Diabetic retinopathy: recent advances towards understanding neurodegeneration and vision loss

Science China Life Sciences

Volumn 58, Issue 6, 2015, Pages 541-549

  Barber, Alistair J ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

apoptosis; dendrite; diabetes; neurodegeneration; retina; synapse; vascular function; visual function

Indexed keywords

ANIMALIA;

ANIMAL; APOPTOSIS; BLINDNESS; CYTOLOGY; DENDRITE; DIABETIC RETINOPATHY; DISEASE COURSE; GLIA; HUMAN; METABOLISM; MOUSE; NERVE CELL; NEURODEGENERATIVE DISEASES; OPTICAL COHERENCE TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; RAT; RETINA; SYNAPSE;

ANIMALS; APOPTOSIS; BLINDNESS; DENDRITES; DIABETIC RETINOPATHY; DISEASE PROGRESSION; HUMANS; MICE; NEURODEGENERATIVE DISEASES; NEUROGLIA; NEURONS; RATS; RETINA; SYNAPSES; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84931562120     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-015-4856-x     Document Type: Review

References (88)

1. Gastinger MJ, Singh RS, Barber AJ. Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and ins2akita-diabetic mouse retinas. Invest Ophthalmol Vis Sci, 2006, 47: 3143–3150
2. Gastinger MJ, Kunselman AR, Conboy EE, Bronson SK, Barber AJ. Dendrite remodeling and other abnormalities in the retinal ganglion cells of ins2 akita diabetic mice. Invest Ophthalmol Vis Sci, 2008, 49: 2635–2642
3. Bloodworth JM Jr., Molitor DL. Ultrastructural aspects of human and canine diabetic retinopathy. Invest Ophthalmol, 1965, 4: 1037–1048
4. Bloodworth JM Jr. Diabetic microangiopathy. Diabetes, 1963, 12: 99–114
5. Cunha-Vaz JG. Pathophysiology of diabetic retinopathy. British J Ophthalmol, 1978, 62: 351–355
6. Cunha-Vaz JG. Studies on the pathophysiology of diabetic retinopathy. The blood-retinal barrier in diabetes. Diabetes, 1983, 32(Suppl 2): 20–27
7. Bloodworth JM Jr. Diabetic retinopathy. Diabetes, 1962, 11: 1–22
8. Wolter JR. Diabetic retinopathy. Am J Ophthalmol, 1961, 51: 1123–1139
9. Mizutani M, Kern TS, Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest, 1996, 97: 2883–2890
10. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest, 1998, 102: 783–791
11. Kanamori A, Nakamura M, Mukuno H, Maeda H, Negi A. Diabetes has an additive effect on neural apoptosis in rat retina with chronically elevated intraocular pressure. Curr Eye Res, 2004, 28: 47–54
12. Martin PM, Roon P, Van Ells TK, Ganapathy V, Smith SB. Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci, 2004, 45: 3330–3336
13. Barber AJ, Antonetti DA, Kern TS, Reiter CE, Soans RS, Krady JK, Levison SW, Gardner TW, Bronson SK. The ins2akita mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci, 2005, 46: 2210–2218
14. Ning X, Baoyu Q, Yuzhen L, Shuli S, Reed E, Li QQ. Neuro-optic cell apoptosis and microangiopathy in kkay mouse retina. Int J Mol Med, 2004, 13: 87–92
15. Park SH, Park JW, Park SJ, Kim KY, Chung JW, Chun MH, Oh SJ. Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina. Diabetologia, 2003, 46: 1260–1268
16. Feit-Leichman RA, Kinouchi R, Takeda M, Fan Z, Mohr S, Kern TS, Chen DF. Vascular damage in a mouse model of diabetic retinopathy: relation to neuronal and glial changes. Invest Ophthalmol Vis Sci, 2005, 46: 4281–4287
17. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuro-Psychopharmacol Biol Psychiatry, 2003, 27: 283–290
18. Barber AJ, Gardner TW, Abcouwer SF. The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci, 2011, 52: 1156–1163
