Nerve growth factor in diabetic retinopathy: Beyond neurons

Expert Review of Ophthalmology

Volumn 9, Issue 2, 2014, Pages 99-107

  Mysona, Barbara A ^a,b,c   Shanab, Ahmed Y ^a,b,c   Elshaer, Sally L ^a,b,c   El Remessy, Azza B ^a,b,c  

^a UNIVERSITY OF GEORGIA   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Acellular capillary; Angiogenesis; Diabetic macular edema; Diabetic retinopathy; Inflammation; Neurodegeneration; Neurotrophins

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; NEUROTROPHIN RECEPTOR; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE KINASE;

ASTROCYTE; BLOOD VESSEL PERMEABILITY; DIABETIC RETINOPATHY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; RETINA NEOVASCULARIZATION; RETINITIS; REVIEW;

EID: 84896926680     PISSN: 17469899     EISSN: 17469902     Source Type: Journal    
DOI: 10.1586/17469899.2014.903157     Document Type: Review

References (109)

1. Centers for Disease Control and Prevention: Blindness caused by diabetes: Massachusetts, 1987-1994. 1996;45:937-41
2. Bloodworth JM Jr. Diabetic retinopathy. Diabetes 1962;11:1-22
3. The effect of intensive treatment of diabetes on the development and progression of long-Term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993; 329(14):977-86
4. The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the diabetes control and complications trial. Diabetes 1995;44(8):968-83
5. Lieth E, Gardner TW, Barber AJ, Antonetti DA. Retinal neurodegeneration: Early pathology in diabetes. Clin Experiment Ophthalmol 2000;28(1):3-8
6. Barber AJ, Lieth E, Khin SA, et al. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 1998;102(4):783-91
7. Martin PM, Roon P, Van Ells TK, et al. Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci 2004;45(9):3330-6
8. Lieth E, Barber AJ, Xu B, et al. Glial reactivity and impaired glutamate metabolism in short-Term experimental diabetic retinopathy. Penn State Retina Research Group. Diabetes 1998;47(5):815-20
9. Mizutani M, Gerhardinger C, Lorenzi M. Muller cell changes in human diabetic retinopathy. Diabetes 1998;47(3):445-9
10. Huang H, Gandhi JK, Zhong X, et al. TNFalpha is required for late BRB breakdown in diabetic retinopathy, and its inhibition prevents leukostasis and protects vessels and neurons from apoptosis. Invest Ophthalmol Vis Sci 2011;52(3):1336-44
11. Stem MS, Gardner TW. Neurodegeneration in the pathogenesis of diabetic retinopathy: Molecular mechanisms and therapeutic implications. Curr Med Chem 2013;20(26): 3241-50
12. Simo R, Hernandez C. Neurodegeneration in the diabetic eye: New insights and therapeutic perspectives. Trends Endocrinol Metab 2014;25(1):23-33
13. Abiko T, Abiko A, Clermont AC, et al. Characterization of retinal leukostasis and hemodynamics in insulin resistance and diabetes: Role of oxidants and protein kinase-C activation. Diabetes 2003;52(3): 829-37
14. Hammes HP, Lin J, Wagner P, et al. Angiopoietin-2 causes pericyte dropout in the normal retina: Evidence for involvement in diabetic retinopathy. Diabetes 2004; 53(4):1104-10
15. Hammes HP, Feng Y, Pfister F, Brownlee M. Diabetic retinopathy: Targeting vasoregression. Diabetes 2011;60(1):9-16
16. Miyamoto K, Ogura Y. Pathogenetic potential of leukocytes in diabetic retinopathy. Semin Ophthalmol 1999;14(4): 233-9
17. Cunha-Vaz J, Bernardes R. Nonproliferative retinopathy in diabetes type 2. Initial stages and characterization of phenotypes. Prog Retin Eye Res 2005;24(3):355-77
18. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. Faseb J 2004;18(12):1450-2
19. Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. XV. The long-Term incidence of macular edema. Ophthalmology 1995; 102(1):7-16
