Specific inhibition of the VEGFR-3 tyrosine kinase by SAR131675 reduces peripheral and tumor associated immunosuppressive myeloid cells

Cancers

Volumn 6, Issue 1, 2014, Pages 472-490

  Espagnolle, Nicolas ^a   Barron, Pauline ^b   Mandron, Marie ^b   Blanc, Isabelle ^b   Bonnin, Jacques ^b   Agnel, Magali ^b   Kerbelec, Erwan ^b   Herault, Jean Pascal ^b   Savi, Pierre ^b   Bono, Françoise ^b   Alam, Antoine ^b  

^a CNRS   (France)

^b SANOFI   (France)

Author keywords

Angiogenesis; Lymphangiogenesis; Macrophages; MDSCS; VEGFR 3

Indexed keywords

BIOLOGICAL MARKER; CD11B ANTIGEN; CD206 ANTIGEN; CD86 ANTIGEN; GR1 PROTEIN; LEGUMAIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MGL2 PROTEIN; PROTEIN TYROSINE KINASE INHIBITOR; SAR 131675; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SELECTION; CONTROLLED STUDY; LYMPHOID ORGAN; MACROPHAGE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; SOLID TUMOR; SPLEEN WEIGHT; SPLENOMEGALY; SUPPRESSOR CELL; TRANSCRIPTOMICS; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VOLUME;

EID: 84903368492     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers6010472     Document Type: Article

References (46)

