMINE 4 SULFATASE; TUMOR NECROSIS FACTOR ALPHA; INTERLEUKIN DERIVATIVE; INTERLEUKIN-34, HUMAN; INTERLEUKIN-34, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL INFILTRATION; CELL PROLIFERATION; CELL STIMULATION; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MACROPHAGE MIGRATION; METASTASIS POTENTIAL; MOUSE; MURINE MODEL; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OSTEOSARCOMA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR CELL INOCULATION; TUMOR GROWTH; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION; ANIMAL; BONE TUMOR; CANCER TRANSPLANTATION; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; LUNG TUMOR; MACROPHAGE; METABOLISM; PATHOLOGY;

ANIMALS; BONE NEOPLASMS; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IN VITRO TECHNIQUES; INTERLEUKIN-1BETA; INTERLEUKINS; LUNG NEOPLASMS; MACROPHAGES; MICE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; OSTEOSARCOMA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84930418087     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29376     Document Type: Article

References (56)

1. Adams RH, Alitalo K.; Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007; 8: 464-78.
2. Marcelo KL, Goldie LC, Hirschi KK.; Regulation of endothelial cell differentiation and specification. Circ Res 2013; 112: 1272-87.
3. Cao Z, Bao M, Miele L, et al. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer 2013; 49: 3914-23.
4. Pixley FJ, Stanley ER.; CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol 2004; 14: 628-38.
5. Chitu V, Stanley ER.; Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol 2006, 18: 39-48.
6. Lin EY, Pollard JW.; Role of infiltrated leucocytes in tumor growth and spread. Br J Cancer 2004; 90: 2053 -5 8.
7. Curry JM, Eubank TD, Roberts RD, et al. M-CSF signals through the MAPK/ERK pathway via Sp1 to induce VEGF production and induces angiogenesis in vivo. PLoS One 2008; 3: e3405.
8. Coussens LM, Werb Z.; Inflammation and cancer. Nature 2002; 420: 860-7.
9. McDermott RS, Deneux L, Mosseri V, et al. Circulating macrophage colony stimulating factor as a marker of tumour progression. Eur Cytokine Netw 2002; 13: 121-7.
10. Scholl SM, Lidereau R, de la Rochefordiere A, et al. Circulating levels of the macrophage colony stimulating factor CSF-1 in primary and metastatic breast cancer patients. A pilot study. Breast Cancer Res Treat 1996; 39: 275-83.
11. Sasaki A, Iwashita Y, Shibata K, et al. Prognostic value of preoperative peripheral blood monocyte count in patients with hepatocellular carcinoma. Surgery 2006; 139: 755-64.
12. Espinosa I, Edris B, Lee CH, et al. CSF1 Expression in Non gynecological leiomyosarcoma is associated with increased tumor angiogenesis. Am J Pathol 2011; 179: 2100-7.
13. Lin H, Lee E, Hestir K, et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 2008; 320: 807-11.
14. Wang Y, Szretter KJ, Vermi W, et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 2012; 13: 753-60.
15. Foucher ED, Blanchard S, Preisser L, et al. IL-34 induces the differentiation of human monocytes into immunosuppressive macrophages. Antagonistic effects of GM-CSF and IFNγ. PLoS One 2013; 8: e56045.
16. Baud'huin M, Renault R, Charrier C, et al. Interleukin-34 is expressed by giant cell tumours of bone and plays a key role in RANKL-induced osteoclastogenesis. J Pathol 2010; 221: 77-86.
17. Eda H, Zhang J, Keith RH, et al. Macrophage-colony stimulating factor and interleukin-34 induce chemokines in human whole blood. Cytokine 2010; 52: 215-220.
18. Chemel M, Le Goff B, Brion R, et al. Interleukin 34 expression is associated with synovitis severity in rheumatoid arthritis patients. Ann Rheum Dis 2012; 71: 150-4.
19. Nakamichi Y, Udagawa N, Takahashi N.; IL-34 and CSF-1: similarities and differences. J Bone Miner Metab 2013; 31: 486-95.
20. Benslimane-Ahmim Z, Heymann D, Dizier B, et al. Osteoprotegerin, a new actor in vasculogenesis, stimulates endothelial colony-forming cells properties. J Thromb Haemost 2011; 9: 834-43.
21. Zemani F, Benisvy D, Galy-Fauroux I, et al. Low-molecular-weight fucoidan enhances the proangiogenic phenotype of endothelial progenitor cells. Biochem Pharmacol 2005; 70: 1167-75.
22. Zemani F, Silvestre JS, Fauvel-Lafeve F, et al. Ex vivo priming of endothelial progenitor cells with SDF-1 before transplantation could increase their proangiogenic potential. Arterioscler Thromb Vasc Biol 2008; 28: 644-50.
23. Dias JV, Benslimane-Ahmim Z, Egot M, et al. A motif within the N-terminal domain of TSP-1 specifically promotes the proangiogenic activity of endothelial colony-forming cells. Biochem Pharmacol 2012; 84: 1014-23.
24. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packging system. J Virol 1998; 72: 8463-71.
25. Gobin B, Battaglia S, Lanel R, et al. NVP-BEZ235, a dual PI3K/mTOR inhibitor, inhibits osteosarcoma cell proliferation and tumor development in vivo with an improved survival rate. Cancer Lett 2014; 344: 291-8.