20. Ferris FL. 3rd, Patz A. Macular edema. A complication of diabetic retinopathy. Surv Ophthalmol 1984;28(Suppl):452-61
21. 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(22):1480-7
22. Miller JW, Adamis AP, Aiello LP. Vascular endothelial growth factor in ocular neovascularization and proliferative diabetic retinopathy. Diabetes Metab Rev 1997; 13(1):37-50
23. Kern TS, Engerman RL. Vascular lesions in diabetes are distributed non-uniformly within the retina. Exp Eye Res 1995;60(5): 545-9
24. Arevalo JF, Sanchez JG, Lasave AF, et al. Intravitreal Bevacizumab (Avastin((R))) for Diabetic Retinopathy at 24-months: The 2008 Juan Verdaguer-Planas Lecture. Curr Diabetes Rev 2010;6(5):313-22
25. Yam JC, Kwok AK. Update on the treatment of diabetic retinopathy. Hong Kong Med J 2007;13(1):46-60
26. Von Bartheld CS. Neurotrophins in the developing and regenerating visual system. Histol Histopathol 1998;13(2):437-59
27. Skaper SD. The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol Disord Drug Targets 2008;7(1):46-62
28. Abu El-Asrar AM, Mohammad G, De Hertogh G, et al. Neurotrophins and neurotrophin receptors in proliferative diabetic retinopathy. PLoS One 2013;8:6
29. Hammes HP, Federoff HJ, Brownlee M. Nerve growth factor prevents both neuroretinal programmed cell death and capillary pathology in experimental diabetes. Mol Med 1995;1(5):527-34
30. Ali TK, Matragoon S, Pillai BA, et al. Peroxynitrite mediates retinal neurodegeneration by inhibiting NGF survival signal in experimental and human diabetes. Diabetes 2008;57(4):889-98
31. Ali TK, Al-Gayyar MM, Matragoon S, et al. Diabetes-induced peroxynitrite impairs the balance of pro-nerve growth factor and nerve growth factor, and causes neurovascular injury. Diabetologia 2011; 54(3):657-68
32. Al-Gayyar MM, Matragoon S, Pillai BA, et al. Epicatechin blocks pro-nerve growth factor (proNGF)-mediated retinal neurodegeneration via inhibition of p75 neurotrophin receptor expression in a rat model of diabetes [corrected]. Diabetologia 2011;54(3):669-80
33. Mysona BA, Al-Gayyar MM, Matragoon S, et al. Modulation of p75(NTR) prevents diabetes-And proNGF-induced retinal inflammation and blood-retina barrier breakdown in mice and rats. Diabetologia 2013;56(10):2329-39
34. Al-Gayyar MM, Abdelsaid MA, Matragoon S, et al. Diabetes and overexpression of proNGF cause retinal neurodegeneration via activation of RhoA. PLoS One 2013;8(1):e54692
35. Colafrancesco V, Coassin M, Rossi S, Aloe L. Effect of eye NGF administration on two animal models of retinal ganglion cells degeneration. Ann Ist Super Sanita 2011;47(3):284-9
36. Mantelli F, Lambiase A, Colafrancesco V, et al. NGF and VEGF effects on retinal ganglion cell fate: New evidence from an animal model of diabetes. Eur J Ophthalmol 2014;24(2):247-53
37. Bruno MA, Cuello AC. Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci USA 2006;103(17): 6735-40
38. Bothwell M. Functional interactions of neurotrophins and neurotrophin receptors. Annu Rev Neurosci 1995;18:223-53
39. Hermey G. The Vps10p-domain receptor family. Cell Mol Life Sci 2009;66(16): 2677-89
40. Teng KK, Felice S, Kim T, Hempstead BL. Understanding proneurotrophin actions: Recent advances and challenges. Dev Neurobiol 2010;70(5):350-9
41. Schor NF. The p75 neurotrophin receptor in human development and disease. Prog Neurobiol 2005;77(3):201-14
42. Fortini ME. Gamma-secretase-mediated proteolysis in cell-surface-receptor signalling. Nat Rev Mol Cell Biol 2002;3(9):673-84
43. Frade JM. Nuclear translocation of the p75 neurotrophin receptor cytoplasmic domain in response to neurotrophin binding. J Neurosci 2005;25(6):1407-11
