Seeing through VEGF: Innate and adaptive immunity in pathological angiogenesis in the eye

Trends in Molecular Medicine

Volumn 21, Issue 1, 2015, Pages 43-51

  Sene, Abdoulaye ^a   Chin Yee, David ^a   Apte, Rajendra S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Age related macular degeneration (AMD); Angiogenesis; Diabetic retinopathy; Immune regulation; Neovascularization; Vascular endothelial growth factor (VEGF)

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN A;

ADAPTIVE IMMUNITY; AGE RELATED MACULAR DEGENERATION; ANGIOGENESIS; CELL SURVIVAL; CENTRAL SCOTOMA; CORNEA NEOVASCULARIZATION; EYE; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; LASER COAGULATION; MACROPHAGE; PHOTORECEPTOR CELL; RETINA BLOOD VESSEL; RETROLENTAL FIBROPLASIA; REVIEW; UPREGULATION; ANIMAL; EYE DISEASE; GENETICS; IMMUNOLOGY; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

ADAPTIVE IMMUNITY; ANIMALS; EYE; EYE DISEASES; HUMANS; IMMUNITY, INNATE; NEOVASCULARIZATION, PATHOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84927640278     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.10.005     Document Type: Review

References (99)

1. Rajappa M., et al. Ocular angiogenesis: mechanisms and recent advances in therapy. Adv. Clin. Chem. 2010, 50:103-121.
2. Safi S.Z., et al. Molecular mechanisms of diabetic retinopathy, general preventive strategies, and novel therapeutic targets. BioMed Res. Int. 2014, 2014:801269.
3. Chou J., et al. Role of endothelial cell and pericyte dysfunction in diabetic retinopathy: review of techniques in rodent models. Adv. Exp. Med. Biol. 2014, 801:669-675.
4. Friedman D.S., et al. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 2004, 122:564-572.
5. Sene A., Apte R.S. Eyeballing cholesterol efflux and macrophage function in disease pathogenesis. Trends Endocrinol. Metab. 2014, 25:107-114.
6. Klein R., et al. The epidemiology of age-related macular degeneration. Am. J. Ophthalmol. 2004, 137:486-495.
7. Terry T.L. Fibroblastic overgrowth of persistent tunica vasculosa lentis in infants born prematurely: II. Report of cases-clinical aspects. Trans. Am. Ophthalmol. Soc. 1942, 40:262-284.
8. Anonymous Multicenter trial of cryotherapy for retinopathy of prematurity. Preliminary results. Cryotherapy for Retinopathy of Prematurity Cooperative Group. Arch. Ophthalmol. 1988, 106:471-479.
9. Mechoulam H., Pierce E.A. Retinopathy of prematurity: molecular pathology and therapeutic strategies. Am. J. Pharmacogenom 2003, 3:261-277.
10. Olsson A.K., et al. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 2006, 7:359-371.
11. Qazi Y., et al. Mediators of ocular angiogenesis. J. Genet. 2009, 88:495-515.
12. Dorrell M.I., et al. Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest. Ophthalmol. Vis. Sci. 2002, 43:3500-3510.
13. Dorrell M.I., Friedlander M. Mechanisms of endothelial cell guidance and vascular patterning in the developing mouse retina. Prog. Retin. Eye Res. 2006, 25:277-295.
14. Stalmans I., et al. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 2002, 109:327-336.
15. Bock F., et al. Novel anti(lymph)angiogenic treatment strategies for corneal and ocular surface diseases. Prog. Retin. Eye Res. 2013, 34:89-124.
16. Cursiefen C., 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.
17. Marneros A.G., et al. Vascular endothelial growth factor expression in the retinal pigment epithelium is essential for choriocapillaris development and visual function. Am. J. Pathol. 2005, 167:1451-1459.
18. Saint-Geniez M., et al. VEGF expression and receptor activation in the choroid during development and in the adult. Invest. Ophthalmol. Vis. Sci. 2006, 47:3135-3142.
19. Penn J.S., et al. Vascular endothelial growth factor in eye disease. Prog. Retin. Eye Res. 2008, 27:331-371.
20. Aiello L.P., et al. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:10457-10461.