26. Kobayashi E, Masuda M, Nakayama R, et al. Reduced argininosuccinate synthetase is a predictive biomarker for the development of pulmonary metastasis in patients with osteosarcoma. Mol Cancer Ther 2010; 9: 535-44.
27. Kim YW, West XZ, Byzova TV.; Inflammation and oxidative stress in angiogenesis and vascular disease. J Mol Med 2013; 91: 323-8.
28. Noonan DM, De Lerma Barbaro A, Vannini N, et al. Inflammation, inflammatory cells and angiogenesis: decisions and indecisions. Cancer Metastasis Rev 2008; 27: 31-40.
29. Mantovani A, Biswas SK, Galdiero MR, et al. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013; 229: 176-85.
30. Eltzschig HK, Carmeliet P.; Hypoxia and inflammation. N Engl J Med 2011; 364: 656-65.
31. Heymann D, Redini F.; Bone sarcomas: pathogenesis and new therapeutic approaches. BoneKey Rep 2011; 8: 402-14.
32. Chen Z, Buki K, Vääräniemi J, et al. The critical role of IL-34 in osteoclastogenesis. PLoS One 2011; 6: e18689.
33. Eda H, Shimada H, Beidler DR, Monahan JB.; Proinflammatory cytokines, IL-1β and TNF-α, induce expression of interleukin-34 mRNA via JNK- and p44/42 MAPK-NF-κB pathway but not p38 pathway in osteoblasts. Rheumatol Int 2011; 31: 1525-30.
34. Ilic D, Furuta Y, Kanagawa S, et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995; 377: 539-44.
35. Infusino GA, Jacobson JR.; Endothelial FAK as a therapeutic target in disease. Microvasc Res 2012; 83: 89-96.
36. Zhao X, Guan JL.; Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv Drug Deliv Rev 2011; 63: 610 -1 5.
37. Marx M, Warren SL, Madri JA.; pp60(c-src) modulates microvascular endothelial phenotyp and in vitro angiogenesis. Exp Mol Pathol 2001; 70: 201-13.
38. Pan CC, Kumar S, Shah N, et al. Src-mediated post-trasnlational regulation of endoglin stability and function is critical for angiogenesis. J Biol Chem 2014; 289: 25486-96.
39. Shiojima I, Walsh K.; Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 2002; 90: 1243-50.
40. Somanath PR, Razorenova OV, Chen J, Byzova TV.; Akt1 in endothelial cell and angiogenesis. Cell Cycle 2006; 5: 512-8.
41. Zubilewicz A, Hecquet C, Jeanny JC, et al. Two distinct signalling pathways are involved in FGF2-stimulated proliferation of choriocapillary endothelial cells: a comparative study with VEGF. Oncogene 2001; 20: 1403-13.
42. Slack-Davis JK, Martin KH, Tilghman RW, et al. Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 2007;18; 282: 14845-52.
43. Brandvold KR, Steffey ME, Fox CC, Soellner MB.; Development of a highly selective c-Src kinase inhibitor. ACS Chem Biol 2012; 7: 1393-8.
44. Liu Y1, Jiang N, Wu J, et al. Polo-like kinases inhibited by wortmannin. Labeling site and downstream effects. J Biol Chem 2007; 282: 2505-11.
45. Balogh E, Connolly M, Biniecka M, et al. Interleukin-34 regulates angiogenesis and cell proliferation in inflammatory arthritis, This effect is potentiated by hypoxia. Ann Rheum Dis 2013; 72 (Suppl3): 140.
46. Okazaki T, Ebihara S, Takahashi H, et al. Macrophage colony-stimulating factor induces vascular endothelial growth factor production in skeletal muscle and promotes tumor angiogenesis. J Immunol 2005; 174: 7531-8.
47. Fuster MM, Wang L.; Endothelial heparan sulfate in angiogenesis. Prog Mol Biol Transl Sci 2010; 93: 179-212.
48. Thelin MA, Bartolini B, Axelsson J, et al. Biological functions of iduronic acid in chondroitin/dermatan sulfate. FEBS J 2013; 280: 2431-46.
49. Benslimane-Ahmim Z, Poirier F, Delomenie C, et al. Mechanistic study of the proangiogenic effect of osteoprotegerin. Angiogenesis 2013; 16: 575-593.
50. Nandi S, Cioce M, Yeung YG, et al. Receptor-type protein-tyrosine phosphatase ζ is a functional receptor for interleukin-34. J Biol Chem 2013; 288: 21972-21986.
51. Mikelis C, Sfaelou E, Koutsioumpa M, et al. Integrin alpha(v)beta(3) is a pleiotrophin receptor required for pleiotrophin-induced endothelial cell migration through receptor protein tyrosine phosphatase beta/zeta. FASEB J 2009; 23: 1459-69.
52. Henrotin Y, Lambert C, Richette P.; Importance of synovitis in osteoarthritis: Evidence for the use of glycosaminoglycans against synovial inflammation. Semin Arthritis Rheum 2014; 43: 579-587.
53. Cook J, Hagemann T.; Tumour-associated macrophages and cancer. Curr Opin Pharmacol 2013; 13: 595-601.
54. Buddingh EP, Kuijjer ML, Duim RA, et al. Tumor-infiltrating macrophages are associated with metastasis suppression in high-grade osteosarcoma: a rationale for treatment with macrophage activating agents. Clin Cancer Res 2011; 17: 2110-2119.
55. Nowicki A, Szenajch J, Ostrowska G, et al. Impaired tumor growth in colony-stimulating factor 1 (CSF-1)-deficient, macrophage-deficient op/op mouse: evidence for a role of CSF-1-dependent macrophages in formation of tumor stroma. Int J Cancer 1998; 65: 112-119.
56. DeNardo DG, Brennan DJ, Rexhepaj E, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011; 1: 54-67.