Retinal proteome alterations in a mouse model of type 2 diabetes

Diabetologia

Volumn 57, Issue 1, 2014, Pages 192-203

  Ly, Alice ^a   Scheerer, Markus F ^a   Zukunft, Sven ^a   Muschet, Caroline ^a   Merl, Juliane ^a   Adamski, Jerzy ^a,b   Hrabě De Angelis, Martin ^a,b   Neschen, Susanne ^a   Hauck, Stefanie M ^a   Ueffing, Marius ^a,c  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Complex I; Diabetes; Label free mass spectrometry; Membrane; Metformin; Proteome; Retinopathy; VGLUT1

Indexed keywords

AMINO ACID TRANSPORTER; CYCLIC NUCLEOTIDE GATED CHANNEL; EXCITATORY AMINO ACID TRANSPORTER 1; GLUTAMIC ACID; K RAS PROTEIN; MESSENGER RNA; METFORMIN; NUCLEOTIDASE; ORGANIC ANION TRANSPORTER B; PLACEBO; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PROTEOME; RETINOL DEHYDROGENASE; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1A1; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B1; SUCCINATE DEHYDROGENASE (UBIQUINONE); SYNAPTOGYRIN; VESICULAR GLUTAMATE TRANSPORTER 1; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; MALE; MASS SPECTROMETRY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; POLYMERASE CHAIN REACTION SYSTEM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RETINA; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; MALE; MICE; PROTEOME; RETINA;

EID: 84890894593     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-013-3070-2     Document Type: Article

References (50)

