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Published in: Documenta Ophthalmologica 1/2010

01-02-2010 | Review Article

The significance of neuronal and glial cell changes in the rat retina during oxygen-induced retinopathy

Authors: Erica L. Fletcher, Laura E. Downie, Kate Hatzopoulos, Kirstan A. Vessey, Michelle M. Ward, Chee L. Chow, Michael J. Pianta, Algis J. Vingrys, Michael Kalloniatis, Jennifer L. Wilkinson-Berka

Published in: Documenta Ophthalmologica | Issue 1/2010

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Abstract

Retinopathy of prematurity is a devastating vascular disease of premature infants. A number of studies indicate that retinal function is affected in this disease. Using the rat model of oxygen-induced retinopathy, it is possible to explore more fully the complex relationship between neuronal, glial and vascular pathology in this condition. This review examines the structural and functional changes that occur in the rat retina following oxygen-induced retinopathy. We highlight that vascular pathology in rats is characterized by aberrant growth of blood vessels into the vitreous at the expense of blood vessel growth into the body of the retina. Moreover, amino acid neurochemistry, a tool for examining neuronal changes in a spatially complete manner reveals widespread changes in amacrine and bipolar cells. In addition, neurochemical anomalies within inner retinal neurons are highly correlated with the absence of retinal vessels. The key cell types that link blood flow with neuronal function are macroglia. Macroglia cells, which in the retina include astrocytes and Müller cells, are affected by oxygen-induced retinopathy. Astrocyte loss occurs in the peripheral retina, while Müller cells show signs of reactive gliosis that is highly localized to regions that are devoid of intraretinal blood vessels. Finally, we propose that treatments, such as blockade of the renin–angiotensin system, that not only targets pathological angiogenesis, but that also promotes re-vascularization of the retina are likely to prove important in the treatment of those with retinopathy of prematurity.
Literature
1.
go back to reference Good WV, Hardy RJ, Dobson V, Palmer EA, Phelps DL, Quintos M et al (2005) The incidence and course of retinopathy of prematurity: findings from the early treatment for retinopathy of prematurity study. Pediatrics 116(1):15–23PubMedCrossRef Good WV, Hardy RJ, Dobson V, Palmer EA, Phelps DL, Quintos M et al (2005) The incidence and course of retinopathy of prematurity: findings from the early treatment for retinopathy of prematurity study. Pediatrics 116(1):15–23PubMedCrossRef
2.
go back to reference O’Connor AR, Stephenson T, Johnson A, Tobin MJ, Moseley MJ, Ratib S et al (2002) Long-term ophthalmic outcome of low birth weight children with and without retinopathy of prematurity. Pediatrics 109(1):12–18PubMedCrossRef O’Connor AR, Stephenson T, Johnson A, Tobin MJ, Moseley MJ, Ratib S et al (2002) Long-term ophthalmic outcome of low birth weight children with and without retinopathy of prematurity. Pediatrics 109(1):12–18PubMedCrossRef
3.
go back to reference Slidsborg C, Olesen HB, Jensen PK, Jensen H, Nissen KR, Greisen G et al (2008) Treatment for retinopathy of prematurity in Denmark in a ten-year period (1996–2005): is the incidence increasing? Pediatrics 121(1):97–105PubMedCrossRef Slidsborg C, Olesen HB, Jensen PK, Jensen H, Nissen KR, Greisen G et al (2008) Treatment for retinopathy of prematurity in Denmark in a ten-year period (1996–2005): is the incidence increasing? Pediatrics 121(1):97–105PubMedCrossRef
4.
go back to reference Barnaby AM, Hansen RM, Moskowitz A, Fulton AB (2007) Development of scotopic visual thresholds in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48(10):4854–4860PubMedCrossRef Barnaby AM, Hansen RM, Moskowitz A, Fulton AB (2007) Development of scotopic visual thresholds in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48(10):4854–4860PubMedCrossRef
5.
go back to reference Fulton AB, Hansen RM (1996) Photoreceptor function in infants and children with a history of mild retinopathy of prematurity. J Opt Soc Am 13(3):566–571CrossRef Fulton AB, Hansen RM (1996) Photoreceptor function in infants and children with a history of mild retinopathy of prematurity. J Opt Soc Am 13(3):566–571CrossRef
6.
go back to reference Fulton AB, Hansen RM, Petersen RA, Vanderveen DK (2001) The rod photoreceptors in retinopathy of prematurity: an electroretinographic study. Arch Ophthalmol 119(4):499–505PubMed Fulton AB, Hansen RM, Petersen RA, Vanderveen DK (2001) The rod photoreceptors in retinopathy of prematurity: an electroretinographic study. Arch Ophthalmol 119(4):499–505PubMed
7.
