Soluble vascular endothelial growth factor receptor-3 suppresses allosensitization and promotes corneal allograft survival

Graefe's Archive for Clinical and Experimental Ophthalmology

Volumn 252, Issue 11, 2014, Pages 1755-1762

  Emami Naeini, Parisa ^a,b   Dohlman, Thomas H ^a   Omoto, Masahiro ^a   Hattori, Takaaki ^a   Chen, Yihe ^a   Lee, Hyun Soo ^a   Chauhan, Sunil K ^a   Dana, Reza ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

Author keywords

Allosensitization; Angiogenesis; Cornea; Transplantation

Indexed keywords

ALLOANTIGEN; CD31 ANTIGEN; GLYCOPROTEIN; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3; XLKD1 PROTEIN, MOUSE;

ALLOTRANSPLANTATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; COCULTURE; CORNEA; CORNEAL NEOVASCULARIZATION; DRUG EFFECTS; FLOW CYTOMETRY; GRAFT SURVIVAL; IMMUNOLOGY; LYMPHANGIOGENESIS; MALE; METABOLISM; MIXED LYMPHOCYTE CULTURE; MOUSE; PENETRATING KERATOPLASTY;

ANIMALS; ANTIGENS, CD31; CD4-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; CORNEA; CORNEAL NEOVASCULARIZATION; FLOW CYTOMETRY; GLYCOPROTEINS; GRAFT SURVIVAL; ISOANTIGENS; KERATOPLASTY, PENETRATING; LYMPHANGIOGENESIS; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MICE; MICE, INBRED BALB C; TRANSPLANTATION, HOMOLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR D; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84928770449     PISSN: 0721832X     EISSN: 1435702X     Source Type: Journal    
DOI: 10.1007/s00417-014-2749-5     Document Type: Article

References (32)