19. Barber AJ, Lieth E. Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier. Dev Dyn, 1997, 208: 62–74
20. Abu-El-Asrar AM, Dralands L, Missotten L, Al-Jadaan IA, Geboes K. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci, 2004, 45: 2760–2766
21. Aung MH, Park HN, Han MK, Obertone TS, Abey J, Aseem F, Thule PM, Iuvone PM, Pardue MT. Dopamine deficiency contributes to early visual dysfunction in a rodent model of type 1 diabetes. J Neurosci, 2014, 34: 726–736
22. Lopes de Faria JM, Russ H, Costa VP. Retinal nerve fibre layer loss in patients with type 1 diabetes mellitus without retinopathy. British J Ophthalmol, 2002, 86: 725–728
23. Ozdek S, Lonneville YH, Onol M, Yetkin I, Hasanreisoglu BB. Assessment of nerve fiber layer in diabetic patients with scanning laser polarimetry. Eye (London, England), 2002, 16: 761–765
24. Takahashi H, Goto T, Shoji T, Tanito M, Park M, Chihara E. Diabetes-associated retinal nerve fiber damage evaluated with scanning laser polarimetry. Am J Ophthalmol, 2006, 142: 88–94
25. Sugimoto M, Sasoh M, Ido M, Wakitani Y, Takahashi C, Uji Y. Detection of early diabetic change with optical coherence tomography in type 2 diabetes mellitus patients without retinopathy. Ophthalmologica, 2005, 219: 379–385
26. Biallosterski C, van Velthoven ME, Michels RP, Schlingemann RO, DeVries JH, Verbraak FD. Decreased optical coherence tomographymeasured pericentral retinal thickness in patients with diabetes mellitus type 1 with minimal diabetic retinopathy. British J Ophthalmol, 2007, 91: 1135–1138
27. Peng PH, Lin HS, Lin S. Nerve fibre layer thinning in patients with preclinical retinopathy. Can J Ophthalmol, 2009, 44: 417–422
28. van Dijk HW, Kok PHB, Garvin M, Sonka M, Devries JH, Michels RPJ, van Velthoven MEJ, Schlingemann RO, Verbraak FD, Abramoff MD. Selective loss of inner retinal layer thickness in type 1 diabetic patients with minimal diabetic retinopathy. Invest Ophthalmol Vis Sci, 2009, 50: 3404–3409
29. van Dijk HW, Verbraak FD, Kok PH, Garvin MK, Sonka M, Lee K, Devries JH, Michels RP, van Velthoven ME, Schlingemann RO, Abramoff MD. Decreased retinal ganglion cell layer thickness in patients with type 1 diabetes. Invest Ophthalmol Vis Sci, 2010, 51: 3660–3665
30. van Dijk HW, Verbraak FD, Kok PH, Stehouwer M, Garvin MK, Sonka M, DeVries JH, Schlingemann RO, Abramoff MD. Early neurodegeneration in the retina of type 2 diabetic patients. Invest Ophthalmol Vis Sci, 2012, 53: 2715–2719
31. Vujosevic S, Midena E. Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and muller cells alterations. J Diabetes Res, 2013, 2013: 905058
32. Oshitari T, Hanawa K, Adachi-Usami E. Changes of macular and rnfl thicknesses measured by stratus oct in patients with early stage diabetes. Eye (London, England), 2009, 23: 884–889
33. Browning DJ, Fraser CM, Clark S. The relationship of macular thickness to clinically graded diabetic retinopathy severity in eyes without clinically detected diabetic macular edema. Ophthalmology, 2008, 115: 533–539.e532
34. Asefzadeh B, Fisch BM, Parenteau CE, Cavallerano AA. Macular thickness and systemic markers for diabetes in individuals with no or mild diabetic retinopathy. Clin Exp Ophthalmol, 2008, 36: 455–463
35. Araszkiewicz A, Zozulinska-Ziolkiewicz D, Meller M, Bernardczyk-Meller J, Pilacinski S, Rogowicz-Frontczak A, Naskret D, Wierusz-Wysocka B. Neurodegeneration of the retina in type 1 diabetic patients. Pol Arch Med Wewn, 2012, 122: 464–470