1. Almand, B.; Clark, J.I.; Nikitina, E.; van Beynen, J.; English, N.R.; Knight, S.C.; Carbone, D.P.; Gabrilovich, D.I. Increased production of immature myeloid cells in cancer patients: A mechanism of immunosuppression in cancer. J. Immunol. 2001, 166, 678-689.
2. Pak, A.S.; Wright, M.A.; Matthews, J.P.; Collins, S.L.; Petruzzelli, G.J.; Young, M.R. Mechanisms of immune suppression in patients with head and neck cancer: Presence of CD34(+) cells which suppress immune functions within cancers that secrete granulocyte-macrophage colony-stimulating factor. Clin. Cancer Res. 1995, 1, 95-103.
3. Zea, A.H.; Rodriguez, P.C.; Atkins, M.B.; Hernandez, C.; Signoretti, S.; Zabaleta, J.; McDermott, D.; Quiceno, D.; Youmans, A.; O'Neill, A.; et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: A mechanism of tumor evasion. Cancer Res. 2005, 65, 3044-3048.
4. Baniyash, M. Chronic inflammation, immunosuppression and cancer: New insights and outlook. Semin. Cancer Biol. 2006, 16, 80-88.
5. Ostrand-Rosenberg, S.; Sinha, P. Myeloid-derived suppressor cells: Linking inflammation and cancer. J. Immunol. 2009, 182, 4499-4506.
6. Gabrilovich, D.I.; Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9, 162-174.
7. Movahedi, K.; Guilliams, M.; van den Bossche, J.; van den Bergh, R.; Gysemans, C.; Beschin, A.; de Baetselier, P.; van Ginderachter, J.A. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008, 111, 4233-4244.
8. Youn, J.I.; Nagaraj, S.; Collazo, M.; Gabrilovich, D.I. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 2008, 181, 5791-5802.
9. Kusmartsev, S.; Su, Z.; Heiser, A.; Dannull, J.; Eruslanov, E.; Kubler, H.; Yancey, D.; Dahm, P.; Vieweg, J. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin. Cancer Res. 2008, 14, 8270-8278.
10. Diaz-Montero, C.M.; Salem, M.L.; Nishimura, M.I.; Garrett-Mayer, E.; Cole, D.J.; Montero, A.J. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother. 2009, 58, 49-59.
11. Liu, C.Y.; Wang, Y.M.; Wang, C.L.; Feng, P.H.; Ko, H.W.; Liu, Y.H.; Wu, Y.C.; Chu, Y.; Chung, F.T.; Kuo, C.H.; et al. Population alterations of L-arginase- and inducible nitric oxide synthase-expressed CD11b+/CD14(-)/CD15+/CD33+ myeloid-derived suppressor cells and CD8+ T lymphocytes in patients with advanced-stage non-small cell lung cancer. J. Cancer Res. Clin. Oncol. 2010, 136, 35-45.
12. Wang, L.; Chang, E.W.; Wong, S.C.; Ong, S.M.; Chong, D.Q.; Ling, K.L. Increased myeloid-derived suppressor cells in gastric cancer correlate with cancer stage and plasma S100A8/A9 proinflammatory proteins. J. Immunol. 2013, 190, 794-804.
13. Martinez, F.O.; Helming, L.; Gordon, S. Alternative activation of macrophages: An immunologic functional perspective. Annu. Rev. Immunol. 2009, 27, 451-483.
14. Sica, A.; Schioppa, T.; Mantovani, A.; Allavena, P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: Potential targets of anti-cancer therapy. Eur. J. Cancer 2006, 42, 717-727.
15. Murdoch, C.; Muthana, M.; Coffelt, S.B.; Lewis, C.E. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 2008, 8, 618-631.
16. Lin, C.Y.; Lin, C.J.; Chen, K.H.; Wu, J.C.; Huang, S.H.; Wang, S.M. Macrophage activation increases the invasive properties of hepatoma cells by destabilization of the adherens junction. FEBS Lett. 2006, 580, 3042-3050.
17. Pollard, J.W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 2004, 4, 71-78.
18. Ryder, M.; Ghossein, R.A.; Ricarte-Filho, J.C.; Knauf, J.A.; Fagin, J.A. Increased density of tumor-associated macrophages is associated with decreased survival in advanced thyroid cancer. Endocr. Relat. Cancer 2008, 15, 1069-1074.
19. Shabo, I.; Stal, O.; Olsson, H.; Dore, S.; Svanvik, J. Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int. J. Cancer 2008, 123, 780-786.
20. Fridlender, Z.G.; Sun, J.; Mishalian, I.; Singhal, S.; Cheng, G.; Kapoor, V.; Horng, W.; Fridlender, G.; Bayuh, R.; Worthen, G.S.; et al. Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS One 2012, 7, e31524.
21. Gabrilovich, D.I.; Ostrand-Rosenberg, S.; Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012, 12, 253-268.
22. Kusmartsev, S.; Gabrilovich, D.I. STAT1 signaling regulates tumor-associated macrophage-mediated T cell deletion. J. Immunol. 2005, 174, 4880-4891.
23. Alam, A.; Blanc, I.; Gueguen-Dorbes, G.; Duclos, O.; Bonnin, J.; Barron, P.; Laplace, M.C.; Morin, G.; Gaujarengues, F.; Dol, F.; et al. SAR131675, a potent and selective VEGFR-3-TK inhibitor with antilymphangiogenic, antitumoral, and antimetastatic activities. Mol. Cancer Ther. 2012, 11, 1637-1649.
24. DuPre, S.A.; Hunter, K.W., Jr. Murine mammary carcinoma 4T1 induces a leukemoid reaction with splenomegaly: Association with tumor-derived growth factors. Exp. Mol. Pathol. 2007, 82, 12-24.
25. Pulaski, B.A.; Ostrand-Rosenberg, S. Mouse 4T1 breast tumor model. Curr. Protoc. Immunol. 2001, doi:10.1002/0471142735.im2002s39.
