Early distal axonopathy of the visual pathway in experimental diabetes

American Journal of Pathology

Volumn 180, Issue 1, 2012, Pages 303-313

  Fernandez, Diego C ^a,b   Pasquini, Laura A ^a   Dorfman, Damián ^a   Aldana Marcos, Hernán J ^b,c   Rosenstein, Ruth E ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSIDAD DE MORÓN   (Argentina)

^c UNIVERSIDAD DE BELGRANO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; MALE; MORPHOMETRICS; NERVE CELL; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA; SUPERIOR COLLICULUS; VISION;

ANIMALS; AXONS; CELL COUNT; CHOLERA TOXIN; COLORING AGENTS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DIABETIC RETINOPATHY; MALE; MICROSCOPY, ELECTRON; RATS; RATS, WISTAR; RETINAL GANGLION CELLS; VISUAL PATHWAYS;

EID: 83455258090     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.09.018     Document Type: Article

References (49)

1. R.A. Kowluru, P.S. Chan Oxidative stress and diabetic retinopathy Exp Diabetes Res 2007 2007 43603 43614
2. T.S. Kern, A.J. Barber Retinal ganglion cells in diabetes J Physiol 586 2008 4401 4408
3. A.J. Barber, E. Lieth, S.A. Khin, D.A. Antonetti, A.G. Buchanan, 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 (Pubitemid 28399611)
4. J. Kusari, S. Zhou, E. Padillo, K.G. Clarke, D.W. Gil Effect of memantine on neuroretinal function and retinal vascular changes of streptozotocin-induced diabetic rats Invest Ophthalmol Vis Sci 48 2007 5152 5159 (Pubitemid 351260926)
5. G.M. Seigel, S.B. Lupien, L.M. Campbell, D.N. Ishii Systemic IGF-I treatment inhibits cell death in diabetic rat retina J Diabetes Complications 20 2006 196 204
6. G.H. Bresnick Diabetic retinopathy viewed as a neurosensory disorder Arch Ophthalmol 104 1986 989 990
7. I.M. Ghafour, W.S. Foulds, D. Allan, E. McClure Contrast sensitivity in diabetic subjects with and without retinopathy Br J Ophthalmol 66 1982 492 495 (Pubitemid 12049948)
8. S. Della Sala, G. Bertoni, L. Somazzi, F. Stubbe, A.J. Wilkins Impaired contrast sensitivity in diabetic patients with and without retinopathy: a new technique for rapid assessment Br J Ophthalmol 69 1985 136 142 (Pubitemid 15085000)
9. S. Sokol, A. Moskowitz, B. Skarf, R. Evans, M. Molitch, B. Senior Contrast sensitivity in diabetics with and without background retinopathy Arch Ophthalmol 103 1985 51 54 (Pubitemid 15152624)
10. C.D. Georgakopoulos, M.I. Eliopoulou, A.M. Exarchou, V. Tzimis, N.M. Pharmakakis, B.E. Spiliotis Decreased contrast sensitivity in children and adolescents with type 1 diabetes mellitus J Pediatr Ophthalmol Strabismus 48 2011 92 97
11. B. Falsini, V. Porciatti, G. Scalia, S. Caputo, A. Minnella, M.A. Di Leo, G. Ghirlanda Steady-state pattern electroretinogram in insulin-dependent diabetics with no or minimal retinopathy Doc Ophthalmol 73 1989 193 200 (Pubitemid 20238190)
12. T.C. Prager, C.A. Garcia, C.A. Mincher, J. Mishra, H.H. Chu The pattern electroretinogram in diabetes Am J Ophthalmol 109 1990 279 284 (Pubitemid 20078945)
13. V. Martinelli, P.M. Piatti, M. Filippi, M. Pacchioni, M.R. Pastore, N. Canal, G. Comi Effects of hyperglycaemia on visual evoked potentials in insulin-dependent diabetic patients Acta Diabetol 29 1992 34 37
14. A. Uberall, C. Renner, S. Edl, E. Parzinger, D. Wenzel VEP and ERP abnormalities in children and adolescents with prepubertal onset of insulin dependent diabetes mellitus Neuropediatrics 27 1996 88 93 (Pubitemid 26159376)
