Characterization of retinal function and glial cell response in a mouse model of oxygen-induced retinopathy

Journal of Comparative Neurology

Volumn 519, Issue 3, 2011, Pages 506-527

  Vessey, K A ^a   Wilkinson Berka, J L ^b   Fletcher, E L ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Electroretinogram (ERG); Hypoxia; Microglia; M ller cell; Neovascularization; Retinopathy of prematurity

Indexed keywords

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL LOSS; CONTROLLED STUDY; ELECTRORETINOGRAM; FUNCTIONAL ASSESSMENT; GLIA CELL; MICROGLIA; MOUSE; MUELLER CELL; NERVE CELL; NERVOUS SYSTEM FUNCTION; NONHUMAN; PHOTORECEPTOR OUTER SEGMENT; PRIORITY JOURNAL; RETINA CONE; RETINA ROD; RETINOPATHY; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; MICE; MICE, INBRED C57BL; NEUROGLIA; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; RETINOPATHY OF PREMATURITY;

EID: 78650661723     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22530     Document Type: Article

References (56)

1. Abercrombie M, Johnson ML. 1946. Quantitative histology of Wallerian degeneration: I. Nuclear population in rabbit sciatic nerve. J Anat 80: 37-50.
2. Asnaghi V, Gerhardinger C, Hoehn T, Adeboje A, Lorenzi M. 2003. A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat. Diabetes 52: 506-511.
3. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, Hubbard WC, Calkins DJ, Horner PJ, Vetter ML. 2008. Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 49: 1437-1446.
4. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A. 2006. Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25: 397-424.
5. Bringmann A, Pannicke T, Biedermann B, Francke M, Iandiev I, Grosche J, Wiedemann P, Albrecht J, Reichenbach A. 2009. Role of retinal glial cells in neurotransmitter uptake and metabolism. Neurochem Int 54: 143-160.
6. Chan-Ling T, Tout S, Hollander H, Stone J. 1992. Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 33: 2128-2147.
7. Chan-Ling T, Gock B, Stone J. 1995. The effect of oxygen on vasoformative cell division. Evidence that 'physiological hypoxia' is the stimulus for normal retinal vasculogenesis. Invest Ophthalmol Vis Sci 36: 1201-214.
8. Checchin D, Sennlaub F, Levavasseur E, Leduc M, Chemtob S. 2006. Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci 47: 3595-3602.
9. Chen H, Weber AJ. 2002. Expression of glial fibrillary acidic protein and glutamine synthetase by Muller cells after optic nerve damage and intravitreal application of brain-derived neurotrophic factor. Glia 38: 115-125.
10. Cho EY, Choi HL, Chan FL. 2002. Expression pattern of glycoconjugates in rat retina as analysed by lectin histochemistry. Histochem J 34: 589-600.
11. Dembinska O, Rojas LM, Chemtob S, Lachapelle P. 2002. Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 43: 2481-2490.
12. Dorrell MI, Aguilar E, Jacobson R, Trauger SA, Friedlander J, Siuzdak G, Friedlander M. 2010. Maintaining retinal astrocytes normalizes revascularization and prevents vascular pathology associated with oxygen-induced retinopathy. Glia 2010 58: 43-54.
13. Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. 2007. Neuronal and glial cell changes are determined by retinal vascularization in retinopathy of prematurity. J Comp Neurol 504: 404-417.
14. Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. 2008. AT1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy. Glia 56: 1076-1090.
15. Eichler W, Yafai Y, Keller T, Wiedemann P, Reichenbach A. 2004. PEDF derived from glial Muller cells: a possible regulator of retinal angiogenesis. Exp Cell Res 299: 68-78.
16. Eisenfeld AJ, Bunt-Milam AH, Sarthy PV. 1984. Muller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Invest Ophthalmol Vis Sci 25: 1321-1328.
17. Fei Y. 2003. Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. Mol Vis 9: 31-42.
18. Fulton AB, Hansen RM. 2000. The development of scotopic sensitivity. Invest Ophthalmol Vis Sci 41: 1588-1596.
19. Fulton AB, Rushton WA. 1978. The human rod ERG: correlation with psychophysical responses in light and dark adaptation. Vis Res 18: 793-800.
20. Fulton AB, Reynaud X, Hansen RM, Lemere CA, Parker C, Williams TP. 1999. Rod photoreceptors in infant rats with a history of oxygen exposure. Invest Ophthalmol Vis Sci 40: 168-174.
21. Fulton AB, Hansen RM, Petersen RA, Vanderveen DK. 2001. The rod photoreceptors in retinopathy of prematurity: an electroretinographic study. Arch Ophthalmol 119: 499-505.
22. Fulton AB, Hansen RM, Moskowitz A. 2008. The cone electroretinogram in retinopathy of prematurity. Invest Ophthalmol Vis Sci 49: 814-819.
23. Fulton AB, Hansen RM, Moskowitz A, Akula JD. 2009. The neurovascular retina in retinopathy of prematurity. Prog Retin Eye Res 28: 452-482.
24. Goodyear MJ, Crewther SG, Junghans BM. 2009. A role for aquaporin-4 in fluid regulation in the inner retina. Vis Neurosci 26: 159-165.
25. Guillery RW, Herrup K. 1997. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol 386: 2-7.
