Immune cells regulate VEGF signalling via release of VEGF and antagonistic soluble VEGF receptor-1

Clinical and Experimental Immunology

Volumn 192, Issue 1, 2018, Pages 54-67

  Hoeres, T ^a   Wilhelm, M ^a   Smetak, M ^a   Holzmann, E ^a   Schulze Tanzil, G ^a   Birkmann, J ^a  

^a Paracelsus Medical University   (Germany)

Author keywords

interleukin 2; monocyte; soluble VEGF receptor; VEGF;

Indexed keywords

CD14 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; SOLUBLE VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR 1; SOLUBLE VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR 2; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3; ZOLEDRONIC ACID; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR; VEGFA PROTEIN, HUMAN;

ADULT; ALPHA BETA T LYMPHOCYTE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DAUDI CELL LINE; DRUG MECHANISM; FEMALE; GAMMA DELTA T LYMPHOCYTE; GENE EXPRESSION; HL-60 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IN VITRO STUDY; INFLAMMATION; K-562 CELL LINE; KG-1 CELL LINE; MALE; MONOCYTE; NATURAL KILLER CELL; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REGULATORY MECHANISM; REH CELL LINE; T LYMPHOCYTE; THP-1 CELL LINE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; U266B1 CELL LINE; VEGF SIGNALING; BLOOD; DRUG EFFECT; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); SIGNAL TRANSDUCTION; TUMOR CELL LINE; YOUNG ADULT;

ADULT; CELL LINE, TUMOR; FEMALE; HUMANS; INTERLEUKIN-2; KILLER CELLS, NATURAL; MALE; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; YOUNG ADULT; ZOLEDRONIC ACID;

EID: 85043351688     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.13090     Document Type: Article

References (67)

1. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140:883–99.
2. Gentles AJ, Newman AM, Liu CL et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med 2015; 21:938–45.
3. Wakita D, Sumida K, Iwakura Y et al. Tumor-infiltrating IL-17-producing gammadelta T cells support the progression of tumor by promoting angiogenesis. Eur J Immunol 2010; 40:1927–37.
4. Rei M, Pennington DJ, Silva-Santos B. The emerging protumor role of gammadelta T lymphocytes: implications for cancer immunotherapy. Cancer Res 2015; 75:798–802.
5. Kunzmann V, Bauer E, Feurle J, Weissinger F, Tony HP, Wilhelm M. Stimulation of gammadelta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood 2000; 96:384–92.
6. Viey E, Fromont G, Escudier B et al. Phosphostim-activated gamma delta T cells kill autologous metastatic renal cell carcinoma. J Immunol 2005; 174:1338–47.
7. Kabelitz D, Wesch D, Pitters E, Zoller M. Characterization of tumor reactivity of human V gamma 9V delta 2 gamma delta T cells in vitro and in SCID mice in vivo. J Immunol 2004; 173:6767–76.
8. Wilhelm M, Kunzmann V, Eckstein S et al. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood 2003; 102:200–6.
9. Fisher JP, Heuijerjans J, Yan M, Gustafsson K, Anderson J. Gammadelta T cells for cancer immunotherapy: a systematic review of clinical trials. Oncoimmunology 2014; 3:e27572.
10. Van Acker HH, Anguille S, Willemen Y, Smits EL, Van Tendeloo VF. Bisphosphonates for cancer treatment: mechanisms of action and lessons from clinical trials. Pharmacol Ther 2016; 158:24–40.
11. Santini D, Vincenzi B, Avvisati G et al. Pamidronate induces modifications of circulating angiogenetic factors in cancer patients. Clin Cancer Res 2002; 8:1080–4.
12. Santini D, Vincenzi B, Dicuonzo G et al. Zoledronic acid induces significant and long-lasting modifications of circulating angiogenic factors in cancer patients. Clin Cancer Res 2003; 9:2893–7.
13. Santini D, Vincenzi B, Galluzzo S et al. Repeated intermittent low-dose therapy with zoledronic acid induces an early, sustained, and long-lasting decrease of peripheral vascular endothelial growth factor levels in cancer patients. Clin Cancer Res 2007; 13:4482–6.
14. Goel HL, Mercurio AM. VEGF targets the tumour cell. Nat Rev Cancer 2013; 13:871–82.
15. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 1999; 13:9–22.
16. Lee S, Chen TT, Barber CL et al. Autocrine VEGF signalling is required for vascular homeostasis. Cell 2007; 130:691–703.
17. Ferrara N, Adamis AP. Ten years of anti-vascular endothelial growth factor therapy. Nat Rev Drug Discov 2016; 15:385–403.
18. Li YL, Zhao H, Ren XB. Relationship of VEGF/VEGFR with immune and cancer cells: staggering or forward? Cancer Biol Med 2016; 13:206–14.
19. Finley SD, Chu LH, Popel AS. Computational systems biology approaches to anti-angiogenic cancer therapeutics. Drug Discov Today 2015; 20:187–97.
20. Atkins MB, McDermott DF, Powles T et al. IMmotion150: a phase II trial in untreated metastatic renal cell carcinoma (mRCC) patients (pts) of atezolizumab (atezo) and bevacizumab (bev) vs and following atezo or sunitinib (sun). J Clin Oncol 2017; 35:4505.
21. Kunzmann V, Smetak M, Kimmel B et al. Tumor-promoting versus tumor-antagonizing roles of gammadelta T cells in cancer immunotherapy: results from a prospective phase I/II trial. J Immunother 2012; 35:205–13.
22. Edelbauer M, Datta D, Vos IH et al. Effect of vascular endothelial growth factor and its receptor KDR on the transendothelial migration and local trafficking of human T cells in vitro and in vivo. Blood 2010; 116:1980–9.
23. Gavalas NG, Tsiatas M, Tsitsilonis O et al. VEGF directly suppresses activation of T cells from ascites secondary to ovarian cancer via VEGF receptor type 2. Br J Cancer 2012; 107:1869–75.
24. Zhang J, Silva T, Yarovinsky T et al. VEGF blockade inhibits lymphocyte recruitment and ameliorates immune-mediated vascular remodeling. Circ Res 2010; 107:408–17.
25. Basu A, Hoerning A, Datta D et al. Cutting edge: vascular endothelial growth factor-mediated signalling in human CD45RO+ CD4+ T cells promotes Akt and ERK activation and costimulates IFN-gamma production. J Immunol 2010; 184:545–9.
26. Laggner U, Di Meglio P, Perera GK et al. Identification of a novel proinflammatory human skin-homing Vgamma9Vdelta2 T cell subset with a potential role in psoriasis. J Immunol 2011; 187:2783–93.
27. Schilbach K, Frommer K, Meier S, Handgretinger R, Eyrich M. Immune response of human propagated gammadelta-T cells to neuroblastoma recommend the Vdelta1+ subset for gammadelta-T cell-based immunotherapy. J Immunother 2008; 31:896–905.
28. Eubank TD, Roberts R, Galloway M, Wang Y, Cohn DE, Marsh CB. GM-CSF induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity 2004; 21:831–42.
29. Eubank TD, Galloway M, Montague CM, Waldman WJ, Marsh CB. M-CSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J Immunol 2003; 171:2637–43.
30. Bottomley MJ, Webb NJ, Watson CJ, Holt PJ, Freemont AJ, Brenchley PE. Peripheral blood mononuclear cells from patients with rheumatoid arthritis spontaneously secrete vascular endothelial growth factor (VEGF): specific up-regulation by tumour necrosis factor-alpha (TNF-alpha) in synovial fluid. Clin Exp Immunol 1999; 117:171–6.
31. Fava RA, Olsen NJ, Spencer GG et al. Vascular permeability factor/endothelial growth factor (VPF/VEGF): accumulation and expression in human synovial fluids and rheumatoid synovial tissue. J Exp Med 1994; 180:341–6.
32. Freeman MR, Schneck FX, Gagnon ML et al. Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res 1995; 55:4140–5.
