VEGF as a modulator of the innate immune response in glioblastoma

GLIA

Volumn 66, Issue 1, 2018, Pages 161-174

  Turkowski, Kati ^a,b   Brandenburg, Susan ^a   Mueller, Annett ^a   Kremenetskaia, Irina ^a   Bungert, Alexander D ^a   Blank, Anne ^a   Felsenstein, Matthäus ^a   Vajkoczy, Peter ^a  

^a BERLIN INSTITUTE OF HEALTH   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

GBM; microglia macrophages; SDF1 ; tumor angiogenesis; VEGFR2

Indexed keywords

STROMAL CELL DERIVED FACTOR 1ALPHA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; CD68 ANTIGEN, HUMAN; CHEMOKINE RECEPTOR CXCR4; CXCL12 PROTEIN, MOUSE; CXCR4 PROTEIN, MOUSE; DIFFERENTIATION ANTIGEN; KDR PROTEIN, MOUSE; KI 67 ANTIGEN; LEUKOCYTE ANTIGEN; MAPK8IP PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEEDBACK SYSTEM; GLIOBLASTOMA; INNATE IMMUNITY; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BRAIN TUMOR; C57BL MOUSE; CELL MOTION; CELL SURVIVAL; DIAGNOSTIC IMAGING; DRUG EFFECT; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; APOPTOSIS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; CHEMOKINE CXCL12; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; IMMUNITY, INNATE; KI-67 ANTIGEN; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROGLIA; RECEPTORS, CXCR4; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85034020937     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.23234     Document Type: Article

References (47)