36. Bronson-Castain KW, Bearse MA, Jr., Neuville J, Jonasdottir S, King-Hooper B, Barez S, Schneck ME, Adams AJ. Adolescents with type 2 diabetes: Early indications of focal retinal neuropathy, retinal thinning, and venular dilation. Retina, 2009, 29: 618–626
37. van Dijk HW, Verbraak FD, Stehouwer M, Kok PH, Garvin MK, Sonka M, DeVries JH, Schlingemann RO, Abramoff MD. Association of visual function and ganglion cell layer thickness in patients with diabetes mellitus type 1 and no or minimal diabetic retinopathy. Vis Res, 2011, 51: 224–228
38. Frisen L. New, sensitive window on abnormal spatial vision: rarebit probing. Vis Res, 2002, 42: 1931–1939
39. Zhi Z, Chao JR, Wietecha T, Hudkins KL, Alpers CE, Wang RK. Noninvasive imaging of retinal morphology and microvasculature in obese mice using optical coherence tomography and optical microangiography. Invest Ophthalmol Vis Sci, 2014, 55: 1024–1030
40. Yang JH, Kwak HW, Kim TG, Han J, Moon SW, Yu SY. Retinal neurodegeneration in type ii diabetic otsuka long-evans tokushima fatty rats. Invest Ophthalmol Vis Sci, 2013, 54: 3844–3851
41. McLenachan S, Chen X, McMenamin PG, Rakoczy EP. Absence of clinical correlates of diabetic retinopathy in the ins2akita retina. Clin Exp Ophthalmol, 2013, 41: 582–592
42. Hombrebueno JR, Chen M, Penalva RG, Xu H. Loss of synaptic connectivity, particularly in second order neurons is a key feature of diabetic retinal neuropathy in the ins2akita mouse. PLoS One, 2014, 9: e97970
43. VanGuilder HD, Brucklacher RM, Patel K, Ellis RW, Freeman WM, Barber AJ. Diabetes downregulates presynaptic proteins and reduces basal synapsin i phosphorylation in rat retina. Eur J Neurosci, 2008, 28: 1–11
44. Gaspar JM, Baptista FI, Galvao J, Castilho AF, Cunha RA, Ambrosio AF. Diabetes differentially affects the content of exocytotic proteins in hippocampal and retinal nerve terminals. Neuroscience, 2010, 169: 1589–1600
45. Masser DR, VanGuilder Starkey HD, Bixler GV, Dunton W, Bronson SK, Freeman WM. Insulin treatment normalizes retinal neuroinflammation but not markers of synapse loss in diabetic rats. Exp Eye Res, 2014, 125: 95–106
46. Kurihara T, Ozawa Y, Nagai N, Shinoda K, Noda K, Imamura Y, Tsubota K, Okano H, Oike Y, Ishida S. Angiotensin II type 1 receptor signaling contributes to synaptophysin degradation and neuronal dysfunction in the diabetic retina. Diabetes, 2008, 57: 2191–2198
47. Sasaki M, Ozawa Y, Kurihara T, Kubota S, Yuki K, Noda K, Kobayashi S, Ishida S, Tsubota K. Neurodegenerative influence of oxidative stress in the retina of a murine model of diabetes. Diabetologia, 2010, 53: 971–979
48. D’Cruz TS, Weibley BN, Kimball SR, Barber AJ. Post-translational processing of synaptophysin in the rat retina is disrupted by diabetes. PLoS One, 2012, 7: e44711
49. Qin Y, Xu G, Wang W. Dendritic abnormalities in retinal ganglion cells of three-month diabetic rats. Curr Eye Res, 2006, 31: 967–974
50. Meyer-Rusenberg B, Pavlidis M, Stupp T, Thanos S, Meyer-Rusenberg B, Pavlidis M, Stupp T, Thanos S. Pathological changes in human retinal ganglion cells associated with diabetic and hypertensive retinopathy. Graefes Arch Clin Exp Ophthalmol, 2007, 245: 1009–1018
51. Simonsen SE. Prognostic value of erg (oscillatory potential) in juvenile diabetics. Acta Ophthalmol Suppl, 1974, 123: 223–224
52. Frost-Larsen K, Larsen HW, Simonsen SE. Oscillatory potential and nyctometry in insulin-dependent diabetics. Acta Ophthalmol (Copenh), 1980, 58: 879–888