33. Mor F, Quintana FJ, Cohen IR. Angiogenesis–inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J Immunol 2004; 172:4618–23.
34. Matsuyama W, Kubota R, Hashiguchi T et al. Purified protein derivative of tuberculin upregulates the expression of vascular endothelial growth factor in T lymphocytes in vitro. Immunology 2002; 106:96–101.
35. R&D Systems Inc. Quantikine ELISA human VEGF handbook. 2015.
36. Gunsilius E, Petzer A, Stockhammer G et al. Thrombocytes are the major source for soluble vascular endothelial growth factor in peripheral blood. Oncology 2000; 58:169–74.
37. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, Marmé D. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 1996; 87:3336–43.
38. Clauss M, Weich H, Breier G et al. The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 1996; 271:17629–34.
39. Shin JY, Yoon IH, Kim JS, Kim B, Park CG. Vascular endothelial growth factor-induced chemotaxis and IL-10 from T cells. Cell Immunol 2009; 256:72–8.
40. Voron T, Colussi O, Marcheteau E et al. VEGF-A modulates expression of inhibitory checkpoints on CD8+ T cells in tumors. J Exp Med 2015; 212:139–48.
41. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signaling – in control of vascular function. Nat Rev Mol Cell Biol 2006; 7:359–71.
42. Santos SC, Dias S. Internal and external autocrine VEGF/KDR loops regulate survival of subsets of acute leukemia through distinct signalling pathways. Blood 2004; 103:3883–9.
43. Kerbel RS. Tumor angiogenesis. N Engl J Med 2008; 358:2039–49.
44. Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 1996; 226:324–8.
45. Barleon B, Reusch P, Totzke F et al. Soluble VEGFR-1 secreted by endothelial cells and monocytes is present in human serum and plasma from healthy donors. Angiogenesis 2001; 4:143–54.
46. Roeckl W, Hecht D, Sztajer H, Waltenberger J, Yayon A, Weich HA. Differential binding characteristics and cellular inhibition by soluble VEGF receptors 1 and 2. Exp Cell Res 1998; 241:161–70.
47. Pavlakovic H, Becker J, Albuquerque R, Wilting J, Ambati J. Soluble VEGFR-2: an anti-lymphangiogenic variant of VEGF receptors. Ann NY Acad Sci 2010; 1207:E7–15.
48. Reinders ME, Sho M, Izawa A et al. Proinflammatory functions of vascular endothelial growth factor in alloimmunity. J Clin Invest 2003; 112:1655–65.
49. Gabrilovich DI, Chen HL, Girgis KR et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med 1996; 2:1096–103.
50. Terme M, Tartour E, Taieb J. VEGFA/VEGFR2-targeted therapies prevent the VEGFA-induced proliferation of regulatory T cells in cancer. Oncoimmunology 2013; 2:e25156.
51. Sabatino M, Kim-Schulze S, Panelli MC et al. Serum vascular endothelial growth factor and fibronectin predict clinical response to high-dose interleukin-2 therapy. J Clin Oncol 2009; 27:2645–52.
52. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002; 196:254–65.
53. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011; 11:723–37.
54. Insalaco L, Di Gaudio F, Terrasi M et al. Analysis of molecular mechanisms and anti-tumoural effects of zoledronic acid in breast cancer cells. J Cell Mol Med 2012; 16:2186–95.
55. Steidl C, Lee T, Shah SP et al. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med 2010; 362:875–85.
56. Kridel R, Steidl C, Gascoyne RD. Tumor-associated macrophages in diffuse large B-cell lymphoma. Haematologica 2015; 100:143–5.
57. Wu WK, Llewellyn OP, Bates DO, Nicholson LB, Dick AD. IL-10 regulation of macrophage VEGF production is dependent on macrophage polarisation and hypoxia. Immunobiology 2010; 215:796–803.
58. Justiniano SE, Elavazhagan S, Fatehchand K et al. Fcgamma receptor-induced soluble vascular endothelial growth factor receptor-1 (VEGFR-1) production inhibits angiogenesis and enhances efficacy of anti-tumor antibodies. J Biol Chem 2013; 288:26800–9.
59. Kishuku M, Nishioka Y, Abe S et al. Expression of soluble vascular endothelial growth factor receptor-1 in human monocyte-derived mature dendritic cells contributes to their antiangiogenic property. J Immunol 2009; 183:8176–85.
60. Wu WK, Georgiadis A, Copland DA et al. IL-4 regulates specific Arg-1(+) macrophage sFlt-1-mediated inhibition of angiogenesis. Am J Pathol 2015; 185:2324–35.
61. Melton DW, McManus LM, Gelfond JA, Shireman PK. Temporal phenotypic features distinguish polarized macrophages in vitro. Autoimmunity 2015; 48:161–76.
62. Zloza A, Dharmadhikari ND, Huelsmann EJ, Broucek JR, Hughes T, Kohlhapp FJ, Kaufman HL. Low-dose interleukin-2 impairs host anti-tumor immunity and inhibits therapeutic responses in a mouse model of melanoma. Cancer Immunol Immunother 2016; 66:9–16.
63. Burdach S, Zessack N, Dilloo D, Shatsky M, Thompson D, Levitt L. Differential regulation of lymphokine production by distinct subunits of the T cell interleukin 2 receptor. J Clin Invest 1991; 87:2114–21.
64. Levitt LJ, Nagler A, Lee F, Abrams J, Shatsky M, Thompson D. Production of granulocyte/macrophage-colony-stimulating factor by human natural killer cells. Modulation by the p75 subunit of the interleukin 2 receptor and by the CD2 receptor. J Clin Invest 1991; 88:67–75.
65. Panelli MC, Wang E, Phan G et al. Gene-expression profiling of the response of peripheral blood mononuclear cells and melanoma metastases to systemic IL-2 administration. Genome Biol 2002; 3:RESEARCH0035.
66. Wu FTH, Stefanini MO, Mac Gabhann F, Popel AS, Lucia A. A compartment model of VEGF distribution in humans in the presence of soluble VEGF receptor-1 acting as a ligand trap. PLOS ONE 2009; 4:e5108.
67. Stefanini MO, Wu FT, Mac Gabhann F, Popel AS. A compartment model of VEGF distribution in blood, healthy and diseased tissues. BMC Syst Biol 2008; 2:77.