Sunitinib inhibits inflammatory corneal lymphangiogenesis

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 5, 2013, Pages 3082-3093

  Detry, Benoît ^a   Blacher, Silvia ^a   Erpicum, Charlotte ^a   Paupert, Jenny ^a   Maertens, Ludovic ^a   Maillard, Catherine ^a   Munaut, Carine ^a   Sounni, Nor Eddine ^a   Lambert, Vincent ^a,b   Foidart, Jean Michel ^a   Rakic, Jean Marie ^b   Cataldo, Didier ^a   Noël, Agnès ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Corneal neovascularization; Lymphangiogenesis; Sunitinib

Indexed keywords

PLACENTAL GROWTH FACTOR; SUNITINIB; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAUTERIZATION; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; CORNEA NEOVASCULARIZATION; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; LYMPHANGIOGENESIS; MACROPHAGE; MALE; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIOIMMUNOPRECIPITATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CORNEAL NEOVASCULARIZATION; LYMPHANGIOGENESIS; SUNITINIB;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIGENS, CD31; CELL PROLIFERATION; CORNEAL NEOVASCULARIZATION; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLYCOPROTEINS; INDOLES; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; PREGNANCY PROTEINS; PROTEIN-TYROSINE KINASES; PYRROLES; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84877116642     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-10856     Document Type: Article

References (44)