21. Robinson G.S., et al. Nonvascular role for VEGF: VEGFR-1, 2 activity is critical for neural retinal development. FASEB J. 2001, 15:1215-1217.
22. Jin K., et al. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11946-11950.
23. Zachary I. Neuroprotective role of vascular endothelial growth factor: signalling mechanisms, biological function, and therapeutic potential. Neurosignals 2005, 14:207-221.
24. Kurihara T., et al. Targeted deletion of VEGFA in adult mice induces vision loss. J. Clin. Invest. 2012, 122:4213-4217.
25. Kim I., et al. Constitutive expression of VEGF, VEGFR-1, and VEGFR-2 in normal eyes. Invest. Ophthalmol. Vis. Sci. 1999, 40:2115-2121.
26. Tsutsumi C., et al. The critical role of ocular-infiltrating macrophages in the development of choroidal neovascularization. J. Leukoc. Biol. 2003, 74:25-32.
27. Sapieha P. Eyeing central neurons in vascular growth and reparative angiogenesis. Blood 2012, 120:2182-2194.
28. Vadlapatla R.K., et al. Hypoxia-inducible factor-1 (HIF-1): a potential target for intervention in ocular neovascular diseases. Curr. Drug Targets 2013, 14:919-935.
29. Gragoudas E.S., et al. Pegaptanib for neovascular age-related macular degeneration. N. Engl. J. Med. 2004, 351:2805-2816.
30. Brown D.M., et al. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N. Engl. J. Med. 2006, 355:1432-1444.
31. Rosenfeld P.J., et al. Ranibizumab for neovascular age-related macular degeneration. N. Engl. J. Med. 2006, 355:1419-1431.
32. Brown D.M., et al. Ranibizumab for macular edema following central retinal vein occlusion: six-month primary end point results of a phase III study. Ophthalmology 2010, 117:1124-1133.e1.
33. Campochiaro P.A., et al. Ranibizumab for macular edema following branch retinal vein occlusion: six-month primary end point results of a phase III study. Ophthalmology 2010, 117:1102-1112.e1.
34. Martin D.F., et al. Ranibizumab and bevacizumab for neovascular age-related macular degeneration. The CATT Research Group. N. Engl. J. Med. 2011, 364:1897-1908.
35. Mintz-Hittner H.A., et al. Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity. N. Engl. J. Med. 2011, 364:603-615.
36. Boyer D., et al. Vascular endothelial growth factor trap-eye for macular edema secondary to central retinal vein occlusion: six-month results of the phase 3 COPERNICUS study. Ophthalmology 2012, 119:1024-1032.
37. Heier J.S., et al. Intravitreal aflibercept (VEGF trap-eye) in wet age-related macular degeneration. Ophthalmology 2012, 119:2537-2548.
38. Brown D.M., et al. Long-term outcomes of ranibizumab therapy for diabetic macular edema: the 36-month results from two phase III trials RISE and RIDE. Ophthalmology 2013, 120:2013-2022.
39. Holz F.G., et al. VEGF trap-eye for macular oedema secondary to central retinal vein occlusion: 6-month results of the phase III GALILEO study. Br. J. Ophthalmol. 2013, 97:278-284.
40. Midena E., Invest V.D. Intravitreal aflibercept for the treatment of diabetic macular edema (DME): findings from the VIVID-DME and VISTA-DME clinical trials. Eur. J. Ophthalmol. 2014, 24:459.
41. Rofagha S., et al. Seven-year outcomes in ranibizumab-treated patients in ANCHOR, MARINA, and HORIZON: a multicenter cohort study (SEVEN-UP). Ophthalmology 2013, 120:2292-2299.
42. Pelletier J., et al. VEGF-A promotes both pro-angiogenic and neurotrophic capacities for nerve recovery after compressive neuropathy in rats. Mol. Neurobiol. 2014, Published online May 28, 2014. 10.1007/s12035-014-8754-1.
43. Park H.Y., et al. Neuronal cell death in the inner retina and the influence of vascular endothelial growth factor inhibition in a diabetic rat model. Am. J. Pathol. 2014, 184:1752-1762.
44. Newman A.C., Hughes C.C. Macrophages and angiogenesis: a role for Wnt signaling. Vasc. Cell 2012, 4:13.
45. Frantz S., et al. Innate immunity and angiogenesis. Circ. Res. 2005, 96:15-26.