15. A. Verrotti, L. Lobefalo, D. Trotta, G. Della Loggia, F. Chiarelli, C. Luigi, G. Morgese, P. Gallenga Visual evoked potentials in young persons with newly diagnosed diabetes: a long-term follow-up Dev Med Child Neurol 42 2000 240 244 (Pubitemid 30175923)
16. B.E. Wolff, M.A. Bearse Jr, M.E. Schneck, S. Barez, A.J. Adams Multifocal VEP (mfVEP) reveals abnormal neuronal delays in diabetes Doc Ophthalmol 1211 2010 89 96
17. M. Ino-ue, N. Ohgiya, M. Yamamoto Effect of aminoguanidine on optic nerve involvement in experimental diabetic rats Brain Res 800 1998 319 322 (Pubitemid 28361913)
18. M. Ino-Ue, L. Zhang, H. Naka, H. Kuriyama, M. Yamamoto Polyol metabolism of retrograde axonal transport in diabetic rat large optic nerve fiber Invest Ophthalmol Vis Sci 41 2000 4055 4058
19. G.L. Trick, R.M. Burde, M.D. Gordon, C. Kilo, J.V. Santiago Retinocortical conduction time in diabetics with abnormal pattern reversal electroretinograms and visual evoked potentials Doc Ophthalmol 70 1988 19 28
20. H.J. Aldana Marcos, C.C. Ferrari, I. Benitez, J.M. Affanni Standardization of fixation, processing and staining methods for the central nervous system of vertebrates Biocell 20 1996 265 272 (Pubitemid 126486884)
21. G. Paxinos, C. Watson The Rat Brain in Stereotaxic Coordinates 1997 Elsevier Amsterdam
22. D.C. Fernandez, M.P. Bordone, M.S. Chianelli, R.E. Rosenstein Retinal neuroprotection against ischemia-reperfusion damage induced by postconditioning Invest Ophthalmol Vis Sci 50 2009 3922 3930
23. S.D. Crish, R.M. Sappington, D.M. Inman, P.J. Horner, D.J. Calkins Distal axonopathy with structural persistence in glaucomatous neurodegeneration Proc Natl Acad Sci U S A 107 2010 5196 5201
24. A. Angelucci, F. Clascá, M. Sur Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains J Neurosci Methods 65 1996 101 112 (Pubitemid 26107803)
25. J.R. Prichard, H.S. Armacanqui, R.M. Benca, M. Behan Light-dependent retinal innervation of the rat superior colliculus Anat Rec (Hoboken) 290 2007 341 348 (Pubitemid 46731698)
26. L. Zhang, M. Ino-ue, K. Dong, M. Yamamoto Retrograde axonal transport impairment of large- and medium-sized retinal ganglion cells in diabetic rat Curr Eye Res 20 2000 131 136 (Pubitemid 30099166)
27. M.C. Moreno, H.J. Marcos, J. Oscar Croxatto, P.H. Sande, J. Campanelli, C.O. Jaliffa, J. Benozzi, R.E. Rosenstein A new experimental model of glaucoma in rats through intracameral injections of hyaluronic acid Exp Eye Res 81 2005 71 80 (Pubitemid 40840548)
28. N. Belforte, P. Sande, N. de Zavalía, P.A. Knepper, R.E. Rosenstein Effect of chondroitin sulfate on intraocular pressure in rats Invest Ophthalmol Vis Sci 51 2010 5768 5775
29. C. Escartin, G. Bonvento Targeted activation of astrocytes: a potential neuroprotective strategy Mol Neurobiol 38 2008 231 241
30. E. Rungger-Brndle, A.A. Dosso, P.M. Leuenberger Glial reactivity, an early feature of diabetic retinopathy Invest Ophthalmol Vis Sci 41 2000 1971 1980 (Pubitemid 30354375)
31. A.S. Ibrahim, A.B. El-Remessy, S. Matragoon, W. Zhang, Y. Patel, S. Khan, M.M. Al-Gayyar, M.M. El-Shishtawy, G.I. Liou Retinal microglial activation and inflammation induced by amadori-glycated albumin in a rat model of diabetes Diabetes 60 2011 1122 1133
32. D.A. Greene, A.A. Sima, M.J. Stevens, E.L. Feldman, S.A. Lattimer Complications: neuropathy, pathogenetic considerations Diabetes Care 15 1992 1902 1925