26. Hageman GS, Johnson LV. 1986. Biochemical characterization of the major peanut-agglutinin-binding glycoproteins in vertebrate retinae. J Comp Neurol 249: 499-510, 482-493.
27. Hood DC, Birch DG. 1990. The A-wave of the human electroretinogram and rod receptor function. Invest Ophthalmol Vis Sci 31: 2070-2081.
28. Hughes S, Gardiner T, Hu P, Baxter L, Rosinova E, Chan-Ling T. 2006. Altered pericyte-endothelial relations in the rat retina during aging: implications for vessel stability. Neurobiol Aging 27: 1838-1847.
29. Iandiev I, Pannicke T, Hollborn M, Wiedemann P, Reichenbach A, Grimm C, Reme CE, Bringmann A. 2008. Localization of glial aquaporin-4 and Kir4.1 in the light-injured murine retina. Neurosci Lett 434: 317-321.
30. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. 1998. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res 57: 1-9.
31. Kaur C, Foulds WS, Ling EA. 2008. Blood-retinal barrier in hypoxic ischaemic conditions: basic concepts, clinical features and management. Prog Retin Eye Res 27: 622-647.
32. Liu K, Akula JD, Falk C, Hansen RM, Fulton AB. 2006. The retinal vasculature and function of the neural retina in a rat model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 47: 2639-2647.
33. Lundkvist A, Reichenbach A, Betsholtz C, Carmeliet P, Wolburg H, Pekny M. 2004. Under stress, the absence of intermediate filaments from Muller cells in the retina has structural and functional consequences. J Cell Sci 117: 3481-3488.
34. Lynch MA. 2009. The multifaceted profile of activated microglia. Mol Neurobiol 40: 139-156.
35. Lyubarsky AL, Pugh EN Jr. 1996. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci 16: 563-571.
36. Naka KI, Rushton WA. 1966. S-potentials from luminosity units in the retina of fish (Cyprinidae). J Physiol 185: 587-599.
37. 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.
38. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145: 61-83.
39. Ransohoff RM, Perry VH. 2009. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27: 119-145.
40. Reynaud X, Hansen RM, Fulton AB. 1995. Effect of prior oxygen exposure on the electroretinographic responses of infant rats. Invest Ophthalmol Vis Sci 36: 2071-2079.
41. Ritter MR, Banin E, Moreno SK, Aguilar E, Dorrell MI, Friedlander M. 2006. Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest 116: 3266-3276.
42. Smith LE, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R, D'Amore PA. 1994. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35: 101-111.
43. Stone J, Itin A, Alon T, Peéer J, Gnessin H, Chan-Ling T, Keshet E. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15: 4738-4747.
44. Tanihara H, Hangai M, Sawaguchi S, Abe H, Kageyama M, Nakazawa F, Shirasawa E, Honda Y. 1997. Up-regulation of glial fibrillary acidic protein in the retina of primate eyes with experimental glaucoma. Arch Ophthalmol 115: 752-756.
45. Tyler NK, Burns MS. 1991. Comparison of lectin reactivity in the vessel beds of the rat eye. Curr Eye Res 10: 801-810.
46. van Wijngaarden P, Brereton HM, Gibbins IL, Coster DJ, Williams KA. 2007. Kinetics of strain-dependent differential gene expression in oxygen-induced retinopathy in the rat. Exp Eye Res 85: 508-517.
47. Verardo MR, Lewis GP, Takeda M, Linberg KA, Byun J, Luna G, Wilhelmsson U, Pekny M, Chen DF, Fisher SK. 2008. Abnormal reactivity of muller cells after retinal detachment in mice deficient in GFAP and vimentin. Invest Ophthalmol Vis Sci 49: 3659-3665.
48. Vinores SA, Xiao WH, Aslam S, Shen J, Oshima Y, Nambu H, Liu H, Carmeliet P, Campochiaro PA. 2006. Implication of the hypoxia response element of the Vegf promoter in mouse models of retinal and choroidal neovascularization, but not retinal vascular development. J Cell Physiol 206: 749-758.
49. Wachtmeister L. 1998. Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res 17: 485-521.
50. Ward MM, Jobling AI, Kalloniatis M, Fletcher EL. 2005. Glutamate uptake in retinal glial cells during diabetes. Diabetologia 48: 351-360.
51. Ward MM, Puthussery T, Fletcher EL. 2008. Localization and possible function of P2Y(4) receptors in the rodent retina. Neuroscience 155: 1262-1274.
52. Weymouth AE, Vingrys AJ. 2008. Rodent electroretinography: methods for extraction and interpretation of rod and cone responses. Prog Retin Eye Res 27: 1-44.
53. Wilkinson-Berka JL, Alousis NS, Kelly DJ, Gilbert RE. 2003. COX-2 inhibition and retinal angiogenesis in a mouse model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 44: 974-979.
54. Woldemussie E, Wijono M, Ruiz G. 2004. Muller cell response to laser-induced increase in intraocular pressure in rats. Glia 47: 109-119.
55. Zhang Y, Stone J. 1997. Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38: 1653-1666.
56. Zhao L, Ma W, Fariss RN, Wong WT. 2009. Retinal vascular repair and neovascularization are not dependent on CX3CR1 signaling in a model of ischemic retinopathy. Exp Eye Res 88: 1004-1013.