1. Dietrich T, Bock F, Yuen D et al (2010) Cutting edge: lymphatic vessels, not blood vessels, primarily mediate immune rejections after transplantation. J Immunol 184:535–539. doi:10.4049/jimmunol.0903180
2. Cursiefen C, Cao J, Chen L et al (2004) Inhibition of hemangiogenesis and lymphangiogenesis after normal-risk corneal transplantation by neutralizing VEGF promotes graft survival. Invest Ophthalmol Vis Sci 45:2666–2673. doi:10.1167/iovs.03-1380
3. Bachmann BO, Bock F, Wiegand SJ et al (2008) Promotion of graft survival by vascular endothelial growth factor a neutralization after high-risk corneal transplantation. Arch Ophthalmol 126:71–77. doi:10.1001/archopht.126.1.71
4. Dastjerdi MH, Saban DR, Okanobo A et al (2010) Effects of topical and subconjunctival bevacizumab in high-risk corneal transplant survival. Invest Ophthalmol Vis Sci 51:2411–2417. doi:10.1167/iovs.09-3745
5. Dietrich T, Onderka J, Bock F et al (2007) Inhibition of inflammatory lymphangiogenesis by integrin alpha5 blockade. Am J Pathol 171:361–372
6. Cursiefen C, Chen L, Borges LP et al (2004) VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113:1040–1050. doi:10.1172/JCI20465
7. McGhee CNJ, Dean S, Danesh-Meyer H (2002) Locally administered ocular corticosteroids: benefits and risks. Drug Saf 25:33–55
8. Dana MR, Zhu SN, Yamada J (1998) Topical modulation of interleukin-1 activity in corneal neovascularization. Cornea 17:403–409
9. Dana MR, Qian Y, Hamrah P (2000) Twenty-five-year panorama of corneal immunology: emerging concepts in the immunopathogenesis of microbial keratitis, peripheral ulcerative keratitis, and corneal transplant rejection. Cornea 19:625–643
10. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27–31
11. Nakao S, Zandi S, Hata Y et al (2011) Blood vessel endothelial VEGFR-2 delays lymphangiogenesis: an endogenous trapping mechanism links lymph- and angiogenesis. Blood 117:1081–1090. doi:10.1182/blood-2010-02-267427
12. Cursiefen C, Chen L, Saint-Geniez M et al (2006) Nonvascular VEGF receptor 3 expression by corneal epithelium maintains avascularity and vision. Proc Natl Acad Sci U S A 103:11405–11410. doi:10.1073/pnas.0506112103
13. Hamrah P, Chen L, Zhang Q, Dana MR (2003) Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells. Am J Pathol 163:57–68. doi:10.1016/S0002-9440(10)63630-9
14. Hamrah P, Chen L, Cursiefen C et al (2004) Expression of vascular endothelial growth factor receptor-3 (VEGFR-3) on monocytic bone marrow-derived cells in the conjunctiva. Exp Eye Res 79:553–561. doi:10.1016/j.exer.2004.06.028
15. Hajrasouliha AR, Funaki T, Sadrai Z et al (2012) Vascular endothelial growth factor-C promotes alloimmunity by amplifying antigen-presenting cell maturation and lymphangiogenesis. Invest Ophthalmol Vis Sci 53:1244–1250. doi:10.1167/iovs.11-8668
16. Chen L, Hamrah P, Cursiefen C et al (2004) Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nat Med 10:813–815. doi:10.1038/nm1078
17. Yang H, Kim C, Kim M-J et al (2011) Soluble vascular endothelial growth factor receptor-3 suppresses lymphangiogenesis and lymphatic metastasis in bladder cancer. Mol Cancer 10:36. doi:10.1186/1476-4598-10-36
18. Mäkinen T, Jussila L, Veikkola T et al (2001) Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med 7:199–205. doi:10.1038/84651
19. Hattori T, Saban DR, Emami-Naeini P et al (2012) Donor-derived, tolerogenic dendritic cells suppress immune rejection in the indirect allosensitization-dominant setting of corneal transplantation. J Leukoc Biol 91:621–627. doi:10.1189/jlb.1011500
20. Sonoda Y, Streilein JW (1992) Orthotopic corneal transplantation in mice–evidence that the immunogenetic rules of rejection do not apply. Transplantation 54:694–704
21. Chung E-S, Chauhan SK, Jin Y et al (2009) Contribution of macrophages to angiogenesis induced by vascular endothelial growth factor receptor-3-specific ligands. Am J Pathol 175:1984–1992. doi:10.2353/ajpath.2009.080515
22. Streilein JW, Bradley D, Sano Y, Sonoda Y (1996) Immunosuppressive properties of tissues obtained from eyes with experimentally manipulated corneas. Invest Ophthalmol Vis Sci 37:413–424
23. Chauhan SK, Saban DR, Dohlman TH, Dana R (2014) CCL-21 conditioned regulatory T cells induce allotolerance through enhanced homing to lymphoid tissue. J Immunol 192:817–823. doi:10.4049/jimmunol.1203469
24. Stevenson W, Cheng S-F, Emami-Naeini P et al (2012) Gamma-irradiation reduces the allogenicity of donor corneas. Invest Ophthalmol Vis Sci 53:7151–7158. doi:10.1167/iovs.12-9609
25. Zhang H, Grimaldo S, Yuen D, Chen L (2011) Combined blockade of VEGFR-3 and VLA-1 markedly promotes high-risk corneal transplant survival. Invest Ophthalmol Vis Sci 52:6529–6535. doi:10.1167/iovs.11-7454
26. Thelen A, Scholz A, Benckert C et al (2008) VEGF-D promotes tumor growth and lymphatic spread in a mouse model of hepatocellular carcinoma. Int J Cancer 122:2471–2481. doi:10.1002/ijc.23439
27. Jin Y, Chauhan SK, El Annan J et al (2011) A novel function for programmed death ligand-1 regulation of angiogenesis. Am J Pathol 178:1922–1929. doi:10.1016/j.ajpath.2010.12.027
28. Mor F, Quintana FJ, Cohen IR (2004) Angiogenesis-inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J Immunol 172:4618–4623
29. Pedersen IH, Willerslev-Olsen A, Vetter-Kauczok C et al (2013) Vascular endothelial growth factor receptor-3 expression in mycosis fungoides. Leuk Lymphoma 54:819–826. doi:10.3109/10428194.2012.726720
30. Singh N, Tiem M, Watkins R et al (2013) Soluble vascular endothelial growth factor receptor 3 is essential for corneal alymphaticity. Blood 121:4242–4249. doi:10.1182/blood-2012-08-453043
31. Dana MR (2004) Corneal antigen-presenting cells: diversity, plasticity, and disguise: the Cogan lecture. Invest Ophthalmol Vis Sci 45:722–727, 721
32. Jin Y, Shen L, Chong E-M et al (2007) The chemokine receptor CCR7 mediates corneal antigen-presenting cell trafficking. Mol Vis 13:626–634