VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment

Journal of Clinical Investigation

Volumn 113, Issue 7, 2004, Pages 1040-1050

  Cursiefen, Claus ^a   Chen, Lu ^a   Borges, Leonardo P ^a   Jackson, David ^b   Cao, Jingtai ^c   Radziejewski, Czeslaw ^c   D'Amore, Patricia A ^a   Dana, M Reza ^a   Wiegand, Stanley J ^c   Streilein, J Wayne ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLODRONIC ACID; HYBRID PROTEIN; ISOPROTEIN; VASCULOTROPIN A; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CHEMOTAXIS; CONTROLLED STUDY; CORNEA INJURY; HEMANGIOGENESIS; INFLAMMATION; IRRADIATION; LYMPH VESSEL; LYMPHANGIOGENESIS; MACROPHAGE MIGRATION; METASTASIS; MONOCYTE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TRANSPLANTATION;

EID: 11144355004     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI20465     Document Type: Article

References (54)

1. Folkman, J. 1995. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1:27-31.
2. Carmeliet, P. 2003. Angiogenesis in health and disease. Nat. Med. 9:653-660.
3. Kerbel, R., and Folkman, J. 2002. Clinical translation of angiogenesis inhibitors. Nat. Rev. Cancer. 2:727-739.
4. Stacker, S.A., Achen, M.G., Jussila, L., Baldwin, M.E., and Alitalo, K. 2002. Lymphangiogenesis and cancer metastasis. Nat. Rev. Cancer. 2:573-583.
5. He, Y., et al. 2002. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J. Natl. Cancer. Inst. 94:819-825.
6. Skobe, M., et al. 2001. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat. Med. 7:192-198.
7. Padera, T.P., et al. 2002. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science. 296:1883-1886.
8. Schoppmann, S.F., et al. 2002. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am. J. Pathol. 161:947-956.
9. Rissanen, T.T., et al. 2003. VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ. Res. 92:1098-1106.
10. Cao, Y., et al. 1998. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 95:14389-14394.
11. Kubo, H., et al. 2002. Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc. Natl. Acad. Sci. U. S. A. 99:8868-8873.
12. Byzova, T.V., et al. 2002. Adenovirus encoding vascular endothelial growth factor-D induces tissue-specific vascular patterns in vivo. Blood. 99:4434-4442.
13. Enholm, B., et al. 2001. Adenoviral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ. Res. 88:623-629.
14. Saaristo, A., et al. 2002. Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J. 16:1041-1049.
15. Oh, S.J., et al. 1997. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev. Biol. 188:96-109.
16. Podgrabinska, S., et al. 2002. Molecular characterization of lymphatic endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 99:16069-16074.
17. Hirakawa, S., et al. 2003. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 162:575-586.
18. Petrova, T.V., et al. 2002. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 21:4593-4599.
19. Jeltsch, M., et al. 1997. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 276:1423-1425.
20. Nagy, J.A., et al. 2002. Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J. Exp. Med. 196:1497-1506.
21. Streilein, J.W., Yamada, J., Dana, M.R., and Ksander, B.R. 1999. Anterior chamber-associated immune deviation, ocular immune privilege, and orthotopic corneal allografts. Transplant. Proc. 31:1472-1475.
22. Cursiefen, C., et al. 2002. Lymphatic vessels in vascularized human corneas: immunohistochemical investigation using LYVE-1 and podoplanin. Invest. Ophthalmol. Vis. Sci. 43:2127-2135.
23. Chang, L., Kaipainen, A., and Folkman, J. 2002. Lymphangiogenesis new mechanisms. Ann. N. Y. Acad. Sci. 979:111-119.
24. Holash, J., et al. 2002. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc. Natl. Acad. Sci. U. S. A. 99:11393-11398.
25. Shima, D.T., et al. 1996. The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and post-transcriptional regulatory sequences. J. Biol. Chem. 271:3877-3883.
26. Stalmans, I., et al. 2002. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109:327-336.
27. Shen, H., et al. 1993. Characterization of vascular permeability factor/vascular endothelial growth factor receptors on mononuclear phagocytes. Blood. 81:2767-2773.