go back to reference Akula JD, Hansen RM, Martinez-Perez ME, Fulton AB (2007) Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48(9):4351–4359PubMedCrossRef Akula JD, Hansen RM, Martinez-Perez ME, Fulton AB (2007) Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48(9):4351–4359PubMedCrossRef
8.
go back to reference 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(6):2639–2647PubMedCrossRef 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(6):2639–2647PubMedCrossRef
9.
go back to reference Ames A 3rd, Li YY, Heher EC, Kimble CR (1992) Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J Neurosci 12(3):840–853PubMed Ames A 3rd, Li YY, Heher EC, Kimble CR (1992) Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J Neurosci 12(3):840–853PubMed
10.
go back to reference Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN et al (2006) Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25(4):397–424PubMedCrossRef Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN et al (2006) Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25(4):397–424PubMedCrossRef
11.
go back to reference Dorrell MI, Friedlander M (2006) Mechanisms of endothelial cell guidance and vascular patterning in the developing mouse retina. Prog Retin Eye Res 25(3):277–295PubMedCrossRef Dorrell MI, Friedlander M (2006) Mechanisms of endothelial cell guidance and vascular patterning in the developing mouse retina. Prog Retin Eye Res 25(3):277–295PubMedCrossRef
12.
go back to reference Anderson CM, Nedergaard M (2003) Astrocyte-mediated control of cerebral microcirculation. Trends Neurosci 26(7):340–344 author reply 4–5PubMedCrossRef Anderson CM, Nedergaard M (2003) Astrocyte-mediated control of cerebral microcirculation. Trends Neurosci 26(7):340–344 author reply 4–5PubMedCrossRef
13.
go back to reference Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26(11):2862–2870PubMedCrossRef Metea MR, Newman EA (2006) Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J Neurosci 26(11):2862–2870PubMedCrossRef
14.
go back to reference Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431(7005):195–199PubMedCrossRef Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431(7005):195–199PubMedCrossRef
15.
go back to reference Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387–1394PubMedCrossRef Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10(11):1387–1394PubMedCrossRef
16.
go back to reference 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(8):3595–3602PubMedCrossRef 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(8):3595–3602PubMedCrossRef
17.
go back to reference Davies MH, Eubanks JP, Powers MR (2006) Microglia and macrophages are increased in response to ischemia-induced retinopathy in the mouse retina. Mol Vis 12:467–477PubMed Davies MH, Eubanks JP, Powers MR (2006) Microglia and macrophages are increased in response to ischemia-induced retinopathy in the mouse retina. Mol Vis 12:467–477PubMed
18.
go back to reference 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(6):1004–1013PubMedCrossRef 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(6):1004–1013PubMedCrossRef
19.
go back to reference Lutty GA, Chan-Ling T, Phelps DL, Adamis AP, Berns KI, Chan CK et al (2006) Proceedings of the third international symposium on retinopathy of prematurity: an update on ROP from the lab to the nursery (November 2003, Anaheim, California). Mol Vis 12:532–580PubMed Lutty GA, Chan-Ling T, Phelps DL, Adamis AP, Berns KI, Chan CK et al (2006) Proceedings of the third international symposium on retinopathy of prematurity: an update on ROP from the lab to the nursery (November 2003, Anaheim, California). Mol Vis 12:532–580PubMed
20.
go back to reference Penn JS, Henry MM, Wall PT, Tolman BL (1995) The range of PaO2 variation determines the severity of oxygen-induced retinopathy in newborn rats. Invest Ophthalmol Vis Sci 36(10):2063–2070PubMed Penn JS, Henry MM, Wall PT, Tolman BL (1995) The range of PaO2 variation determines the severity of oxygen-induced retinopathy in newborn rats. Invest Ophthalmol Vis Sci 36(10):2063–2070PubMed
21.
go back to reference Penn JS, Tolman BL, Lowery LA, Koutz CA (1992) Oxygen-induced retinopathy in the rat: hemorrhages and dysplasias may lead to retinal detachment. Curr Eye Res 11(10):939–953PubMedCrossRef Penn JS, Tolman BL, Lowery LA, Koutz CA (1992) Oxygen-induced retinopathy in the rat: hemorrhages and dysplasias may lead to retinal detachment. Curr Eye Res 11(10):939–953PubMedCrossRef
22.
go back to reference Penn JS, Tolman BL, Henry MM (1994) Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci 35(9):3429–3435PubMed Penn JS, Tolman BL, Henry MM (1994) Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci 35(9):3429–3435PubMed
