Neuronal cell death in the inner retina and the influence of vascular endothelial growth factor inhibition in a diabetic rat model

American Journal of Pathology

Volumn 184, Issue 6, 2014, Pages 1752-1762

  Park, Hae Young Lopilly ^a   Kim, Jie Hyun ^a   Park, Chan Kee ^a  

^a The Catholic University of Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; PROTEIN KINASE B; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; NEUTRALIZING ANTIBODY; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT; VASCULOTROPIN A;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NECROSIS; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA GANGLION CELL; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; DIABETIC RETINOPATHY; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIBODIES, NEUTRALIZING; APOPTOSIS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; MALE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84901020200     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.02.016     Document Type: Article

References (41)

1. T.S. Kern, and R.L. Engerman Vascular lesions in diabetes are distributed non-uniformly within the retina Exp Eye Res 60 1995 545 549
2. A.V. Ljubimov, R.E. Burgeson, R.J. Butkowski, J.R. Couchman, L. Zardi, Y. Ninomiya, Y. Sado, Z.S. Huang, A.B. Nesburn, and M.C. Kenney Basement membrane abnormalities in human eyes with diabetic retinopathy J Histochem Cytochem 44 1996 1469 1479
3. D.A. Antonetti, A.J. Barber, S.K. Bronson, W.M. Freeman, T.W. Gardner, L.S. Jefferson, M. Kester, S.R. Kimball, J.K. Krady, K.F. LaNoue, C.C. Norbury, P.G. Quinn, L. Sandirasegarane, I.A. Simpson Group JDRC Diabetic retinopathy: seeing beyond glucose-induced microvascular disease Diabetes 55 2006 2401 2411
4. A.J. Barber, E. Lieth, S.A. Khin, D.A. Antonetti, A.G. Buchanan, and T.W. Gardner Neural apoptosis in the retina during experimental and human diabetes: early onset and effect of insulin J Clin Invest 102 1998 783 791
5. M.J. Gastinger, R.S. Singh, and A.J. Barber Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas Invest Ophthalmol Vis Sci 47 2006 3143 3150
6. P.M. Martin, P. Roon, T.K. Van Ells, V. Ganapathy, and S.B. Smith Death of retinal neurons in streptozotocin-induced diabetic mice Invest Ophthalmol Vis Sci 45 2004 3330 3336
7. S.H. Park, J.W. Park, S.J. Park, K.Y. Kim, J.W. Chung, M.H. Chun, and S.J. Oh Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina Diabetologia 46 2003 1260 1268
8. R.H. Foxton, A. Finkelstein, S. Vijay, A. Dahlmann-Noor, P.T. Khaw, J.E. Morgan, D.T. Shima, and Y.S. Ng VEGF-A is necessary and sufficient for retinal neuroprotection in models of experimental glaucoma Am J Pathol 182 2013 1379 1390
9. L.A. Kim, and P.A. D'Amore A brief history of anti-VEGF for the treatment of ocular angiogenesis Am J Pathol 181 2012 376 379
10. H. Ozaki, M.S. Seo, K. Ozaki, H. Yamada, E. Yamada, N. Okamoto, F. Hofmann, J.M. Wood, and P.A. Campochiaro Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization Am J Pathol 156 2000 697 707
11. P.A. D'Amore Vascular endothelial cell growth factor-A: not just for endothelial cells anymore Am J Pathol 171 2007 14 18
12. N. Beazley-Long, J. Hua, T. Jehle, R.P. Hulse, R. Dersch, C. Lehrling, H. Bevan, Y. Qiu, W.A. Lagreze, D. Wynick, A.J. Churchill, P. Kehoe, S.J. Harper, D.O. Bates, and L.F. Donaldson VEGF-A165b is an endogenous neuroprotective splice isoform of vascular endothelial growth factor A in vivo and in vitro Am J Pathol 183 2013 918 929
13. N.C. Miguel, M. Matsuda, A.L. Portes, S. Allodi, R. Mendez-Otero, T. Puntar, A. Sholl-Franco, P.G. Krempel, and M.L. Monteiro In vitro effects of bevacizumab treatment on newborn rat retinal cell proliferation, death, and differentiation Invest Ophthalmol Vis Sci 53 2012 7904 7911
14. I. Kim, A.M. Ryan, R. Rohan, S. Amano, S. Agular, J.W. Miller, and A.P. Adamis Constitutive expression of VEGF, VEGFR-1, and VEGFR-2 in normal eyes Invest Ophthalmol Vis Sci 40 1999 2115 2121
15. K.L. Jin, X.O. Mao, and D.A. Greenberg Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia Proc Natl Acad Sci U S A 97 2000 10242 10247
16. E. Gomes, L. Papa, T. Hao, and P. Rockwell The VEGFR2 and PKA pathways converge at MEK/ERK1/2 to promote survival in serum deprived neuronal cells Mol Cell Biochem 305 2007 179 190
17. L. Tolosa, M. Mir, V.J. Asensio, G. Olmos, and J. Llado Vascular endothelial growth factor protects spinal cord motoneurons against glutamate-induced excitotoxicity via phosphatidylinositol 3-kinase J Neurochem 105 2008 1080 1090
18. L. Kowalczuk, E. Touchard, S. Omri, L. Jonet, C. Klein, F. Valamanes, M. Berdugo, P. Bigey, P. Massin, J.C. Jeanny, and F. Behar-Cohen Placental growth factor contributes to micro-vascular abnormalization and blood-retinal barrier breakdown in diabetic retinopathy PLoS One 6 2011 e17462