53. Simonsen SE. The value of the oscillatory potential in selecting juvenile diabetics at risk of developing proliferative retinopathy. Acta Ophthalmol (Copenh), 1980, 58: 865–878
54. Li Q, Zemel E, Miller B, Perlman I. Early retinal damage in experimental diabetes: electroretinographical and morphological observations. Exp Eye Res, 2002, 74: 615–625
55. Shinoda K, Rejdak R, Schuettauf F, Blatsios G, Volker M, Tanimoto N, Olcay T, Gekeler F, Lehaci C, Naskar R, Zagorski Z, Zrenner E. Early electroretinographic features of streptozotocin-induced diabetic retinopathy. Clin Exp Ophthalmol, 2007, 35: 847–854
56. Kohzaki K, Vingrys AJ, Bui BV, Kohzaki K, Vingrys AJ, Bui BV. Early inner retinal dysfunction in streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci, 2008, 49: 3595–3604
57. Hancock HA, Kraft TW. Oscillatory potential analysis and ergs of normal and diabetic rats. Invest Ophthalmol Vis Sci, 2004, 45: 1002–1008
58. Aung MH, Kim MK, Olson DE, Thule PM, Pardue MT. Early visual deficits in streptozotocin-induced diabetic long evans rats. Invest Ophthalmol Vis Sci, 2013, 54: 1370–1377
59. Bush RA, Hawks KW, Sieving PA. Preservation of inner retinal responses in the aged royal college of surgeons rat. Evidence against glutamate excitotoxicity in photoreceptor degeneration. Invest Ophthalmol Vis Sci, 1995, 36: 2054–2062
60. Sugawara T, Sieving PA, Iuvone PM, Bush RA. The melatonin antagonist luzindole protects retinal photoreceptors from light damage in the rat. Invest Ophthalmol Vis Sci, 1998, 39: 2458–2465
61. Bui BV, Fortune B. Ganglion cell contributions to the rat full-field electroretinogram. J Physiol, 2004, 555: 153–173
62. Abraham FA, Haimovitz J, Berezin M. The photopic and scotopic visual thresholds in diabetics without diabetic retinopathy. Metab Pediatr Syst Ophthalmol, 1988, 11: 76–77
63. Aylward GW, Billson FA. The scotopic threshold response in diabetic retinopathy—a preliminary report. Aus New Zealand J Ophthalmol, 1989, 17: 369–372
64. Nasralah Z, Robinson W, Jackson G, Barber A. Measuring visual function in diabetic retinopathy: progress in basic and clinical research. J Clin Exp Ophthalmol, 2013, 4: 1000306
65. Ha Y, Saul A, Tawfik A, Zorrilla EP, Ganapathy V, Smith SB. Diabetes accelerates retinal ganglion cell dysfunction in mice lacking sigma receptor 1. Mol Vis, 2012, 18: 2860–2870
66. Bui BV, Loeliger M, Thomas M, Vingrys AJ, Rees SM, Nguyen CTO, He Z, Tolcos M. Investigating structural and biochemical correlates of ganglion cell dysfunction in streptozotocin-induced diabetic rats. Exp Eye Res, 2009, 88: 1076–1083
67. Prusky GT, Alam NM, Beekman S, Douglas RM. Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci, 2004, 45: 4611–4616
68. Kirwin SJ, Kanaly ST, Hansen CR, Cairns BJ, Ren M, Edelman JL. Retinal gene expression and visually evoked behavior in diabetic long evans rats. Invest Ophthalmol Vis Sci, 2011, 52: 7654–7663
69. Akimov NP, Renteria RC. Spatial frequency threshold and contrast sensitivity of an optomotor behavior are impaired in the ins2akita mouse model of diabetes. Behav Brain Res, 2012, 226: 601–605
70. Umino Y, Solessio E. Loss of scotopic contrast sensitivity in the optomotor response of diabetic mice. Invest Ophthalmol Vis Sci, 2013, 54: 1536–1543
71. Muir ER, Renteria RC, Duong TQ. Reduced ocular blood flow as an early indicator of diabetic retinopathy in a mouse model of diabetes. Invest Ophthalmol Vis Sci, 2012, 53: 6488–6494