1. King H, Aubert RE, Herman WH (1998) Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care 21:1414-1431
2. Cusi K, Consoli A, DeFronzo RA (1996) Metabolic effects of metformin on glucose and lactate metabolism in noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 81:4059-4067
3. UKPDS (1998) Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34) UK Prospective Diabetes Study (UKPDS) Group. Lancet 352:854-865
4. Stamler J, Vaccaro O, Neaton JD, Wentworth D (1993) Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 16:434-444
5. Perneger TV, Brancati FL, Whelton PK, Klag MJ (1994) End-stage renal disease attributable to diabetes mellitus. Ann Intern Med 121:912-918
6. Fong DS, Aiello L, Gardner TW et al (2003) Diabetic retinopathy. Diabetes Care 26:226-229
7. Cogan DG, Toussaint D, Kuwabara T (1961) Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol 66:366-378
8. Di Leo MA, Caputo S, Falsini B et al (1992) Nonselective loss of contrast sensitivity in visual system testing in early type I diabetes. Diabetes Care 15:620-625
9. Hardy KJ, Lipton J, Scase MO, Foster DH, Scarpello JH (1992) Detection of colour vision abnormalities in uncomplicated type 1 diabetic patients with angiographically normal retinas. Br J Ophthalmol 76:461-464
10. Mizutani M, Gerhardinger C, Lorenzi M (1998) Muller cell changes in human diabetic retinopathy. Diabetes 47:445-449
11. Bearse MA Jr, Han Y, Schneck ME, Adams AJ (2004) Retinal function in normal and diabetic eyes mapped with the slow flash multifocal electroretinogram. Invest Ophthalmol Vis Sci 45:296-304
12. Phipps JA, Fletcher EL, Vingrys AJ (2004) Paired-flash identification of rod and cone dysfunction in the diabetic rat. Invest Ophthalmol Vis Sci 45:4592-4600
13. Tyrberg M, Lindblad U, Melander A, Lovestam-Adrian M, Ponjavic V, Andreasson S (2011) Electrophysiological studies in newly onset type 2 diabetes without visible vascular retinopathy. Doc Ophthalmol 123:193-198
14. Ottlecz A, Garcia CA, Eichberg J, Fox DA (1993) Alterations in retinal Na+, K(+)-ATPase in diabetes: streptozotocin-induced and Zucker diabetic fatty rats. Curr Eye Res 12:1111-1121
15. Phipps JA, Yee P, Fletcher EL, Vingrys AJ (2006) Rod photoreceptor dysfunction in diabetes: activation, deactivation, and dark adaptation. Invest Ophthalmol Vis Sci 47:3187-3194
16. Yee P, Weymouth AE, Fletcher EL, Vingrys AJ (2009) A role for omega-3 polyunsaturated fatty acid supplements in diabetic neuropathy. Invest Ophthalmol Vis Sc 51:1755-1764
17. Kodama H, Fujita M, Yamaguchi I (1994) Development of hyperglycaemia and insulin resistance in conscious genetically diabetic (C57BL/KsJ-db/db) mice. Diabetologia 37:739-744
18. Barile GR, Pachydaki SI, Tari SR et al (2005) The RAGE axis in early diabetic retinopathy. Invest Ophthalmol Vis Sci 46:2916-2924
19. Cheung AK, Fung MK, Lo AC et al (2005) Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes 54:3119-3125
20. Xiao C, He M, Nan Y et al (2012) Physiological effects of superoxide dismutase on altered visual function of retinal ganglion cells in db/db mice. PloS One 7:e30343
21. Fuchs H, Gailus-Durner V, Neschen S et al (2012) Innovations in phenotyping of mouse models in the German Mouse Clinic. Mamm Genome 23:611-622
22. Gailus-Durner V, Fuchs H, Becker L et al (2005) Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nat Methods 2:403-404
23. Ly A, Yee P, Vessey KA, Phipps JA, Jobling AI, Fletcher EL (2011) Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress, and neuronal functional loss. Invest Ophthalmol Vis Sci 52:9316-9326
24. Hauck SM, Dietter J, Kramer RL et al (2010) Deciphering membrane-associated molecular processes in target tissue of autoimmune uveitis by label-free quantitative mass spectrometry. Mol Cell Proteomics: MCP 9:2292-2305
25. Vogt A, Fuerholzner B, Kinkl N, Boldt K, Ueffing M (2013) Isotope coded protein labeling coupled immunoprecipitation (ICPL-IP): a novel approach for quantitative protein complex analysis from native tissue. Mol Cell Proteomics 12:1395-1406
26. Chomczynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. BioTech 15(532-534):536-537
27. Sherry DM, Wang MM, Bates J, Frishman LJ (2003) Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465:480-498
28. Quin G, Len AC, Billson FA, Gillies MC (2007) Proteome map of normal rat retina and comparison with the proteome of diabetic rat retina: new insight in the pathogenesis of diabetic retinopathy. Proteomics 7:2636-2650
29. Wang YD, Wu JD, Jiang ZL et al (2007) Comparative proteome analysis of neural retinas from type 2 diabetic rats by two-dimensional electrophoresis. Curr Eye Res 32:891-901
30. Fort PE, Freeman WM, Losiewicz MK, Singh RS, Gardner TW (2009) The retinal proteome in experimental diabetic retinopathy: up-regulation of crystallins and reversal by systemic and periocular insulin. Mol Cell Proteomics: MCP 8:767-779
31. VanGuilder HD, Bixler GV, Kutzler L et al (2011) Multi-modal proteomic analysis of retinal protein expression alterations in a rat model of diabetic retinopathy. PloS One 6:e16271
32. Zhang C, Gehlbach P, Gongora C et al (2005) A potential role for beta- and gamma-crystallins in the vascular remodeling of the eye. Dev Dyn 234:36-47
33. Mao YW, Liu JP, Xiang H, Li DW (2004) Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ 11:512-526
34. Gao BB, Phipps JA, Bursell D, Clermont AC, Feener EP (2009) Angiotensin AT1 receptor antagonism ameliorates murine retinal proteome changes induced by diabetes. J Proteome Res 8:5541-5549
35. Gao BB, Chen X, Timothy N, Aiello LP, Feener EP (2008) Characterization of the vitreous proteome in diabetes without diabetic retinopathy and diabetes with proliferative diabetic retinopathy. J Proteome Res 7:2516-2525
36. Decanini A, Karunadharma PR, Nordgaard CL, Feng X, Olsen TW, Ferrington DA (2008) Human retinal pigment epithelium proteome changes in early diabetes. Diabetologia 51:1051-1061
37. Simo R, Higuera M, Garcia-Ramirez M, Canals F, Garcia-Arumi J, Hernandez C (2008) Elevation of apolipoprotein A-I and apolipoprotein H levels in the vitreous fluid and overexpression in the retina of diabetic patients. Arch Ophthalmol 126:1076-1081
38. Garcia-Ramirez M, Canals F, Hernandez C et al (2007) Proteomic analysis of human vitreous fluid by fluorescence-based difference gel electrophoresis (DIGE): a new strategy for identifying potential candidates in the pathogenesis of proliferative diabetic retinopathy. Diabetologia 50:1294-1303
39. Barber AJ, Antonetti DA, Gardner TW (2000) Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. The Penn State Retina Research Group. Invest Ophthalmol Vis Sci 41:3561-3568
40. Bobbie MW, Roy S, Trudeau K, Munger SJ, Simon AM (2010) Reduced connexin 43 expression and its effect on the development of vascular lesions in retinas of diabetic mice. Invest Ophthalmol Vis Sci 51:3758-3763
41. Hancock HA, Kraft TW (2004) Oscillatory potential analysis and ERGs of normal and diabetic rats. Invest Ophthalmol Vis Sci 45:1002-1008
42. Rodieck RW (1972) Components of the electroretinogram - a reappraisal. Vis Res 12:773-780
43. Labuzek K, Suchy D, Gabryel B, Bielecka A, Liber S, Okopien B (2010) Quantification of metformin by the HPLC method in brain regions, cerebrospinal fluid and plasma of rats treated with lipopolysaccharide. Pharmacol Rep: PR 62:956-965
44. Salceda R, Vilchis C, Coffe V, Hernandez-Munoz R (1998) Changes in the redox state in the retina and brain during the onset of diabetes in rats. Neurochem Res 23:893-897
45. Obrosova IG, Stevens MJ, Lang HJ (2001) Diabetes-induced changes in retinal NAD-redox status: pharmacological modulation and implications for pathogenesis of diabetic retinopathy. Pharmacology 62:172-180
46. Owen MR, Doran E, Halestrap AP (2000) Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 348:607-614
47. Larsen S, Rabol R, Hansen CN, Madsbad S, Helge JW, Dela F (2012) Metformin-treated patients with type 2 diabetes have normal mitochondrial complex I respiration. Diabetologia 55:443-449
48. Bixler GV, Vanguilder HD, Brucklacher RM, Kimball SR, Bronson SK, Freeman WM (2011) Chronic insulin treatment of diabetes does not fully normalize alterations in the retinal transcriptome. BMC Med Genomics 4:40
49. Sjolie AK, Klein R, Porta M et al (2008) Effect of candesartan on progression and regression of retinopathy in type 2 diabetes (DIRECT-Protect 2): a randomised placebo-controlled trial. Lancet 372:1385-1393
50. Matthews DR, Stratton IM, Aldington SJ, Holman RR, Kohner EM (2004) Risks of progression of retinopathy and vision loss related to tight blood pressure control in type 2 diabetes mellitus: UKPDS 69. Arch Ophthalmol 122:1631-1640