1. Aghi, M., Cohen, K. S., Klein, R. J., Scadden, D. T., & Chiocca, E. A. (2006). Tumor stromal-derived factor-1 recruits vascular progenitors to mitotic neovasculature, where microenvironment influences their differentiated phenotypes. Cancer Research, 66, 9054–9064.
2. Ausman, J. I., Shapiro, W. R., & Rall, D. P. (1970). Studies on the chemotherapy of experimental brain tumors: Development of an experimental model. Cancer Research, 30, 2394–2400.
3. Badie, B., & Schartner, J. (2001). Role of microglia in glioma biology. Microscopy Research and Technique, 54, 106–113.
4. Barbero, S., Bonavia, R., Bajetto, A., Porcile, C., Pirani, P., Ravetti, J. L., … Schettini, G. (2003). Stromal cell-derived factor 1alpha stimulates human glioblastoma cell growth through the activation of both extracellular signal-regulated kinases 1/2 and Akt. Cancer Research, 63, 1969–1974.
5. Bergers, G., & Hanahan, D. (2008). Modes of resistance to anti-angiogenic therapy. Nature Reviews: Cancer, 8, 592–603.
6. Brandenburg, S., Muller, A., Turkowski, K., Radev, Y. T., Rot, S., Schmidt, C., … Vajkoczy, P. (2016). Resident microglia rather than peripheral macrophages promote vascularization in brain tumors and are source of alternative pro-angiogenic factors. Acta Neuropathologica, 131, 365–378.
7. Byrne, A. M., Bouchier-Hayes, D. J., & Harmey, J. H. (2005). Angiogenic and cell survival functions of Vascular Endothelial Growth Factor (VEGF). Journal of Cellular and Molecular Medicine, 9, 777–794.
8. Chaudhry, I. H., O'Donovan, D. G., Brenchley, P. E., Reid, H., & Roberts, I. S. (2001). Vascular endothelial growth factor expression correlates with tumour grade and vascularity in gliomas. Histopathology, 39, 409–415.
9. Chen, W., He, D., Li, Z., Zhang, X., Pan, D., & Chen, G. (2015). Overexpression of vascular endothelial growth factor indicates poor outcomes of glioma: A systematic review and meta-analysis. International Journal of Clinical and Experimental Medicine, 8, 8709–8719.
10. Chen, X., Zhang, L., Zhang, I. Y., Liang, J., Wang, H., Ouyang, M., … Badie, B. (2014). RAGE Expression in Tumor-Associated Macrophages Promotes Angiogenesis in Glioma. Cancer Research, 74, 7285–7297.
11. Ehtesham, M., Winston, J. A., Kabos, P., & Thompson, R. C. (2006). CXCR4 expression mediates glioma cell invasiveness. Oncogene, 25, 2801–2806.
12. Ferrara, N. (2002). VEGF and the quest for tumour angiogenesis factors. Nature reviews. Cancer, 2, 795–803.
13. Forstreuter, F., Lucius, R., & Mentlein, R. (2002). Vascular endothelial growth factor induces chemotaxis and proliferation of microglial cells. Journal of Neuroimmunology, 132, 93–98.
14. Kerber, M., Reiss, Y., Wickersheim, A., Jugold, M., Kiessling, F., Heil, M., … Machein, M. R. (2008). Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Research, 68, 7342–7351.
15. Kim, H. K., De La Luz Sierra, M., Williams, C. K., Gulino, A. V., & Tosato, G. (2006). G-CSF down-regulation of CXCR4 expression identified as a mechanism for mobilization of myeloid cells. Blood, 108, 812–820.
16. Kioi, M., Vogel, H., Schultz, G., Hoffman, R. M., Harsh, G. R., & Brown, J. M. (2010). Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. Journal of Clinical Investigation, 120, 694–705.
17. Kushchayev, S. V., Kushchayeva, Y. S., Wiener, P. C., Scheck, A. C., Badie, B., & Preul, M. C. (2014). Monocyte-derived cells of the brain and malignant gliomas: The double face of Janus. World Neurosurgery, 82, 1171–1186.
18. Lu-Emerson, C., Snuderl, M., Kirkpatrick, N. D., Goveia, J., Davidson, C., Huang, Y., … Jain, R. K. (2013). Increase in tumor-associated macrophages after antiangiogenic therapy is associated with poor survival among patients with recurrent glioblastoma. Neuro-Oncology, 15, 1079–1087.
19. Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., … Rafii, S. (2001). Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nature Medicine, 7, 1194–1201.
20. Maderna, E., Salmaggi, A., Calatozzolo, C., Limido, L., & Pollo, B. (2007). Nestin, PDGFRbeta, CXCL12 and VEGF in glioma patients: Different profiles of (pro-angiogenic) molecule expression are related with tumor grade and may provide prognostic information. Cancer Biology & Therapy, 6, 1018–1024.
21. Markovic, D. S., Glass, R., Synowitz, M., Rooijen, N. V., & Kettenmann, H. (2005). Microglia stimulate the invasiveness of glioma cells by increasing the activity of metalloprotease-2. Journal of Neuropathology and Experimental Neurology, 64, 754–762.
22. Markovic, D. S., Vinnakota, K., Chirasani, S., Synowitz, M., Raguet, H., Stock, K., … Kettenmann, H. (2009). Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion. Proceedings of the National Academy of Sciences of the United States of America, 106, 12530–12535.
23. Masood, R., Cai, J., Zheng, T., Smith, D. L., Hinton, D. R., & Gill, P. S. (2001). Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood, 98, 1904–1913.
24. Mellinghoff, I. K., Lassman, A. B., & Wen, P. Y. (2011). Signal transduction inhibitors and antiangiogenic therapies for malignant glioma. Glia, 59, 1205–1212.
