Retinopathy is reduced during experimental diabetes in a mouse model of outer retinal degeneration

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 12, 2006, Pages 5561-5568

  De Gooyer, Tanyth E ^a   Stevenson, Kathryn A ^a   Humphries, Pete ^b   Simpson, David A C ^a   Gardiner, Tom A ^a   Stitt, Alan W ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; GLYCOSYLATED HEMOGLOBIN; MESSENGER RNA; PARAFFIN; PIMONIDAZOLE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A; APYRASE; RHODOPSIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; C57BL 6 MOUSE; CONTROLLED STUDY; DIABETIC RETINOPATHY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION; HYPERGLYCEMIA; HYPOXIA; MALE; MICROVASCULATURE; MOUSE; MOUSE STRAIN; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RETINA DEGENERATION; RETINOPATHY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; ANIMAL; ANOXIA; C57BL MOUSE; CYTOCHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINA BLOOD VESSEL; RETINITIS PIGMENTOSA; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOXIA; APYRASE; BASEMENT MEMBRANE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOSYLATION END PRODUCTS, ADVANCED; HEMOGLOBIN A, GLYCOSYLATED; HISTOCYTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RETINAL VESSELS; RETINITIS PIGMENTOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHODOPSIN; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 34248215127     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.06-0647     Document Type: Article

References (50)