44. Kanning KC, Hudson M, Amieux PS, et al. Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-Terminal fragments with signaling capability. J Neurosci 2003; 23(13):5425-36
45. Zampieri N, Xu CF, Neubert TA, Chao MV. Cleavage of p75 neurotrophin receptor by alpha-secretase and gamma-secretase requires specific receptor domains. J Biol Chem 2005;280(15): 14563-71
46. Kenchappa RS, Zampieri N, Chao MV, et al. Ligand-dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 2006;50(2): 219-32
47. Parkhurst CN, Zampieri N, Chao MV. Nuclear localization of the p75 neurotrophin receptor intracellular domain. J Biol Chem 2010;285(8):5361-8
48. Khursigara G, Orlinick JR, Chao MV. Association of the p75 neurotrophin receptor with TRAF6. J Biol Chem 1999; 274(5):2597-600
49. Reichardt LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006;361(1473):1545-64
50. Azar ST, Major SC, Safieh-Garabedian B. Altered plasma levels of nerve growth factor and transforming growth factor-beta2 in type-1 diabetes mellitus. Brain Behav Immun 1999;13(4):361-6
51. 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(3):432-7
52. Lee R, Kermani P, Teng KK, Hempstead BL. Regulation of cell survival by secreted proneurotrophins. Science 2001; 294(5548):1945-8
53. Marsh HN, Dubreuil CI, Quevedo C, et al. SHP-1 negatively regulates neuronal survival by functioning as a TrkA phosphatase. J Cell Biol 2003;163(5):999-1010
54. Al-Gayyar MM, Mysona BA, Matragoon S, et al. Diabetes and overexpression of proNGF cause retinal neurodegeneration via activation of RhoA pathway. PLoS One 2013;8(1):e54692
55. Yune TY, Lee JY, Jung GY, et al. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J Neurosci 2007;27(29): 7751-61
56. Semenova MM, Maki-Hokkonen AM, Cao J, et al. Rho mediates calcium-dependent activation of p38alpha and subsequent excitotoxic cell death. Nat Neurosci 2007;10(4):436-43
57. Dubreuil CI, Winton MJ, Mckerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J Cell Biol 2003;162(2):233-43
58. Nwariaku FE, Rothenbach P, Liu Z, et al. Rho inhibition decreases TNF-induced endothelial MAPK activation and monolayer permeability. J Appl Physiol 2003;95(5):1889-95
59. Nwariaku FE, Chang J, Zhu X, et al. The role of p38 map kinase in tumor necrosis factor-induced redistribution of vascular endothelial cadherin and increased endothelial permeability. Shock 2002;18(1): 82-5
60. Matragoon S, Al-Gayyar MM, Mysona BA, et al. Electroporation-mediated gene delivery of cleavage-resistant pro-nerve growth factor causes retinal neuro-And vascular degeneration. Mol Vis 2012;18:2993-3003
61. Kern TS. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007;2007:95103
62. Tang J, Kern TS. Inflammation in diabetic retinopathy. Prog Retin Eye Res 2011; 30(5):343-58
63. Gardner TW, Antonetti DA, Barber AJ, et al. Diabetic retinopathy: More than meets the eye. Surv Ophthalmol 2002; 47(Suppl 2):S253-62
64. Lee KF, Li E, Huber LJ, et al. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 1992;69(5):737-49
65. Carter BD, Kaltschmidt C, Kaltschmidt B, et al. Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science 1996; 272(5261):542-5
66. Bhakar AL, Roux PP, Lachance C, et al. The p75 neurotrophin receptor (p75NTR) alters tumor necrosis factor-mediated NFkappaB activity under physiological conditions, but direct p75NTR-mediated NF-kappaB activation requires cell stress. J Biol Chem 1999;274(30):21443-9
67. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV. Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 1996;383(6602): 716-19
68. Bhakar AL, Howell JL, Paul CE, et al. Apoptosis induced by p75NTR overexpression requires Jun kinase-dependent phosphorylation of Bad. J Neurosci 2003;23(36):11373-81