26. Koebel, C.M.; Vermi, W.; Swann, J.B.; Zerafa, N.; Rodig, S.J.; Old, L.J.; Smyth, M.J.; Schreiber, R.D. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007, 450, 903-907.
27. Sinha, P.; Clements, V.K.; Ostrand-Rosenberg, S. Interleukin-13-regulated M2 macrophages in combination with myeloid suppressor cells block immune surveillance against metastasis. Cancer Res. 2005, 65, 11743-11751.
28. Shojaei, F.; Wu, X.; Malik, A.K.; Zhong, C.; Baldwin, M.E.; Schanz, S.; Fuh, G.; Gerber, H.P.; Ferrara, N. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat. Biotechnol. 2007, 25, 911-920.
29. Movahedi, K.; Laoui, D.; Gysemans, C.; Baeten, M.; Stange, G.; van den Bossche, J.; Mack, M.; Pipeleers, D.; In'Tveld, P.; de Baetselier, P.; et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 2010, 70, 5728-5739.
30. Loercher, A.E.; Nash, M.A.; Kavanagh, J.J.; Platsoucas, C.D.; Freedman, R.S. Identification of an IL-10-producing HLA-DR-negative monocyte subset in the malignant ascites of patients with ovarian carcinoma that inhibits cytokine protein expression and proliferation of autologous T cells. J. Immunol. 1999, 163, 6251-6260.
31. Schartner, J.M.; Hagar, A.R.; van Handel, M.; Zhang, L.; Nadkarni, N.; Badie, B. Impaired capacity for upregulation of MHC class II in tumor-associated microglia. Glia 2005, 51, 279-285.
32. Fridlender, Z.G.; Albelda, S.M. Tumor-associated neutrophils: Friend or foe? Carcinogenesis 2012, 33, 949-955.
33. Gu, Y.; Zhao, W.; Meng, F.; Qu, B.; Zhu, X.; Sun, Y.; Shu, Y.; Xu, Q. Sunitinib impairs the proliferation and function of human peripheral T cell and prevents T-cell-mediated immune response in mice. Clin. Immunol. 2010, 135, 55-62.
34. Zhao, W.; Gu, Y.H.; Song, R.; Qu, B.Q.; Xu, Q. Sorafenib inhibits activation of human peripheral blood T cells by targeting LCK phosphorylation. Leukemia 2008, 22, 1226-1233.
35. Van Dongen, M.; Savage, N.D.; Jordanova, E.S.; Briaire-de Bruijn, I.H.; Walburg, K.V.; Ottenhoff, T.H.; Hogendoorn, P.C.; van der Burg, S.H.; Gelderblom, H.; van Hall, T. Anti-inflammatory M2 type macrophages characterize metastasized and tyrosine kinase inhibitor-treated gastrointestinal stromal tumors. Int. J. Cancer 2010, 127, 899-909.
36. Zhang, W.; Zhu, X.D.; Sun, H.C.; Xiong, Y.Q.; Zhuang, P.Y.; Xu, H.X.; Kong, L.Q.; Wang, L.; Wu, W.Z.; Tang, Z.Y. Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects. Clin. Cancer Res. 2010, 16, 3420-3430.
37. Baluk, P.; Tammela, T.; Ator, E.; Lyubynska, N.; Achen, M.G.; Hicklin, D.J.; Jeltsch, M.; Petrova, T.V.; Pytowski, B.; Stacker, S.A.; et al. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Investig. 2005, 115, 247-257.
38. Cursiefen, C.; Chen, L.; Borges, L.P.; Jackson, D.; Cao, J.; Radziejewski, C.; D'Amore, P.A.; Dana, M.R.; Wiegand, S.J.; Streilein, J.W. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J. Clin. Investig. 2004, 113, 1040-1050.
39. Hamrah, P.; Chen, L.; Zhang, Q.; Dana, M.R. Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells. Am. J. Pathol. 2003, 163, 57-68.
40. Maruyama, K.; Ii, M.; Cursiefen, C.; Jackson, D.G.; Keino, H.; Tomita, M.; van Rooijen, N.; Takenaka, H.; D'Amore, P.A.; Stein-Streilein, J.; et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J. Clin. Investig. 2005, 115, 2363-2372.
41. Shin, Y.J.; Choi, J.S.; Choi, J.Y.; Hou, Y.; Cha, J.H.; Chun, M.H.; Lee, M.Y. Induction of vascular endothelial growth factor receptor-3 mRNA in glial cells following focal cerebral ischemia in rats. J. Neuroimmunol. 2010, 229, 81-90.
42. Schoppmann, S.F.; Birner, P.; Stockl, J.; Kalt, R.; Ullrich, R.; Caucig, C.; Kriehuber, E.; Nagy, K.; Alitalo, K.; Kerjaschki, D. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am. J. Pathol. 2002, 161, 947-956.
43. Yang, H.; Kim, C.; Kim, M.J.; Schwendener, R.A.; Alitalo, K.; Heston, W.; Kim, I.; Kim, W.J.; Koh, G.Y. Soluble vascular endothelial growth factor receptor-3 suppresses lymphangiogenesis and lymphatic metastasis in bladder cancer. Mol. Cancer 2011, 10, 36.
44. Alitalo, A.K.; Proulx, S.T.; Karaman, S.; Aebischer, D.; Martino, S.; Jost, M.; Schneider, N.; Bry, M.; Detmar, M. VEGF-C and VEGF-D blockade inhibits inflammatory skin carcinogenesis. Cancer Res. 2013, 73, 4212-4221.
45. Bogos, K.; Renyi-Vamos, F.; Dobos, J.; Kenessey, I.; Tovari, J.; Timar, J.; Strausz, J.; Ostoros, G.; Klepetko, W.; Ankersmit, H.J.; et al. High VEGFR-3-positive circulating lymphatic/vascular endothelial progenitor cell level is associated with poor prognosis in human small cell lung cancer. Clin. Cancer Res. 2009, 15, 1741-1746.
46. Favier, B.; Alam, A.; Barron, P.; Bonnin, J.; Laboudie, P.; Fons, P.; Mandron, M.; Herault, J.P.; Neufeld, G.; Savi, P.; et al. Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood 2006, 108, 1243-1250.