46. Ricklin D., et al. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 2010, 11:785-797.
47. Parmeggiani F., et al. Mechanism of inflammation in age-related macular degeneration: an up-to-date on genetic landmarks. Mediators Inflamm. 2013, 2013:435607.
48. Langer H.F., et al. Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis. Blood 2010, 116:4395-4403.
49. Sweigard J.H., et al. The alternative complement pathway regulates pathological angiogenesis in the retina. FASEB J. 2014, 28:3171-3182.
50. Stahl A., et al. The mouse retina as an angiogenesis model. Invest. Ophthalmol. Vis. Sci. 2010, 51:2813-2826.
51. Muller-Eberhard H.J. The membrane attack complex of complement. Annu. Rev. Immunol. 1986, 4:503-528.
52. Forneris F., et al. Structures of C3b in complex with factors B and D give insight into complement convertase formation. Science 2010, 330:1816-1820.
53. Apte R.S., et al. Macrophages inhibit neovascularization in a murine model of age-related macular degeneration. PLoS Med. 2006, 3:e310.
54. Checchin D., et al. Potential role of microglia in retinal blood vessel formation. Invest. Ophthalmol. Vis. Sci. 2006, 47:3595-3602.
55. Fantin A., et al. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010, 116:829-840.
56. Kubota Y., et al. M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J. Exp. Med. 2009, 206:1089-1102.
57. Lobov I.B., et al. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 2005, 437:417-421.
58. Outtz H.H., et al. Notch1 controls macrophage recruitment and Notch signaling is activated at sites of endothelial cell anastomosis during retinal angiogenesis in mice. Blood 2011, 118:3436-3439.
59. Mosser D.M. The many faces of macrophage activation. J. Leukoc. Biol. 2003, 73:209-212.
60. Mantovani A., et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004, 25:677-686.
61. Sica A., Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 2012, 122:787-795.
62. Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000prime Rep. 2014, 6:13.
63. Murray P.J., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014, 41:14-20.
64. Kelly J., et al. Senescence regulates macrophage activation and angiogenic fate at sites of tissue injury in mice. J. Clin. Invest. 2007, 117:3421-3426.
65. Cherepanoff S., et al. Bruch's membrane and choroidal macrophages in early and advanced age-related macular degeneration. Br. J. Ophthalmol. 2010, 94:918-925.
66. Cao X., et al. Macrophage polarization in the maculae of age-related macular degeneration: a pilot study. Pathol. Int. 2011, 61:528-535.
67. Roychoudhury J., et al. Targeting immune privilege to prevent pathogenic neovascularization. Invest. Ophthalmol. Vis. Sci. 2010, 51:3560-3566.
68. Sene A., et al. Impaired cholesterol efflux in senescent macrophages promotes age-related macular degeneration. Cell Metab. 2013, 17:549-561.
69. Raimondi C., et al. Imatinib inhibits VEGF-independent angiogenesis by targeting neuropilin 1-dependent ABL1 activation in endothelial cells. J. Exp. Med. 2014, 211:1167-1183.
70. Rivera J.C., et al. Microglia and interleukin-1β in ischemic retinopathy elicit microvascular degeneration through neuronal semaphorin-3A. Arterioscler. Thromb. Vasc. Biol. 2013, 33:1881-1891.
71. Takahashi H., et al. Interleukin-17 enhances bFGF-, HGF- and VEGF-induced growth of vascular endothelial cells. Immunol. Lett. 2005, 98:189-193.
72. Morohoshi K., et al. Serum autoantibody biomarkers for age-related macular degeneration and possible regulators of neovascularization. Exp. Mol. Pathol. 2012, 92:64-73.
73. Hasegawa E., et al. IL-23-independent induction of IL-17 from γδT cells and innate lymphoid cells promotes experimental intraocular neovascularization. J. Immunol. 2013, 190:1778-1787.
74. Camelo S. Potential sources and roles of adaptive immunity in age-related macular degeneration: shall we rename AMD into autoimmune macular disease?. Autoimmune Dis. 2014, 2014:532487.