69. Hu B, Yip HK, So KF. Localization of p75 neurotrophin receptor in the retina of the adult SD rat: An immunocytochemical study at light and electron microscopic levels. Glia 1998;24(2):187-97
70. Harada C, Harada T, Nakamura K, et al. Effect of p75NTR on the regulation of naturally occurring cell death and retinal ganglion cell number in the mouse eye. Dev Biol 2006;290(1):57-65
71. Garcia M, Forster V, Hicks D, Vecino E. In vivo expression of neurotrophins and neurotrophin receptors is conserved in adult porcine retina in vitro. Invest Ophthalmol Vis Sci 2003;44(10):4532-41
72. Lebrun-Julien F, Bertrand MJ, De Backer O, et al. ProNGF induces TNFalpha-dependent death of retinal ganglion cells through a p75NTR non-cell-Autonomous signaling pathway. Proc Natl Acad Sci USA 2010;107(8): 3817-22
73. Bai Y, Dergham P, Nedev H, et al. Chronic and acute models of retinal neurodegeneration TrkA activity are neuroprotective whereas p75NTR activity is neurotoxic through a paracrine mechanism. J Biol Chem 2010;285(50):39392-400
74. Kim H, Li Q, Hempstead BL, Madri JA. Paracrine and autocrine functions of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in brain-derived endothelial cells. J Biol Chem 2004;279(32):33538-46
75. Siao CJ, Lorentz CU, Kermani P, et al. ProNGF, a cytokine induced after myocardial infarction in humans, targets pericytes to promote microvascular damage and activation. J Exp Med 2012;209(12): 2291-305
76. Aveleira CA, Lin CM, Abcouwer SF, et al. TNF-Alpha signals through PKCzeta/NFkappaB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes 2010;59(11):2872-82
77. Busik JV, Mohr S, Grant MB. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes 2008;57(7):1952-65
78. Zhang Q, Jiang Y, Miller MJ, et al. IGFBP-3 and TNF-Alpha regulate retinal endothelial cell apoptosis. Invest Ophthalmol Vis Sci 2013;54(8):5376-84
79. Joussen AM, Doehmen S, Le ML, et al. TNF-Alpha mediated apoptosis plays an important role in the development of early diabetic retinopathy and long-Term histopathological alterations. Mol Vis 2009;15:1418-28
80. Saishin Y, Takahashi K, Melia M, et al. Inhibition of protein kinase C decreases prostaglandin-induced breakdown of the blood-retinal barrier. J Cell Physiol 2003; 195(2):210-19
81. Witmer AN, Vrensen GFJM, Van Noorden CJF, Schlingemann RO. Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res 2003;22(1):1-29
82. Salis MB, Graiani G, Desortes E, et al. Nerve growth factor supplementation reverses the impairment, induced by Type 1 diabetes, of hindlimb post-ischaemic recovery in mice. Diabetologia 2004;47(6): 1055-63
83. Hansen-Algenstaedt N, Algenstaedt P, Schaefer C, et al. Neural driven angiogenesis by overexpression of nerve growth factor. Histochem Cell Biol 2006;125(6):637-49
84. Graiani G, Emanueli C, Desortes E, et al. Nerve growth factor promotes reparative angiogenesis and inhibits endothelial apoptosis in cutaneous wounds of Type 1 diabetic mice. Diabetologia 2004; 47(6):1047-54
85. Jee D, Lee WK. Inhibitory effect of intravitreal injection of bevacizumab on nerve growth factor. Curr Eye Res 2012; 37(5):408-15
86. Colafrancesco V, Cirulli F, Rossi S, et al. 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(3):203-6
87. Spranger J, Pfeiffer AF. New concepts in pathogenesis and treatment of diabetic retinopathy. Exp Clin Endocrinol Diabetes 2001;109(Suppl 2):S438-50
88. Liu X, Wang D, Liu Y, et al. Neuronal-driven angiogenesis: Role of NGF in retinal neovascularization in an oxygen-induced retinopathy model. Invest Ophthalmol Vis Sci 2010;51(7):3749-57