28. Barleon, B., et al. 1996. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood. 87:3336-3343.
29. Streilein, J.W., Bradley, D., Sano, Y., and Sonoda, Y. 1996. Immunosuppressive properties of tissues obtained from eyes with experimentally manipulated corneas. Invest. Ophthalmol. Vis. Sci. 37:413-424.
30. Banerji, S., et al. 1999. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell. Biol. 144:789-801.
31. Van der Veen, G., et al. 1994. Prevention of corneal allograft rejection in rats treated with subconjunctival injections of liposomes containing dichloromethylene diphosphonate. Invest. Ophthalmol. Vis. Sci. 35:3505-3515.
32. Van Rooijen, N., and Sanders, A. 1994. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods. 174:83-93.
33. Rutherford, M.S., and Schook, L.B. 1992. Differential immunocompetence of macrophages derived using macrophage or granulocyte-macrophage colony-stimulating factor. J. Leukoc. Biol. 51:69-76.
34. Paavonen, K., Puolakkainen, P., Jussila, L., Jahkola, T., and Alitalo, K. 2000. Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am. J. Pathol. 156:1499-1504.
35. Berse, B., Brown, L.F., Van de Water, L., Dvorak, H.F., and Senger, D.R. 1992. Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues; macrophages, and tumors. Mol. Biol. Cell. 3:211-220.
36. Alitalo, K., and Carmeliet, P. 2002. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell. 1:219-227.
37. Partanen, TA., Alitalo, K., and Miettinen, M. 1999. Lack of lymphatic vascular specificity of vascular endothelial growth factor receptor 3 in 185 vascular tumors. Cancer. 86:2406-2412.
38. Clauss, M., et al. 1996. 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. 271:17629-17634.
39. Hiratsuka, S., Minowa, O., Kuno, J., Noda, T., and Shibuya, M. 1998. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 95:9349-9354.
40. Freeman, M.R., et al. 1995. Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res. 55:4140-4145.
41. Taichman, N.S., Young, S., Cruchley, A.T., Taylor, P., and Paleolog, E. 1997. Human neutrophils secrete vascular endothelial growth factor. J. Leukoc. Biol. 62:397-400.
42. Schoppmann, S.F., et al. 2001. Inflammatory stromal reaction correlates with lymphatic microvessel density in early-stage cervical cancer. Anticancer Res. 21:3419-3423.
43. Paavonen, K., et al. 2002. Vascular endothelial growth factors C and D and their VEGFR-2 and 3 receptors in blood and lymphatic vessels in healthy and arthritic synovium. J. Rheumatol. 29:39-45.
44. Ristimaki, A., Narko, K., Enholm, B., Joukov, V., and Alitalo, K. 1998. Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J. Biol. Chem. 273:8413-8418.
45. Ishida, S., et al. 2003. VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J. Exp. Med. 198:483-489.
46. Fromer, C.H., and Klintworth, G.K. 1975. An evaluation of the role of leukocytes in the pathogenesis of experimentally induced corneal vascularization. II. Studies on the effect of leukocytic elimination on corneal vascularization. Am. J. Pathol. 81:531-544.
47. Melder, R.J., et al. 1996. During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat. Med. 2:992-997.
48. Lu, M., et al. 1999. VEGF increases retinal vascular ICAM-1 expression in vivo. Invest. Ophthalmol. Vis. Sci. 40:1808-1812.
49. Boardman, K.C., and Swartz, M.A. 2003. Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 92:801-808.
50. Gerhardt, H., et al. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell. Biol. 161:1163-1177.
51. Luttun, A., Tjwa, M., and Carmeliet, P. 2002. Placental growth factor (PIGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann. N. Y. Acad. Sci. 979:80-93.
52. Luttun, A., et al. 2002. Revascularization of ischemic tissues by PIGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat. Med. 8:831-840.
53. Karkkainen, M.J., and Petrova, T.V. 2000. Vascular endothelial growth factor receptors in the regulation of angiogenesis and lymphangiogenesis. Oncogene. 19:5598-5605.
54. Veikkola, T., et al. 2001. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J. 20:1223-1231.