Neuronal-driven angiogenesis: Role of NGF in retinal neovascularization in an oxygen-induced retinopathy model

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 7, 2010, Pages 3749-3757

  Liu, Xialin ^a   Wang, Dingding ^a   Liu, Yizhi ^a   Luo, Yan ^a   Ma, Wei ^a   Xiao, Wei ^a   Yu, Qiang ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

K 252A; MESSENGER RNA; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR ANTIBODY; OXYGEN; VASCULOTROPIN; CARBAZOLE DERIVATIVE; ENZYME INHIBITOR; INDOLE ALKALOID; K 252; PROTEIN TYROSINE KINASE A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL NUCLEUS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HISTOPATHOLOGY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RETINA NEOVASCULARIZATION; RETINOPATHY; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; NEWBORN; PATHOLOGY; PHYSIOLOGY; RETINA BLOOD VESSEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANIMALS, NEWBORN; CARBAZOLES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; INDOLE ALKALOIDS; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; OXYGEN; RECEPTOR, TRKA; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 77955867263     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4226     Document Type: Article

References (81)

1. Simo R, Carrasco E, Garcia-Ramirez M, Hernandez C. Angiogenic and antiangiogenic factors in proliferative diabetic retinopathy. Curr Diabetes Rev. 2006;2:71-98.
2. Colombo ES, Menicucci G, McGuire PG, Das A. Hepatocyte growth factor/scatter factor promotes retinal angiogenesis through increased urokinase expression. Invest Ophthalmol Vis Sci. 2007; 48:1793-1800.
3. Watanabe D, Suzuma K, Matsui S, et al. Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med. 2005;353:782-792.
4. Butler JM, Guthrie SM, Koc M, et al. SDF-1 is both necessary and sufficient to promote proliferative retinopathy. J Clin Invest. 2005; 115:86-93.
5. Beauchamp MH, Marrache AM, Hou X, et al. Platelet-activating factor in vasoobliteration of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2002;43:3327-3337.
6. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331:1480-1487.
7. Keck PJ, Hauser SD, Krivi G, et al. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science. 1989;246:1309-1312.
8. Feit-Leichman RA, Kinouchi R, Takeda M, et al. Vascular damage in a mouse model of diabetic retinopathy: relation to neuronal and glial changes. Invest Ophthalmol Vis Sci. 2005;46:4281-4287.
9. Duda DG, Jain RK. Pleiotropy of tissue-specific growth factors: from neurons to vessels via the bone marrow. J Clin Invest. 2005;115:596-598.
10. West H, Richardson WD, Fruttiger M. Stabilization of the retinal vascular network by reciprocal feedback between blood vessels and astrocytes. Development. 2005;132:1855-1862.
11. Eichmann A, Makinen T, Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev. 2005;19:1013-1021.
12. Vogel G. Developmental biology: the unexpected brains behind blood vessel growth. Science. 2005;307:665-667.
13. Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature. 2005;436:193-200.
14. Suchting S, Bicknell R, Eichmann A. Neuronal clues to vascular guidance. Exp Cell Res. 2006;312:668-675
15. Ijichi A, Sakuma S, Tofilon PJ. Hypoxia-induced vascular endothelial growth factor expression in normal rat astrocyte cultures. Glia. 1995;14:87-93.
16. Eichler W, Yafai Y, Kuhrt H, et al. Hypoxia: modulation of endothelial cell proliferation by soluble factors released by retinal cells. Neuroreport. 2001;12:4103-4108.
17. Eichler W, Kuhrt H, Hoffmann S, Wiedemann P, Reichenbach A. VEGF release by retinal glia depends on both oxygen and glucose supply. Neuroreport. 2000;11:3533-3537.
18. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003; 161:1163-1177.
19. Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell. 2002;109:693-705.
20. Aloe L, Simone MD, Properzi F. Nerve growth factor: a neurotro-phin with activity on cells of the immune system. Microsc Res Tech. 1999;45:285-291
21. Lambiase A, Rama P, Bonini S, Caprioglio G, Aloe L. Topical treatment with nerve growth factor for corneal neurotrophic ulcers. N Engl J Med. 1998;338:1174-1180.
22. Bernabei R, Landi F, Bonini S, et al. Effect of topical application of nerve-growth factor on pressure ulcers. Lancet. 1999;354:307.
23. Ransohoff RM, Trebst C. Surprising pleiotropy of nerve growth factor in the treatment of experimental autoimmune encephalomyelitis. J Exp Med. 2000;191:1625-1630.
24. Donovan MJ, Lin MI, Wiegn P, et al. Brain derived neurotrophic factor is an endothelial cell survival factor required for intramyo-cardial vessel stabilization. Development. 2000;127:4531-4540.
25. Calza L, Giardino L, Giuliani A, Aloe L, Levi-Montalcini R. Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. ProcNatlAcadSci USA. 2001;98:4160-4165.