89. Jadhao CS, Bhatwadekar AD, Jiang Y, et al. Nerve growth factor promotes endothelial progenitor cell-mediated angiogenic responses. Invest Ophthalmol Vis Sci 2012; 53(4):2030-7
90. Cristofaro B, Stone OA, Caporali A, et al. Neurotrophin-3 is a novel angiogenic factor capable of therapeutic neovascularization in a mouse model of limb ischemia. Arterioscler Thromb Vasc Biol 2010;30(6): 1143-50
91. Nakamura K, Tan F, Li Z, Thiele CJ. NGF activation of TrkA induces vascular endothelial growth factor expression via induction of hypoxia-inducible factor-1alpha. Mol Cell Neurosci 2011; 46(2):498-506
92. Kim YS, Jo DH, Lee H, et al. Nerve growth factor-mediated vascular endothelial growth factor expression of astrocyte in retinal vascular development. Biochem Biophys Res Commun 2013;431(4):740-5
93. Elshaer SL, Abdelsaid MA, Al-Azayzih A, et al. Pronerve growth factor induces angiogenesis via activation of TrkA: Possible role in proliferative diabetic retinopathy. J Diabetes Res 2013;2013:432659
94. Landi S, Sale A, Berardi N, et al. Retinal functional development is sensitive to environmental enrichment: A role for BDNF. FASEB J 2007;21(1):130-9
95. Seki M, Tanaka T, Nawa H, et al. Involvement of brain-derived neurotrophic factor in early retinal neuropathy of streptozotocin-induced diabetes in rats: Therapeutic potential of brain-derived neurotrophic factor for dopaminergic amacrine cells. Diabetes 2004;53(9):2412-19
96. Ola MS, Nawaz MI, El-Asrar AA, et al. Reduced levels of brain derived neurotrophic factor (BDNF) in the serum of diabetic retinopathy patients and in the retina of diabetic rats. Cell Mol Neurobiol 2013;33(3):359-67
97. Abu-El-Asrar AM, Dralands L, Missotten L, et al. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci 2004;45(8): 2760-6
98. Liu Y, Tao L, Fu X, et al. BDNF protects retinal neurons from hyperglycemia through the TrkB/ERK/MAPK pathway. Mol Med Rep 2013;7(6):1773-8
99. Oshitari T, Yoshida-Hata N, Yamamoto S. Effect of neurotrophic factors on neuronal apoptosis and neurite regeneration in cultured rat retinas exposed to high glucose. Brain Res 2010;1346:43-51
100. Kermani P, Hempstead B. Brain-derived neurotrophic factor: A newly described mediator of angiogenesis. Trends Cardiovasc Med 2007;17(4):140-3
101. Atkinson J, Panni MK, Lund RD. Effects of neurotrophins on embryonic retinal outgrowth. Brain Res Dev Brain Res 1999; 112(2):173-80
102. Bosco A, Linden R. BDNF and NT-4 differentially modulate neurite outgrowth in developing retinal ganglion cells. J Neurosci Res 1999;57(6):759-69
103. Yoshida M, Feng L, Grimbert F, et al. Overexpression of neurotrophin-3 stimulates a second wave of dopaminergic amacrine cell genesis after birth in the mouse retina. J Neurosci 2011;31(35):12663-73
104. Das I, Sparrow JR, Lin MI, et al. Trk C signaling is required for retinal progenitor cell proliferation. J Neurosci 2000;20(8): 2887-95
105. Cohen A, Bray GM, Aguayo AJ. Neurotrophin-4/5 (NT-4/5) increases adult rat retinal ganglion cell survival and neurite outgrowth in vitro. J Neurobiol 1994;25(8): 953-9
106. Avwenagha O, Campbell G, Bird MM. The outgrowth response of the axons of developing and regenerating rat retinal ganglion cells in vitro to neurotrophin treatment. J Neurocytol 2003;32(9):1055-75
107. Bikbova G, Oshitari T, Yamamoto S. Neurite regeneration in adult rat retinas exposed to advanced glycation end-products and regenerative effects of neurotrophin-4. Brain Res 2013;1534:33-45
108. Oshitari T, Yoshida-Hata N, Yamamoto S. Effect of neurotrophin-4 on endoplasmic reticulum stress-related neuronal apoptosis in diabetic and high glucose exposed rat retinas. Neurosci Lett 2011;501(2):102-6
109. 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(3): 653-63.