19. Q. Xu, T. Qaum, and A.P. Adamis Sensitive blood-retinal barrier breakdown quantitation using Evans blue Invest Ophthalmol Vis Sci 42 2001 789 794
20. E.M. Kohner, V. Patel, and S.M. Rassam Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy Diabetes 44 1995 603 607
21. T.A. Gardiner, D.B. Archer, T.M. Curtis, and A.W. Stitt Arteriolar involvement in the microvascular lesions of diabetic retinopathy: implications for pathogenesis Microcirculation 14 2007 25 38
22. M. Mizutani, T.S. Kern, and M. Lorenzi Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy J Clin Invest 97 1996 2883 2890
23. T. Qaum, Q. Xu, A.M. Joussen, M.W. Clemens, W. Qin, K. Miyamoto, H. Hassessian, S.J. Wiegand, J. Rudge, G.D. Yancopoulos, and A.P. Adamis VEGF-initiated blood-retinal barrier breakdown in early diabetes Invest Ophthalmol Vis Sci 42 2001 2408 2413
24. A.W. Stitt, N. Lois, R.J. Medina, P. Adamson, and T.M. Curtis Advances in our understanding of diabetic retinopathy Clin Sci 125 2013 1 17
25. E.V. Famiglietti, E.G. Stopa, E.D. McGookin, P. Song, V. LeBlanc, and B.W. Streeten Immunocytochemical localization of vascular endothelial growth factor in neurons and glial cells of human retina Brain Res 969 2003 195 204
26. D.T. Shima, A. Gougos, J.W. Miller, M. Tolentino, G. Robinson, A.P. Adamis, and P.A. D'Amore Cloning and mRNA expression of vascular endothelial growth factor in ischemic retinas of Macaca fascicularis Invest Ophthalmol Vis Sci 37 1996 1334 1340
27. T.N. Jelsma, H.H. Friedman, M. Berkelaar, G.M. Bray, and A.J. Aguayo Different forms of the neurotrophin receptor trkB mRNA predominate in rat retina and optic nerve J Neurobiol 24 1993 1207 1214
28. S. Mansour-Robaey, D.B. Clarke, Y.C. Wang, G.M. Bray, and A.J. Aguayo Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells Proc Natl Acad Sci U S A 91 1994 1632 1636
29. M.T. Perez, and E. Caminos Expression of brain-derived neurotrophic factor and of its functional receptor in neonatal and adult rat retina Neurosci Lett 183 1995 96 99
30. J.M. Martinez-de-la-Casa, A. Ruiz-Calvo, F. Saenz-Frances, J. Reche-Frutos, C. Calvo-Gonzalez, J. Donate-Lopez, and J. Garcia-Feijoo Retinal nerve fiber layer thickness changes in patients with age-related macular degeneration treated with intravitreal ranibizumab Invest Ophthalmol Vis Sci 53 2012 6214 6218
31. R.K. Seth, S. Salim, M.B. Shields, and R.A. Adelman Assessment of optic nerve cup-to-disk ratio changes in patients receiving multiple intravitreal injections of antivascular endothelial growth factor agents Retina 29 2009 956 959
32. M.B. Horsley, N. Mandava, M.A. Maycotte, and M.Y. Kahook Retinal nerve fiber layer thickness in patients receiving chronic anti-vascular endothelial growth factor therapy Am J Ophthalmol 150 2010 558 561.e1
33. H.Y. Park, I.T. Kim, and C.K. Park Early diabetic changes in the nerve fibre layer at the macula detected by spectral domain optical coherence tomography Br J Ophthalmol 95 2011 1223 1228
34. Y. Wang, X.O. Mao, L. Xie, S. Banwait, H.H. Marti, D.A. Greenberg, and K. Jin Vascular endothelial growth factor overexpression delays neurodegeneration and prolongs survival in amyotrophic lateral sclerosis mice J Neurosci 27 2007 304 307
35. M. Al-Latayfeh, P.S. Silva, J.K. Sun, and L.P. Aiello Antiangiogenic therapy for ischemic retinopathies Cold Spring Harb Perspect Med 2 2012 a006411
36. A. Iriyama, Y.N. Chen, Y. Tamaki, and Y. Yanagi Effect of anti-VEGF antibody on retinal ganglion cells in rats Br J Ophthalmol 91 2007 1230 1233
37. S. Thaler, M. Fiedorowicz, T.J. Choragiewicz, S. Bolz, A. Tura, S. Henke-Fahle, E. Yoeruek, E. Zrenner, K.U. Bartz-Schmidt, F. Ziemssen, and F. Schuettauf Toxicity testing of the VEGF inhibitors bevacizumab, ranibizumab and pegaptanib in rats both with and without prior retinal ganglion cell damage Acta Ophthalmol 88 2010 e170 e176
38. V.S. Brar, R.K. Sharma, R.K. Murthy, and K.V. Chalam Bevacizumab neutralizes the protective effect of vascular endothelial growth factor on retinal ganglion cells Mol Vis 16 2010 1848 1853
39. M. Saint-Geniez, A.S. Maharaj, T.E. Walshe, B.A. Tucker, E. Sekiyama, T. Kurihara, D.C. Darland, M.J. Young, and P.A. D'Amore Endogenous VEGF is required for visual function: evidence for a survival role on muller cells and photoreceptors PLoS One 3 2008 e3554
40. B. Guo, Y. Wang, Y. Hui, X. Yang, and Q. Fan Effects of anti-VEGF agents on rat retinal Muller glial cells Mol Vis 16 2010 793 799
41. M.R. Romano, F. Biagioni, G. Besozzi, A. Carrizzo, C. Vecchione, F. Fornai, and M.D. Lograno Effects of bevacizumab on neuronal viability of retinal ganglion cells in rats Brain Res 1478 2012 55 63