Laser-induced choroidal neovascularization in mice attenuated by deficiency in the apelin-APJ system

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 6, 2013, Pages 4321-4329

  Hara, Chikako ^a   Kasai, Atsushi ^b   Gomi, Fumi ^a   Satooka, Tatsuya ^b   Sakimoto, Susumu ^a   Nakai, Kei ^a   Yoshioka, Yasuhiro ^b   Yamamuro, Akiko ^b   Maeda, Sadaaki ^b   Nishida, Kohji ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SETSUNAN UNIVERSITY   (Japan)

Author keywords

Agerelated macular degeneration; Apelin; APJ; Choroidal neovascularization; Vascular endothelial growth factor

Indexed keywords

APELIN; APELIN RECEPTOR; SMALL INTERFERING RNA; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LASER COAGULATION; MALE; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBRETINAL NEOVASCULARIZATION;

AGE-RELATED MACULAR DEGENERATION; APELIN; APJ; CHOROIDAL NEOVASCULARIZATION; VASCULAR ENDOTHELIAL GROWTH FACTOR;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANTIGENS, DIFFERENTIATION; CELL PROLIFERATION; CHOROIDAL NEOVASCULARIZATION; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION MEDIATORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LASER COAGULATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; RETINA; RETINAL PIGMENT EPITHELIUM; RNA, MESSENGER; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84879127281     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-11611     Document Type: Article

References (50)