72. Lee CA, Li G, Patel MD, Petrash JM, Benetz BA, Veenstra A, Amengual J, von Lintig J, Burant CJ, Tang J, Kern TS. Diabetesinduced impairment in visual function in mice: Contributions of p38 mapk, rage, leukocytes, and aldose reductase. Invest Ophthalmol Vis Sci, 2014, 55: 2904–2910
73. Xu Z, Wei Y, Gong J, Cho H, Park JK, Sung ER, Huang H, Wu L, Eberhart C, Handa JT, Du Y, Kern TS, Thimmulappa R, Barber AJ, Biswal S, Duh EJ. Nrf2 plays a protective role in diabetic retinopathy in mice. Diabetologia, 2014, 57: 204–213
74. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW. Diabetic retinopathy: more than meets the eye. Survey Ophthalmol, 2002, 47: S253–262
75. Antonetti DA, Barber AJ, Khin S, Lieth E, Tarbell JM, Gardner TW. Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells. Diabetes, 1998, 47: 1953–1959
76. Murakami T, Felinski EA, Antonetti DA. Occludin phosphorylation and ubiquitination regulate tight junction trafficking and vascular endothelial growth factor-induced permeability. J Biol Chem, 2009, 284: 21036–21046
77. Abcouwer SF, Gardner TW. Diabetic retinopathy: loss of neuroretinal adaptation to the diabetic metabolic environment. Ann New York Acad Sci, 2014, 1311: 174–190
78. Lott ME, Slocomb JE, Shivkumar V, Smith B, Gabbay RA, Quillen D, Gardner TW, Bettermann K. Comparison of retinal vasodilator and constrictor responses in type 2 diabetes. Acta Ophthalmol (Oxf), 2012, 90: e434–441
79. Lott ME, Slocomb JE, Shivkumar V, Smith B, Quillen D, Gabbay RA, Gardner TW, Bettermann K. Impaired retinal vasodilator responses in prediabetes and type 2 diabetes. Acta Ophthalmol (Oxf), 2013, 91: e462–469
80. Ott C, Raff U, Schmidt S, Kistner I, Friedrich S, Bramlage P, Harazny JM, Schmieder RE. Effects of saxagliptin on early microvascular changes in patients with type 2 diabetes. Cardiovasc Diabetol, 2014, 13: 19
81. Lasta M, Pemp B, Schmidl D, Boltz A, Kaya S, Palkovits S, Werkmeister R, Howorka K, Popa-Cherecheanu A, Garhofer G, Schmetterer L. Neurovascular dysfunction precedes neural dysfunction in the retina of patients with type 1 diabetes. Invest Ophthalmol Vis Sci, 2013, 54: 842–847
82. Bearse MA, Jr., Adams AJ, Han Y, Schneck ME, Ng J, Bronson-Castain K, Barez S. A multifocal electroretinogram model predicting the development of diabetic retinopathy. Prog Retinal Eye Res, 2006, 25: 425–448
83. Ng JS, Bearse MA, Jr., Schneck ME, Barez S, Adams AJ. Local diabetic retinopathy prediction by multifocal erg delays over 3 years. Invest Ophthalmol Vis Sci, 2008, 49: 1622–1628
84. Cunha-Vaz J, Ribeiro L, Lobo C. Phenotypes and biomarkers of diabetic retinopathy. Prog Retinal Eye Res, 2014, 41: 90–111
85. Jackson GR, Scott IU, Quillen DA, Walter LE, Gardner TW. Inner retinal visual dysfunction is a sensitive marker of non-proliferative diabetic retinopathy. British J Ophthalmol, 2012, 96: 699–703
86. Holfort SK, Jackson GR, Larsen M. Dark adaptation during transient hyperglycemia in type 2 diabetes. Exp Eye Res, 2010, 91: 710–714
87. Jackson GR, Barber AJ. Visual dysfunction associated with diabetic retinopathy. Curr Diabetes Rep, 2010, 10: 380–384
88. Somfai GM, Tatrai E, Laurik L, Varga B, Olvedy V, Jiang H, Wang J, Smiddy WE, Somogyi A, DeBuc DC. Automated classifiers for early detection and diagnosis of retinopathy in diabetic eyes. BMC Bioinformatics, 2014, 15: 106