25. Müller, A., Brandenburg, S., Turkowski, K., Müller, S., & Vajkoczy, P. (2015). Resident microglia, and not peripheral macrophages, are the main source of brain tumor mononuclear cells. International Journal of Cancer, 137, 278–288.
26. Murdoch, C., Muthana, M., Coffelt, S. B., & Lewis, C. E. (2008). The role of myeloid cells in the promotion of tumour angiogenesis. Nature reviews Cancer 8, 618–631.
27. Nishie, A., Ono, M., Shono, T., Fukushi, J., Otsubo, M., Onoue, H., … Kuwano, M. (1999). Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clinical Cancer Research, 5, 1107–1113.
28. Osterberg, N., Ferrara, N., Vacher, J., Gaedicke, S., Niedermann, G., Weyerbrock, A., … Machein, M. R. (2016). Decrease of VEGF-A in myeloid cells attenuates glioma progression and prolongs survival in an experimental glioma model. Neuro-Oncology, 18, 939–949.
29. Ozawa, C. R., Banfi, A., Glazer, N. L., Thurston, G., Springer, M. L., Kraft, P. E., … Blau, H. M. (2004). Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis. Journal of Clinical Investigation, 113, 516–527.
30. Piao, Y., Liang, J., Holmes, L., Zurita, A. J., Henry, V., Heymach, J. V., & de Groot, J. F. (2012). Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro-Oncology, 14, 1379–1392.
31. Rempel, S. A., Dudas, S., Ge, S., & Gutierrez, J. A. (2000). Identification and localization of the cytokine SDF1 and its receptor, CXC chemokine receptor 4, to regions of necrosis and angiogenesis in human glioblastoma. Clinical Cancer Research, 6, 102–111.
32. Ribatti, D. (2016). Tumor refractoriness to anti-VEGF therapy. Oncotarget, 7, 46668–46677.
33. Schmid, M. C., & Varner, J. A. (2012). Myeloid cells in tumor inflammation. Vascular Cell, 4, 14.
34. Sedgwick, J. D., Schwender, S., Imrich, H., Dörries, R., Butcher, G. W., ter Meulen, V. (1991). Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proceedings of the National Academy of Sciences of the United States of America, 88, 7438–7442.
35. Sliwa, M., Markovic, D., Gabrusiewicz, K., Synowitz, M., Glass, R., Zawadzka, M., … Kaminska, B. (2007). The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain, 130, 476–489.
36. Sonoda, Y., Kanamori, M., Deen, D. F., Cheng, S. –Y., Berger, M. S., & Pieper, R. O. (2003). Overexpression of vascular endothelial growth factor isoforms drives oxygenation and growth but not progression to glioblastoma multiforme in a human model of gliomagenesis. Cancer Research, 63, 1962–1968.
37. Szulzewsky, F., Arora, S., de Witte, L., Ulas, T., Markovic, D., Schultze, J. L., … Kettenmann, H. (2016). Human glioblastoma-associated microglia/monocytes express a distinct RNA profile compared to human control and murine samples. Glia, 64, 1416–1436.
38. Szulzewsky, F., Pelz, A., Feng, X., Synowitz, M., Markovic, D., Langmann, T., … Kettenmann, H. (2015). Glioma-associated microglia/macrophages display an expression profile different from M1 and M2 polarization and highly express Gpnmb and Spp1. PLoS One, 10, e0116644.
39. Tanabe, S., Lu, Z., Luo, Y., Quackenbush, E. J., Berman, M. A., Collins-Racie, L. A., … Dorf, M. E. (1997). Identification of a new mouse beta-chemokine, thymus-derived chemotactic agent 4, with activity on T lymphocytes and mesangial cells. Journal of Immunology, 159, 5671–5679.
40. Thiel, M., Wolfs, M. J., Bauer, S., Wenning, A. S., Burckhart, T., Schwarz, E. C., … Hoth, M. (2010). Efficiency of T-cell costimulation by CD80 and CD86 cross-linking correlates with calcium entry. Immunology, 129, 28–40.
41. Tseng, D., Vasquez-Medrano, D. A., & Brown, J. M. (2011). Targeting SDF-1/CXCR4 to inhibit tumour vasculature for treatment of glioblastomas. British Journal of Cancer, 104, 1805–1809.
42. Ubezio, B., Blanco, R. A., Geudens, I., Stanchi, F., Mathivet, T., Jones, M. L., … Gerhardt, H. (2016). Synchronization of endothelial Dll4-Notch dynamics switch blood vessels from branching to expansion. eLife, 5, e12167.
43. Umemura, N., Saio, M., Suwa, T., Kitoh, Y., Bai, J., Nonaka, K., … Takami, T. (2008). Tumor-infiltrating myeloid-derived suppressor cells are pleiotropic-inflamed monocytes/macrophages that bear M1- and M2-type characteristics. Journal of Leukocyte Biology, 83, 1136–1144.
44. Wang, S. C., Hong, J. H., Hsueh, C., & Chiang, C. S. (2012). Tumor-secreted SDF-1 promotes glioma invasiveness and TAM tropism toward hypoxia in a murine astrocytoma model. Laboratory Investigation, 92, 151–162.
45. Yang, J., Li, W., He, X., Zhang, G., Yue, L., & Chai, Y. (2015). VEGF overexpression is a valuable prognostic factor for non-Hodgkin's lymphoma evidence from a systemic meta-analysis. Disease Markers, 2015, 786790.
46. Yuan, A., Yu, C. J., Chen, W. J., Lin, F. Y., Kuo, S. H., Luh, K. T., & Yang, P. C. (2000). Correlation of total VEGF mRNA and protein expression with histologic type, tumor angiogenesis, patient survival and timing of relapse in non-small-cell lung cancer. International Journal of Cancer, 89, 475–483.
47. Zhan, P., Ji, Y. N., & Yu, L. K. (2013). VEGF is associated with the poor survival of patients with prostate cancer: A meta-analysis. Translational Andrology and Urology, 2, 99–105.