26. Turrini P, Gaetano C, Antonelli A, Capogrossi MC, Aloe L. Nerve growth factor induces angiogenic activity in a mouse model of hindlimb ischemia. NeurosciLett. 2002;323:109-112.
27. Cantarella G, Lempereur L, Presta M, et al. Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J. 2002;16:1307-1309
28. Emanueli C, Salis MB, Pinna A, et al. Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation. 2002;106:2257-2262.
29. Emanueli C, Bonaria Salis M, Stacca T, et al. Targeting kinin B(1) receptor for therapeutic neovascularization. Circulation. 2002; 105:360-366.
30. Wilson BD, Ii M, Park KW, et al. Netrins promote developmental and therapeutic angiogenesis. Science. 2006;313:640-644.
31. Kermani P, Rafii D, Jin DK, et al. Neurotrophins promote revascularization by local recruitment of TrkB+ endothelial cells and systemic mobilization of hematopoietic progenitors. J Clin Invest. 2005;115:653-663.
32. Yano H, Chao MV. Neurotrophin receptor structure and interactions. Pharm Acta Helv. 2000;74:253-260.
33. Raychaudhuri SP, Sanyal M, Weltman H, Kundu-Raychaudhuri S. K252a, a high-affinity nerve growth factor receptor blocker, improves psoriasis: an in vivo study using the severe combined immuno deficient mouse-human skin model. J Invest Dermatol. 2004;122:812-819.
34. Hansen-Algenstaedt N, Algenstaedt P, Schaefer C, et al. Neural driven angiogenesis by overexpression of nerve growth factor. Histochem Cell Biol. 2006;125:637-649.
35. Berg MM, Sternberg DW, Parada LF, Chao MV. K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phos-phorylation and kinase activity. J Biol Chem. 1992;267:13-16.
36. Koizumi S, Contreras ML, Matsuda Y, et al. K-252a: a specific inhibitor of the action of nerve growth factor on PC 12 cells. J Neurosci. 1988;8:715-721.
37. Smith LE, Wesolowski E, McLellan A, et al. Oxygen-induced reti-nopathy in the mouse. Invest Ophthalmol Vis Sci. 1994;35:101- 111.
38. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A. 1995;92:905-909.
39. Aiello LP, Pierce EA, Foley ED, et al. Suppression of retinal neo-vascularization 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.
40. Unsoeld AS, Junker B, Mazitschek R, et al. Local injection of receptor tyrosine kinase inhibitor MAE 87 reduces retinal neovas-cularization in mice. Mol Vis. 2004;10:468-475.
41. Mashayekhi F. Neural cell death is induced by neutralizing antibody to nerve growth factor: an in vivo study, Brain Dev. 2008; 30:112-117.
42. Siliprandi R, Canella R, Carmignoto G. Nerve growth factor promotes functional recovery of retinal ganglion cells after ischemia. Invest Ophthalmol Vis Sci. 1993;34:3232-3245.
43. Carmignoto G, Maffei L, Candeo P, Canella R, Comelli C. Effect of NGF on the survival of rat retinal ganglion cells following optic nerve section. J Neurosci. 1989;9:1263-1272.
44. Yoo MH, Hyun HJ, Koh JY, Yoon YH. Riluzole inhibits VEGF-induced endothelial cell proliferation in vitro and hyperoxia-in-duced abnormal vessel formation in vivo. Invest Ophthalmol Vis Sci. 2005;46:4780-4787.
45. Chikaraishi Y, Shimazawa M, Hara H. New quantitative analysis, using high-resolution images, of oxygen-induced retinal neovascu-larization in mice. Exp Eye Res. 2007;84:529-536.
46. Barros LF, Belfort R. The effects of the subconjunctival injection of bevacizumab (Avastin) on angiogenesis in the rat cornea. An Acad Bras Cienc. 2007;79:389-394.
47. Ritter MR, Banin E, Moreno SK, et al. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest. 2006;116:3266-3276.
48. Banin E, Dorrell MI, Aguilar E, et al. T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification. Invest Ophthalmol Vis Sci. 2006;47:2125-2134.
49. Park MJ, Kwak HJ, Lee HC, et al. Nerve growth factor induces endothelial cell invasion and cord formation by promoting matrix metalloproteinase-2 expression through the phosphatidylinositol 3-kinase/Akt signaling pathway and AP-2 transcription factor. J Biol Chem. 2007;282:30485-30496.
50. Dorrell M, Uusitalo-Jarvinen H, Aguilar E, Friedlander M. Ocular neovascularization: basic mechanisms and therapeutic advances. Surv Ophthalmol. 2007;52(suppl 1):S3-S19.
51. Aiello LP, Northrup JM, Keyt BA, Takagi H, Iwamoto MA. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol. 1995;113:1538-1544.
52. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev. 1997;18:4-25.
53. Kuroki M, Voest EE, Amano S, et al. Reactive oxygen intermediates increase vascular endothelial growth factor expression in vitro and in vivo. J Clin Invest. 1996;98:1667-1675
54. Ozaki H, Yu AY, Della N, et al. Hypoxia inducible factor-1a is increased in ischemic retina: temporal and spatial correlation with VEGF expression. Invest Ophthalmol Vis Sci. 1999;40:182-189.