33. L. Giarelli, G. Grandi, M. Delendi, G. Falconieri Optic nerve in diabetes mellitus: a case control study Metab Pediatr Syst Ophthalmol 9 1986 71 73 (Pubitemid 17058328)
34. M. Ino-ue, H. Yokogawa, M. Yamamoto, H. Naka, H. Kuriyama Structural impairments in optic nerve of diabetic rats ameliorated with the aldose reductase inhibitor Exp Eye Res 66 1998 397 401 (Pubitemid 28206773)
35. I.S. Zagon, M.S. Klocek, J.W. Sassani, P.J. McLaughlin Dry eye reversal and corneal sensation restoration with topical naltrexone in diabetes mellitus Arch Ophthalmol 127 2009 1468 1473
36. C. Readhead, B. Popko, N. Takahashi, H.D. Shine, R.A. Saavedra, R.L. Sidman, L. Hood Expression of a myelin basic protein gene in transgenic shiverer mice: correction of the demyelinating phenotype Cell 48 1987 703 712 (Pubitemid 18096947)
37. H.D. Shine, C. Readhead, B. Popko, L. Hood, R.L. Sidman Morphometric analysis of normal, mutant, and transgenic CNS: correlation of myelin basic protein expression to myelinogenesis J Neurochem 58 1992 342 349
38. E.F. Bondan, M.A. Lallo, A.H. Trigueiro, C.P. Ribeiro, I.L. Sinhorini, D.L. Graa Delayed Schwann cell and oligodendrocyte remyelination after ethidium bromide injection in the brainstem of Wistar rats submitted to streptozotocin diabetogenic treatment Braz J Med Biol Res 39 2006 637 646 (Pubitemid 43676614)
39. H.A. Arnett, S.P.J. Fancy, J.A. Alberta, C. Zhao, S.R. Plant, S. Kaing, C.S. Raine, D.H. Rowitch, R.J. Franklin, C.D. Stiles bHLH transcription factor Olig1 is required to repairedmyelinated lesions in the CNS Science 306 2004 2111 2115 (Pubitemid 40007666)
40. A. Chang, W.W. Tourtellotte, R. Rudick, B.D. Trapp Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis N Engl J Med 346 2002 165 173 (Pubitemid 34438882)
41. G. Wolswijk Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells J Neurosci 18 1998 601 609 (Pubitemid 28041896)
42. T. Nakazawa, C. Nakazawa, A. Matsubara, K. Noda, T. Hisatomi, H. She, N. Michaud, A. Hafezi-Moghadam, J.W. Miller, L.I. Benowitz Tumor necrosis factor-α mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma J Neurosci 26 2006 12633 12641 (Pubitemid 44904557)
43. L. Conforti, R. Adalbert, M.P. Coleman Neuronal death: where does the end begin Trends Neurosci 30 2007 159 166 (Pubitemid 46505033)
44. M. Coleman Axon degeneration mechanisms: commonality amid diversity Nat Rev Neurosci 6 2005 889 898 (Pubitemid 41568730)
45. G.B. Stokin, C. Lillo, T.L. Falzone, R.G. Brusch, E. Rockenstein, S.L. Mount, R. Raman, P. Davies, E. Masliah, D.S. Williams, L.S. Goldstein Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease Science 307 2005 1282 1288 (Pubitemid 40299973)
46. B.P. Buckingham, D.M. Inman, W. Lambert, E. Oglesby, D.J. Calkins, M.R. Steele, M.L. Vetter, N. Marsh-Armstrong, P.J. Horner Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma J Neurosci 28 2008 2735 2744 (Pubitemid 351398885)
47. Y. Shirao, K. Kawasaki Electrical responses from diabetic retina Prog Retin Eye Res 17 1998 59 76 (Pubitemid 28040753)
48. E. Lieth, T.W. Gardner, A.J. Barber, D.A. Antonetti Retinal neurodegeneration: early pathology in diabetes Clin Exp Ophthalmol 28 2000 3 8 (Pubitemid 30433242)
49. V. Asnaghi, C. Gerhardinger, T. Hoehn, A. Adeboje, M. Lorenzi A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat Diabetes 52 2003 506 511 (Pubitemid 36173210)