1. Green WR. cegeneration. Mol Vis. 1999;5:27.
2. Fine SL. Age-related macular degeneration 1969-2004: a 35-year personal perspective. Am J Ophthalmol. 2005;139:405-420.
3. Argon laser photocoagulation for neovascular maculopathy. Five-year results from randomized clinical trials. Macular Photocoagulation Study Group. Arch Ophthalmol. 1991;109: 1109-1114.
4. Anderson DH, Mullins RF, Hageman GS, Johnson LV. A role for local inflammation in the formation of drusen in the aging eye. Am J Ophthalmol. 2002;134:411-431.
5. Kvanta A, Algvere PV, Berglin L, Seregard S. Subfoveal fibrovascular membranes in age-related macular degeneration express vascular endothelial growth factor. Invest Ophthalmol Vis Sci. 1996;37:1929-1934.
6. Ishibashi T, Hata Y, Yoshikawa H, Nakagawa K, Sueishi K, Inomata H. Expression of vascular endothelial growth factor in experimental choroidal neovascularization. Graefes Arch Clin Exp Ophthalmol. 1997;235:159-167.
7. Kwak N, Okamoto N, Wood JM, Campochiaro PA. VEGF is major stimulator in model of choroidal neovascularization. Invest Ophthalmol Vis Sci. 2000;41:3158-3164.
8. Heier JS, Brown DM, Chong V, et al. Intravitreal aflibercept (VEGF trap-eye) in wet age-related macular degeneration. Ophthalmology. 2012;119:2537-2548.
9. Tatemoto K, Hosoya M, Habata Y, et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun. 1998;251:471-476.
10. Kleinz MJ, Davenport AP. Immunocytochemical localization of the endogenous vasoactive peptide apelin to human vascular and endocardial endothelial cells. Regul Pept. 2004;118:119-125.
11. del Toro R, Prahst C, Mathivet T, et al. Identification and functional analysis of endothelial tip cell-enriched genes. Blood. 2010;116:4025-4033.
12. Kim J, Kang Y, Kojima Y, et al. An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension. Nat Med. 2013;19:74-82.
13. Kasai A, Shintani N, Oda M, et al. Apelin is a novel angiogenic factor in retinal endothelial cells. Biochem Biophys Res Commun. 2004;325:395-400.
14. Kalin RE, Kretz MP, Meyer AM, Kispert A, Heppner FL, Brandli AW. Paracrine and autocrine mechanisms of apelin signaling govern embryonic and tumor angiogenesis. Dev Biol. 2007; 305:599-614.
15. Saint-Geniez M, Masri B, Malecaze F, Knibiehler B, Audigier Y. Expression of the murine msr/apj receptor and its ligand apelin is upregulated during formation of the retinal vessels. Mech Dev. 2002;110:183-186.
16. Kasai A, Shintani N, Kato H, et al. Retardation of retinal vascular development in apelin-deficient mice. Arterioscler Thromb Vasc Biol. 2008;28:1717-1722.
17. Cox CM, D'Agostino SL, Miller MK, Heimark RL, Krieg PA. Apelin, the ligand for the endothelial G-protein-coupled receptor, APJ, is a potent angiogenic factor required for normal vascular development of the frog embryo. Dev Biol. 2006;296:177-189.
18. Sorli SC, Le Gonidec S, Knibiehler B, Audigier Y. Apelin is a potent activator of tumour neoangiogenesis. Oncogene. 2007; 26:7692-7699.
19. Berta J, Kenessey I, Dobos J, et al. Apelin expression in human non-small cell lung cancer: role in angiogenesis and prognosis. J Thorac Oncol. 2010;5:1120-1129.
20. Kasai A, Ishimaru Y, Kinjo T, et al. Apelin is a crucial factor for hypoxia-induced retinal angiogenesis. Arterioscler Thromb Vasc Biol. 2010;30:2182-2187.
21. Kunduzova O, Alet N, Delesque-Touchard N, et al. Apelin/APJ signaling system: a potential link between adipose tissue and endothelial angiogenic processes. FASEB J. 2008;22:4146-4153.
22. Kidoya H, Ueno M, Yamada Y, et al. Spatial and temporal role of the apelin/APJ system in the caliber size regulation of blood vessels during angiogenesis. EMBO J. 2008;27:522-534.
23. Tao Y, Lu Q, Jiang YR, et al. Apelin in plasma and vitreous and in fibrovascular retinal membranes of patients with proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 2010;51: 4237-4242.
24. Tobe T, Ortega S, Luna JD, et al. Targeted disruption of the FGF2 gene does not prevent choroidal neovascularization in a murine model. Am J Pathol. 1998;153:1641-1646.
25. Nakai K, Fainaru O, Bazinet L, et al. Dendritic cells augment choroidal neovascularization. Invest Ophthalmol Vis Sci. 2008;49:3666-3670.
26. Yamada K, Sakurai E, Itaya M, Yamasaki S, Ogura Y. Inhibition of laser-induced choroidal neovascularization by atorvastatin by downregulation of monocyte chemotactic protein-1 synthesis in mice. Invest Ophthalmol Vis Sci. 2007;48:1839-1843.
27. Secchiero P, Corallini F, Rimondi E, et al. Activation of the p53 pathway down-regulates the osteoprotegerin expression and release by vascular endothelial cells. Blood. 2008;111:1287-1294.
28. Punshon G, Vara DS, Sales KM, Kidane AG, Salacinski HJ, Seifalian AM. Interactions between endothelial cells and a poly(carbonate-silsesquioxane-bridge-urea)urethane. Biomaterials. 2005;26:6271-6279.
29. Shi X, Semkova I, Muther PS, Dell S, Kociok N, Joussen AM. Inhibition of TNF-alpha reduces laser-induced choroidal neovascularization. Exp Eye Res. 2006;83:1325-1334.
30. Noda K, She H, Nakazawa T, et al. Vascular adhesion protein-1 blockade suppresses choroidal neovascularization. FASEB J. 2008;22:2928-2935.
31. Grossniklaus HE, Ling JX, Wallace TM, et al. Macrophage and retinal pigment epithelium expression of angiogenic cytokines in choroidal neovascularization. Mol Vis. 2002;8:119-126.
32. Oh H, Takagi H, Takagi C, et al. The potential angiogenic role of macrophages in the formation of choroidal neovascular membranes. Invest Ophthalmol Vis Sci. 1999;40:1891-1898.
33. Espinosa-Heidmann DG, Suner IJ, Hernandez EP, Monroy D, Csaky KG, Cousins SW. Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:3586-3592.
34. Nozaki M, Raisler BJ, Sakurai E, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci U S A. 2006;103:2328-2333.
35. Masri B, Morin N, Cornu M, Knibiehler B, Audigier Y. Apelin (65-77) activates p70 S6 kinase and is mitogenic for umbilical endothelial cells. FASEB J. 2004;18:1909-1911.
36. McKenzie JA, Fruttiger M, Abraham S, et al. Apelin is required for non-neovascular remodeling in the retina. Am J Pathol. 2012;180:399-409.
37. Edelman JL, Castro MR. Quantitative image analysis of laserinduced choroidal neovascularization in rat. Exp Eye Res. 2000;71:523-533.
38. Han S, Wang G, Qi X, Englander EW, Greeley GH Jr. Involvement of a Stat3 binding site in inflammation-induced enteric apelin expression. Am J Physiol. 2008;295:G1068-G1078.
39. Yu S, Zhang Y, Li MZ, et al. Chemerin and apelin are positively correlated with inflammation in obese type 2 diabetic patients. Chin Med J. 2012;125:3440-3444.
40. Malyszko J, Malyszko JS, Pawlak K, Wolczynski S, Mysliwiec M. Apelin, a novel adipocytokine, in relation to endothelial function and inflammation in kidney allograft recipients. Transplant Proc. 2008;40:3466-3469.
41. Daviaud D, Boucher J, Gesta S, et al. TNFalpha up-regulates apelin expression in human and mouse adipose tissue. FASEB J. 2006;20:1528-1530.
42. Penfold PL, Madigan MC, Gillies MC, Provis JM. Immunological and aetiological aspects of macular degeneration. Prog Retin Eye Res. 2001;20:385-414.
43. Lopez PF, Sippy BD, Lambert HM, Thach AB, Hinton DR. Transdifferentiated retinal pigment epithelial cells are immunoreactive for vascular endothelial growth factor in surgically excised age-related macular degeneration-related choroidal neovascular membranes. Invest Ophthalmol Vis Sci. 1996;37: 855-868.
44. Amin R, Puklin JE, Frank RN. Growth factor localization in choroidal neovascular membranes of age-related macular degeneration. Invest Ophthalmol Vis Sci. 1994;35:3178-3188.
45. Krzystolik MG, Afshari MA, Adamis AP, et al. Prevention of experimental choroidal neovascularization with intravitreal anti-vascular endothelial growth factor antibody fragment. Arch Ophthalmol. 2002;120:338-346.
46. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J. Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2003;44:3578-3585.
47. Tsutsumi C, Sonoda KH, Egashira K, et al. The critical role of ocular-infiltrating macrophages in the development of choroidal neovascularization. J Leukoc Biol. 2003;74:25-32.
48. Kidoya H, Naito H, Takakura N. Apelin induces enlarged and nonleaky blood vessels for functional recovery from ischemia. Blood. 2010;115:3166-3174.
49. Zhao T, Lu Q, Tao Y, Liang XY, Wang K, Jiang YR. Effects of apelin and vascular endothelial growth factor on central retinal vein occlusion in monkey eyes intravitreally injected with bevacizumab: a preliminary study. Mol Vis. 2011;17: 1044-1055.
50. Zhang Y, Jiang YR, Lu Q, Yin H, Tao Y. Apelin in epiretinal fibrovascular membranes of patients with retinopathy of prematurity and the changes after intravitreal bevacizumab. Retina. 2013;33:613-620.