1. Ellenberg D, Azar DT, Hallak JA, et al. Novel aspects of corneal angiogenic and lymphangiogenic privilege. Prog Retin Eye Res. 2010;29:208-248.
2. Albuquerque RJ, Hayashi T, Cho WG, et al. Alternatively spliced vascular endothelial growth factor receptor-2 is an essential endogenous inhibitor of lymphatic vessel growth. Nat Med. 2009;15:1023-1030.
3. Ambati BK, Nozaki M, Singh N, et al. Corneal avascularity is due to soluble VEGF receptor-1. Nature. 2006;443:993-997.
4. Ambati BK, Patterson E, Jani P, et al. Soluble vascular endothelial growth factor receptor-1 contributes to the corneal antiangiogenic barrier. Br J Ophthalmol. 2007;91: 505-508.
5. Cursiefen C, Maruyama K, Bock F, et al. Thrombospondin 1 inhibits inflammatory lymphangiogenesis by CD36 ligation on monocytes. J Exp Med. 2011;208:1083-1092.
6. Azar DT. Corneal angiogenic privilege: angiogenic and antiangiogenic factors in corneal avascularity, vasculogenesis, and wound healing (an American Ophthalmological Society thesis). Trans Am Ophthalmol Soc. 2006;104:264-302.
7. Cursiefen C, Colin J, Dana R, et al. Consensus statement on indications for anti-angiogenic therapy in the management of corneal diseases associated with neovascularisation: outcome of an expert roundtable. Br J Ophthalmol. 2012;96:3-9.
8. Cursiefen C. Immune privilege and angiogenic privilege of the cornea. Chem Immunol Allergy. 2007;92:50-57.
9. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 2009;21:154-165.
10. Regenfuss B, Bock F, Parthasarathy A, Cursiefen C. Corneal (lymph)angiogenesis-from bedside to bench and back: a tribute to Judah Folkman. Lymphat Res Biol. 2008;6:191-201.
11. Wuest TR, Carr DJ. VEGF-A expression by HSV-1-infected cells drives corneal lymphangiogenesis. J Exp Med. 2010;207:101-115.
12. Cursiefen C, Chen L, Borges LP, et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest. 2004;113:1040-1050.
13. Noel A, Jost M, Lambert V, Lecomte J, Rakic JM. Antiangiogenic therapy of exudative age-related macular degeneration: current progress and emerging concepts. Trends Mol Med. 2007;13:345-352.
14. Bock F, Onderka J, Dietrich T, et al. Bevacizumab as a potent inhibitor of inflammatory corneal angiogenesis and lymphangiogenesis. Invest Ophthalmol Vis Sci. 2007;48:2545-2552.
15. Cursiefen C, Cao J, Chen L, et al. Inhibition of hemangiogenesis and lymphangiogenesis after normal-risk corneal transplantation by neutralizing VEGF promotes graft survival. Invest Ophthalmol Vis Sci. 2004;45:2666-2673.
16. Hos D, Bock F, Dietrich T, et al. Inflammatory corneal (lymph)angiogenesis is blocked by VEGFR-tyrosine kinase inhibitor ZK 261991, resulting in improved graft survival after corneal transplantation. Invest Ophthalmol Vis Sci. 2008;49: 1836-1842.
17. Hos D, Saban DR, Bock F, et al. Suppression of inflammatory corneal lymphangiogenesis by application of topical corticosteroids. Arch Ophthalmol. 2011;129:445-452.
18. Faivre S, Demetri G, Sargent W, Raymond E. Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov. 2007;6:734-745.
19. Perez-Santonja JJ, Campos-Mollo E, Lledo-Riquelme M, Javaloy J, Alio JL. Inhibition of corneal neovascularization by topical bevacizumab (anti-VEGF) and sunitinib (anti-VEGF and anti- PDGF) in an animal model. Am J Ophthalmol. 2010;150:519-528. e511.
20. Kodera Y, Katanasaka Y, Kitamura Y, et al. Sunitinib inhibits lymphatic endothelial cell functions and lymph node metastasis in a breast cancer model through inhibition of vascular endothelial growth factor receptor 3. Breast Cancer Res. 2011;13:R66.
21. Blacher S, Detry B, Bruyere F, Foidart JM, Noel A. Additional parameters for the morphometry of angiogenesis and lymphangiogenesis in corneal flat mounts. Exp Eye Res. 2009;89: 274-276.
22. Detry B, Bruyere F, Erpicum C, et al. Digging deeper into lymphatic vessel formation in vitro and in vivo. BMC Cell Biol. 2011;12:29.
23. Detry B, Erpicum C, Paupert J, et al. Matrix metalloproteinase- 2 governs lymphatic vessel formation as an interstitial collagenase. Blood. 2012;119:5048-5056.
24. Soille P. Morphological Image Analysis. Berlin: Springer- Verlag; 1999.
25. Kohler R. A segmentation system based on thresholding. Computer Graphics and Image Processing. 1981;319-338.
26. Davies JQ, Gordon S. Isolation and culture of human macrophages. Methods Mol Biol. 2005;290:105-116.
27. Berndt S, Blacher S, Perrier d'Hauterive S, et al. Chorionic gonadotropin stimulation of angiogenesis and pericyte recruitment. J Clin Endocrinol Metab. 2009;94:4567-4574.
28. Bruyere F, Melen-Lamalle L, Berndt S, Peulen O, Foidart JM, Noel A. The lymphatic ring assay: a 3D-culture model of lymphangiogenesis. Nat Protoc. 2008. doi:10.1038/nprot. 2008.86.
29. Bruyere F, Melen-Lamalle L, Blacher S, et al. Modeling lymphangiogenesis in a three-dimensional culture system. Nat Methods. 2008;5:431-437.
30. Blacher S, Devy L, Burbridge MF, et al. Improved quantification of angiogenesis in the rat aortic ring assay. Angiogenesis. 2001; 4:133-142.
31. Maruyama K, Nakazawa T, Cursiefen C, et al. The maintenance of lymphatic vessels in the cornea is dependent on the presence of macrophages. Invest Ophthalmol Vis Sci. 2012; 53:3145-3153.
32. Dana MR. Angiogenesis and lymphangiogenesis-implications for corneal immunity. Semin Ophthalmol. 2006;21:19-22.
33. Gordon EJ, Rao S, Pollard JW, Nutt SL, Lang RA, Harvey NL. Macrophages define dermal lymphatic vessel calibre during development by regulating lymphatic endothelial cell proliferation. Development. 2010;137:3899-3910.
34. Maruyama K, Ii M, Cursiefen C, et al. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest. 2005;115:2363-2372.
35. Gelati M, Aplin AC, Fogel E, Smith KD, Nicosia RF. The angiogenic response of the aorta to injury and inflammatory cytokines requires macrophages. J Immunol. 2008;181:5711-5719.
36. Nicosia RF, Zorzi P, Ligresti G, Morishita A, Aplin AC. Paracrine regulation of angiogenesis by different cell types in the aorta ring model. Int J Dev Biol. 2011;55:447-453.
37. Bachmann B, Taylor RS, Cursiefen C. Corneal neovascularization as a risk factor for graft failure and rejection after keratoplasty: an evidence-based meta-analysis. Ophthalmology. 2010;117:1300-1305. e1307.
38. Bachmann BO, Luetjen-Drecoll E, Bock F, et al. Transient postoperative vascular endothelial growth factor (VEGF)- neutralisation improves graft survival in corneas with partly regressed inflammatory neovascularisation. Br J Ophthalmol. 2009;93:1075-1080.
39. Dell S, Peters S, Muther P, Kociok N, Joussen AM. The role of PDGF receptor inhibitors and PI3-kinase signaling in the pathogenesis of corneal neovascularization. Invest Ophthalmol Vis Sci. 2006;47:1928-1937.
40. Alitalo K. The lymphatic vasculature in disease. Nat Med. 2011;17:1371-1380.
41. Cao R, Eriksson A, Kubo H, Alitalo K, Cao Y, Thyberg J. Comparative evaluation of FGF-2-, VEGF-A-, and VEGF-Cinduced angiogenesis, lymphangiogenesis, vascular fenestrations, and permeability. Circ Res. 2004;94:664-670.
42. Mimura T, Amano S, Usui T, Kaji Y, Oshika T, Ishii Y. Expression of vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 in corneal lymphangiogenesis. Exp Eye Res. 2001;72:71-78.
43. Chaoran Z, Zhirong L, Gezhi X. Combination of vascular endothelial growth factor receptor/platelet-derived growth factor receptor inhibition markedly improves the antiangiogenic efficacy for advanced stage mouse corneal neovascularization. Graefes Arch Clin Exp Ophthalmol. 2011;249:1493-1501.
44. Jo N, Mailhos C, Ju M, et al. Inhibition of platelet-derived growth factor B signaling enhances the efficacy of anti-vascular endothelial growth factor therapy in multiple models of ocular neovascularization. Am J Pathol. 2006;168:2036-2053.