55. Marti HH. Angiogenesis-a self-adapting principle in hypoxia. EXS. 2005;163-180.
56. Freyberger H, Brocker M, Yakut H, et al. Increased levels of platelet-derived growth factor in vitreous fluid of patients with proliferative diabetic retinopathy. Exp Clin Endocrinol Diabetes. 2000;108: 106 -109
57. Sivilia S, Giuliani A, Fernandez M, et al. Intravitreal NGF administration counteracts retina degeneration after permanent carotid artery occlusion in rat. BMC Neurosci. 2009;10:52.
58. Ali TK, Matragoon S, Pillai BA, Liou GI, El-Remessy AB. Peroxyni-trite mediates retinal neurodegeneration by inhibiting nerve growth factor survival signaling in experimental and human diabetes. Diabetes. 2008;57:889-898.
59. Lambiase A, Tirassa P, Micera A, Aloe L, Bonini S. Pharmacokinetics of conjunctivally applied nerve growth factor in the retina and optic nerve of adult rats. Invest Ophthalmol Vis Sci. 2005;46: 3800-3806.
60. Sun X, Xu X, Wang F, et al. Nerve growth factor helps protect retina in experimental retinal detachment. Ophthalmologica. 2008;222:58-61.
61. Lambiase A, Aloe L, Centofanti M, et al. Experimental and clinical evidence of neuroprotection by nerve growth factor eye drops: implications for glaucoma. Proc Natl Acad Sci USA. 2009;106: 13469-13474.
62. Samii A, Unger J, Lange W. Vascular endothelial growth factor expression in peripheral nerves and dorsal root ganglia in diabetic neuropathy in rats. Neurosci Lett. 1999;262:159-162.
63. Manni L, Antonelli A, Costa N, Aloe L. Stress alters vascular-endothelial growth factor expression in rat arteries: role of nerve growth factor. Basic Res Cardiol. 2005;100:121-130.
64. Raychaudhuri SK, Raychaudhuri SP, Weltman H, Farber EM. Effect of nerve growth factor on endothelial cell biology: proliferation and adherence molecule expression on human dermal microvascular endothelial cells. Arch Dermatol Res. 2001;293:291-295
65. Colafrancesco V, Cirulli F, Rossi S, Berry A, Aloe L. Anti-NGF-antibody administration as collyrium reduces the presence of NGF and enhances the expression of VEGF in the retina, lacrimal gland and hippocampus. Neurosci Lett. 2009;463:203-206.
66. Saint-Geniez M, Maharaj AS, Walshe TE, et al. Endogenous VEGF is required for visual function: evidence for a survival role on Muller cells and photoreceptors. PLoS One. 2008;3:e3554.
67. Sondell M, Lundborg G, Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal out growth,enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci. 1999;19:5731-5740.
68. Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D. Nerve growth factor as an angiogenic factor. Microvasc Res. 2008;75: 135-141.
69. Nishijima K, Ng YS, Zhong L, et al. Vascular endothelial growth factor-A is a survival factor for retinal neurons and a critical neu-roprotectant during the adaptive response to ischemic injury. Am J Pathol. 2007;171:53-67.
70. Park KS, Kim SS, Kim JC, et al. Serum and tear levels of nerve growth factor in diabetic retinopathy patients. Am J Ophthalmol. 2008;145:432-437.
71. Folkman J, D'Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87:1153-1155.
72. Vasa M, Fichtlscherer S, Aicher A, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001; 89:E1-E7.
73. Waltenberger J. Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications. Cardiovasc Res. 2001;49:554-560.
74. Fadini GP, Sartore S, Baesso I, et al. Endothelial progenitor cells and the diabetic paradox. Diabetes Care. 2006;29:714-716.
75. Dorrell MI, Aguilar E, Jacobson R, et al. Antioxidant or neurotro-phic factor treatment preserves function in a mouse model of neovascularization-associated oxidative stress. J Clin Invest. 2009; 119:611-623.
76. Komeima K, Rogers BS, Lu L, Campochiaro PA. Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proc Natl Acad Sci USA. 2006;103:11300-11305.
77. Cordon-Cardo C, Tapley P, Jing SQ, et al. The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell. 1991;66:173-183.
78. Allsopp TE, Robinson M, Wyatt S, Davies AM. Ectopic trkA expression mediates a NGF survival response in NGF-independent sensory neurons but not in parasympathetic neurons. J Cell Biol. 1993;123:1555-1566.
79. Majdan M, Walsh GS, Aloyz R, Miller FD. TrkA mediates developmental sympathetic neuron survival in vivo by silencing an ongoing p75NTR-mediated death signal. J Cell Biol. 2001;155:1275-1285.
80. Seo MS, Kwak N, Ozaki H, et al. Dramatic inhibition of retinal and choroidal neovascularization by oral administration of a kinase inhibitor. Am J Pathol. 1999;154:1743-1753.
81. Maier P, Unsoeld AS, Junker B, et al. Intravitreal injection of specific receptor tyrosine kinase inhibitor PTK787/ZK222 584 improves ischemia-induced retinopathy in mice. Graefes Arch Clin Exp Ophthalmol. 2005;243:593-600.