75. Liu B., et al. Complement component C5a promotes expression of IL-22 and IL-17 from human T cells and its implication in age-related macular degeneration. J. Transl. Med. 2011, 9:1-12.
76. Cruz-Guilloty F., et al. T cells and macrophages responding to oxidative damage cooperate in pathogenesis of a mouse model of age-related macular degeneration. PLoS ONE 2014, 9:e88201.
77. Nussenblatt R.B., et al. Immune responses in age-related macular degeneration and a possible long-term therapeutic strategy for prevention. Am. J. Ophthalmol. 2014, 158:5-11.e2.
78. Chen Z., O'Shea J.J. Regulation of IL-17 production in human lymphocytes. Cytokine 2008, 41:71-78.
79. Gaffen S.L. Recent advances in the IL-17 cytokine family. Curr. Opin. Immunol. 2011, 23:613-619.
80. Wei L., et al. Hypomethylation of the IL17RC promoter associates with age-related macular degeneration. Cell Rep. 2012, 2:1151-1158.
81. Oliver V.F., et al. Hypomethylation of the IL17RC promoter in peripheral blood leukocytes is not a hallmark of age-related macular degeneration. Cell Rep. 2013, 5:1527-1535.
82. Handa J.T. How does the macula protect itself from oxidative stress?. Mol. Aspects Med. 2012, 33:418-435.
83. Gu X., et al. Carboxyethylpyrrole protein adducts and autoantibodies, biomarkers for age-related macular degeneration. J. Biol. Chem. 2003, 278:42027-42035.
84. Hollyfield J.G., et al. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat. Med. 2008, 14:194-198.
85. Hollyfield J.G., et al. A hapten generated from an oxidation fragment of docosahexaenoic acid is sufficient to initiate age-related macular degeneration. Mol. Neurobiol. 2010, 41:290-298.
86. Cruz-Guilloty F., et al. Infiltration of proinflammatory M1 macrophages into the outer retina precedes damage in a mouse model of age-related macular degeneration. Int. J. Inflamm. 2013, 2013:503725.
87. Crabb J.W., et al. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14682-14687.
88. Gu J., et al. Proteomic and genomic biomarkers for age-related macular degeneration. Adv. Exp. Med. Biol. 2010, 664:411-417.
89. Danis R., et al. Pazopanib eye drops: a randomised trial in neovascular age-related macular degeneration. Br. J. Ophthalmol. 2014, 98:172-178.
90. Xue Q., et al. Palomid 529, a novel small-molecule drug, is a TORC1/TORC2 inhibitor that reduces tumor growth, tumor angiogenesis, and vascular permeability. Cancer Res. 2008, 68:9551-9557.
91. Ciulla T.A., et al. Squalamine lactate reduces choroidal neovascularization in a laser-injury model in the rat. Retina 2003, 23:808-814.
92. Smith A.C., et al. Safety of Ad(GV)PEDF.11D administered by subtenon injection following laser disruption of the Bruch's membrane in cynomolgus monkey eyes. Invest. Ophthalmol. Vis. Sci. 2003, 44. E-Abstract 453.
93. Russell S.R., et al. Anecortave acetate for the treatment of exudative age-related macular degeneration - a review of clinical outcomes. Surv. Ophthalmol. 2007, 52:S79-S90.
94. Kaiser P.K. Emerging therapies for neovascular age-related macular degeneration: drugs in the pipeline. Ophthalmology 2013, 120:S11-S15.
95. Dalal M., et al. Subconjunctival palomid 529 in the treatment of neovascular age-related macular degeneration. Graefes Arch. Clin. Exp. Ophthalmol. 2013, 251:2705-2709.
96. Doukas J., et al. Topical administration of a multi-targeted kinase inhibitor suppresses choroidal neovascularization and retinal edema. J. Cell. Physiol. 2008, 216:29-37.
97. Aiello L.P. Angiogenic pathways in diabetic retinopathy. N. Engl. J. Med. 2005, 353:839-841.
98. Connor K.M., et al. Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat. Protoc. 2009, 4:1565-1573.
99. Lambert V., et al. Laser-induced choroidal neovascularization model to study age-related macular degeneration in mice. Nat. Protoc. 2013, 8:2197-2211.