1. Hammes HP. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res. 2005;37(suppl 1):39-43.
2. Lorenzi M, Gerhardinger C. Early cellular and molecular changes induced by diabetes in the retina. Diabetologia. 2001;44:791-804.
3. Fong DS, Aiello L, Gardner TW, et al. Retinopathy in diabetes. Diabetes Care. 2004;27(suppl 1):S84-S87.
4. Arden GB, Wolf JE, Tsang Y. Does dark adaptation exacerbate diabetic retinopathy? - evidence and a linking hypothesis. Vision Res. 1998;38:1723-1729.
5. Arden GB. The absence of diabetic retinopathy in patients with retinitis pigmentosa: implications for pathophysiology and possible treatment. Br J Ophthalmol. 2001;85:366-370.
6. Sternberg P Jr., Landers MB 3rd, Wolbarsht M. The negative coincidence of retinitis pigmentosa and proliferative diabetic retinopathy. Am J Ophthalmol. 1984;97:788-789.
7. Lahdenranta J, Pasqualini R, Schlingemann RO, et al. An anti-angiogenic state in mice and humans with retinal photoreceptor cell degeneration. Proc Natl Acad Sci USA. 2001;98:10368-10373.
8. Penn JS, Li S, Naash MI. Ambient hypoxia reverses retinal vascular attenuation in a transgenic mouse model of autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2000;41:4007-4013.
9. Arden GB, Sidman RL, Arap W, Schlingemann RO. Spare the rod and spoil the eye. Br J Ophthalmol. 2005;89:764-769.
10. Braun RD, Linsenmeier RA, Goldstick TK. Oxygen consumption in the inner and outer retina of the cat. Invest Ophthalmol Vis Sci. 1995;36:542-554.
11. -/- mice reduces retinal hypoxia and hypoxia-related gene expression. Invest Ophthalmol Vis Sci. 2006;47: 5553-5560.
12. Linsenmeier RA, Braun RD, McRipley MA, et al. Retinal hypoxia in long-term diabetic cats. Invest Ophthalmol Vis Sci. 1998;39:1647-1657.
13. Humphries MM, Rancourt D, Farrar GJ, et al. Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat Genet. 1997;15:216-219.
14. Cox OT, Simpson DA, Stitt AW, Gardiner TA. Sources of pdgf expression in murine retina and the effect of short-term diabetes. Mol Vis. 2003;9:665-672.
15. Gardiner TA, Gibson DS, de Gooyer TE, de la Cruz VF, McDonald DM, Stitt AW. Inhibition of tumor necrosis factor-alpha improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am J Pathol. 2005;166:637-644.
16. Raleigh JA, Koch CJ. Importance of thiols in the reductive binding of 2-nitroimidazoles to macromolecules. Biochem Pharmacol. 1990;40:2457-2464.
17. Raleigh JA, La Dine JK, Cline JM, Thrall DE. An enzyme-linked immunosorbent assay for hypoxia marker binding in tumours. Br J Cancer. 1994;69:66-71.
18. Lau J, Borjesson A, Holstad M, Sandler S. Prolactin regulation of the expression of TNF-alpha, IFN-gamma and il-10 by splenocytes in murine multiple low dose streptozotocin diabetes. Immunol Lett. 2006;102:25-30.
19. Nishikawa T, Giardino I, Edelstein D, Brownlee M. Changes in diabetic retinal matrix protein mRNA levels in a common transgenic mouse strain. Curr Eye Res. 2000;21:581-587.
20. Simpson DA, Feeney S, Boyle C, Stitt AW. Retinal VEGF mRNA measured by SYBR I green fluorescence: a versatile approach to quantitative PCR. Mol Vis. 2000;6:178-183.
21. Feeney SA, Simpson DA, Gardiner TA, Boyle C, Jamison P, Stitt AW. Role of vascular endothelial growth factor and placental growth factors during retinal vascular development and hyaloid regression. Invest Ophthalmol Vis Sci. 2003;44:839-847.
22. Morrison TB, Weis JJ, Wittwer CT. Quantification of low-copy transcripts by continuous SYBR green I monitoring during amplification. BioTechniques. 1998;24:954-958,960,962.
23. Higuchi R, Fockler C, Dollinger G, Watson R. Kinetic per analysis: Real-time monitoring of DNA amplification reactions. BioTechnology (NY). 1993;11:1026-1030.
24. Lutty GA, McLeod DS. Phosphatase enzyme histochemistry for studying vascular hierarchy, pathology, and endothelial cell dysfunction in retina and choroid. Vision Res. 2005;45:3504-3511.
25. Johnson MA, Lutty GA, McLeod DS, et al. Ocular structure and function in an aged monkey with spontaneous diabetes mellitus. Exp Eye Res. 2005;80:37-42.
26. Kim SY, Johnson MA, McLeod DS, et al. Retinopathy in monkeys with spontaneous type 2 diabetes. Invest Ophthalmol Vis Sci. 2004;45:4543-4553.
27. Stitt A, Gardiner TA, Alderson NL, et al. The age inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes. Diabetes. 2002;51:2826-2832.
28. Yu DY, Cringle SJ, Su EN, Yu PK. Intraretinal oxygen levels before and after photoreceptor loss in the res rat. Invest Ophthalmol Vis Sci. 2000;41:3999-4006.
29. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol. 1994;118:445-450.
30. Gerhardinger C, Brown LF, Roy S, Mizutani M, Zucker CL, Lorenzi M. Expression of vascular endothelial growth factor in the human retina and in nonproliferative diabetic retinopathy. Am J Pathol. 1998;152:1453-1462.
31. Vinores SA, Youssri AI, Luna JD, et al. Upregulation of vascular endothelial growth factor in ischemic and non-ischemic human and experimental retinal disease. Histol Histopathol. 1997;12:99-109.
32. Engerman RL, Kern TS. Retinopathy in animal models of diabetes. Diabetes Metab Rev. 1995;11:109-120.
33. Hammes HP, Lin J, Bretzel RG, Brownlee M, Breier G. Upregulation of the vascular endothelial growth factor/vascular endothelial growth factor receptor system in experimental background diabetic retinopathy of the rat. Diabetes. 1998;47:401-406.
34. Joussen AM, Huang S, Poulaki V, et al. In vivo retinal gene expression in early diabetes. Invest Ophthalmol Vis Sci. 2001;42:3047-3057.
35. Simpson DA, Murphy GM, Bhaduri T, Gardiner TA, Archer DB, Stitt AW. Expression of the VEGF gene family during retinal vasoobliteration and hypoxia. Biochem Biophys Res Commun. 1999; 262:333-340.
36. Stitt AW, Simpson DA, Boocock C, Gardiner TA, Murphy GM, Archer DB. Expression of vascular endothelial growth factor (VEGF) and its receptors is regulated in eyes with intra-ocular tumours. J Pathol. 1998;186:306-312.
37. Agardh E, Bruun A, Agardh CD. Retinal glial cell immunoreactivity and neuronal cell changes in rats with STZ-induced diabetes. Curr Eye Res. 2001;23:276-284.
38. Winkler BS, Starnes CA, Sauer MW, Firouzgan Z, Chen SC. Cultured retinal neuronal cells and Muller cells both show net production of lactate. Neurochem Int. 2004;45:311-320.
39. Dalton SJ, Mitchell DC, Whiting CV, Tarlton JF. Abnormal extracellular matrix metabolism in chronically ischemic skin: a mechanism for dermal failure in leg ulcers. J Invest Dermatol. 2005;125: 373-379.
40. Norman JT, Orphanides C, Garcia P, Fine LG. Hypoxia-induced changes in extracellular matrix metabolism in renal cells. Exp Nephrol. 1999;7:463-469.
41. Chen YF, Feng JA, Li P, et al. Dominant negative mutation of the tgf-beta receptor blocks hypoxia-induced pulmonary vascular remodeling. J Appl Physiol. 2006;100:564-571.
42. 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.
43. Park SH, Park JW, Park SJ, et al. Apoptotic death of photoreceptors in the streptozotocin-induced diabetic rat retina. Diabetologia. 2003;46:1260-1268.
44. Hancock HA, Kraft TW. Oscillatory potential analysis and ergs of normal and diabetic rats. Invest Ophthalmol Vis Sci. 2004;45: 1002-1008.
45. Fortune B, Schneck ME, Adams AJ. Multifocal electroretinogram delays reveal local retinal dysfunction in early diabetic retinopathy. Invest Ophthalmol Vis Sci. 1999;40:2638-2651.
46. Ewing FM, Deary IJ, Strachan MW, Frier BM. Seeing beyond retinopathy in diabetes: electrophysiological and psychophysical abnormalities and alterations in vision. Endocr Rev. 1998;19:462-476.
47. Jackson GR, Owsley C. Visual dysfunction, neurodegenerative diseases, and aging. Neurol Clin. 2003;21:709-728.
48. Li H, Telemaque S, Miller RE, Marsh JD. High glucose inhibits apoptosis induced by serum deprivation in vascular smooth muscle cells via upregulation of bcl-2 and bcl-xl. Diabetes. 2005;54: 540-545.
49. Levin LA, Schlamp CL, Spieldoch RL, Geszvain KM, Nickells RW. Identification of the bcl-2 family of genes in the rat retina. Invest Ophthalmol Vis Sci. 1997;38:2545-2553.
50. Tsang SH, Chen J, Kjeldbye H, et al. Retarding photoreceptor degeneration in pdegtm1/pdegtml mice by an apoptosis suppressor gene. Invest Ophthalmol Vis Sci. 1997;38:943-950.