23.
go back to reference van Wijngaarden P, Brereton HM, Coster DJ, Williams KA (2007) Genetic influences on susceptibility to oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 48(4):1761–1766PubMedCrossRef van Wijngaarden P, Brereton HM, Coster DJ, Williams KA (2007) Genetic influences on susceptibility to oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 48(4):1761–1766PubMedCrossRef
24.
go back to reference 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(4):508–517PubMedCrossRef 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(4):508–517PubMedCrossRef
25.
go back to reference Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL et al (2001) Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci USA 98(10):5804–5808PubMedCrossRef Hellstrom A, Perruzzi C, Ju M, Engstrom E, Hard AL, Liu JL et al (2001) Low IGF-I suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci USA 98(10):5804–5808PubMedCrossRef
26.
go back to reference Oshima Y, Oshima S, Nambu H, Kachi S, Takahashi K, Umeda N et al (2005) Different effects of angiopoietin-2 in different vascular beds: new vessels are most sensitive. FASEB J 19(8):963–965PubMed Oshima Y, Oshima S, Nambu H, Kachi S, Takahashi K, Umeda N et al (2005) Different effects of angiopoietin-2 in different vascular beds: new vessels are most sensitive. FASEB J 19(8):963–965PubMed
27.
go back to reference Xia XB, Xiong SQ, Song WT, Luo J, Wang YK, Zhou RR (2008) Inhibition of retinal neovascularization by siRNA targeting VEGF(165). Mol Vis 14:1965–1973PubMed Xia XB, Xiong SQ, Song WT, Luo J, Wang YK, Zhou RR (2008) Inhibition of retinal neovascularization by siRNA targeting VEGF(165). Mol Vis 14:1965–1973PubMed
28.
go back to reference 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(10):1076–1090PubMedCrossRef 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(10):1076–1090PubMedCrossRef
29.
go back to reference Provis JM (2001) Development of the primate retinal vasculature. Prog Retin Eye Res 20(6):799–821PubMedCrossRef Provis JM (2001) Development of the primate retinal vasculature. Prog Retin Eye Res 20(6):799–821PubMedCrossRef
30.
go back to reference Dorrell MI, Aguilar E, Friedlander M (2002) Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci 43(11):3500–3510PubMed Dorrell MI, Aguilar E, Friedlander M (2002) Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci 43(11):3500–3510PubMed
31.
go back to reference Fruttiger M, Calver AR, Kruger WH, Mudhar HS, Michalovich D, Takakura N et al (1996) PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17(6):1117–1131PubMedCrossRef Fruttiger M, Calver AR, Kruger WH, Mudhar HS, Michalovich D, Takakura N et al (1996) PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17(6):1117–1131PubMedCrossRef
32.
go back to reference Stone J, Itin A, Alon T, Pe’er J, Gnessin H, Chan-Ling T et al (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15(7 Pt 1):4738–4747PubMed Stone J, Itin A, Alon T, Pe’er J, Gnessin H, Chan-Ling T et al (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15(7 Pt 1):4738–4747PubMed
33.
go back to reference Stone J, Chan-Ling T, Pe’er J, Itin A, Gnessin H, Keshet E (1996) Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37(2):290–299PubMed Stone J, Chan-Ling T, Pe’er J, Itin A, Gnessin H, Keshet E (1996) Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 37(2):290–299PubMed
34.
go back to reference Palmer EA, Hardy RJ, Dobson V, Phelps DL, Quinn GE, Summers CG et al (2005) 15-year outcomes following threshold retinopathy of prematurity: final results from the multicenter trial of cryotherapy for retinopathy of prematurity. Arch Ophthalmol 123(3):311–318PubMedCrossRef Palmer EA, Hardy RJ, Dobson V, Phelps DL, Quinn GE, Summers CG et al (2005) 15-year outcomes following threshold retinopathy of prematurity: final results from the multicenter trial of cryotherapy for retinopathy of prematurity. Arch Ophthalmol 123(3):311–318PubMedCrossRef
35.
go back to reference Reisner DS, Hansen RM, Findl O, Petersen RA, Fulton AB (1997) Dark-adapted thresholds in children with histories of mild retinopathy of prematurity. Invest Ophthalmol Vis Sci 38(6):1175–1183PubMed Reisner DS, Hansen RM, Findl O, Petersen RA, Fulton AB (1997) Dark-adapted thresholds in children with histories of mild retinopathy of prematurity. Invest Ophthalmol Vis Sci 38(6):1175–1183PubMed
36.
go back to reference Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20(3):351–384PubMedCrossRef Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20(3):351–384PubMedCrossRef
37.
go back to reference Mills SL, Massey SC (1999) AII amacrine cells limit scotopic acuity in central macaque retina: a confocal analysis of calretinin labeling. J Comp Neurol 411(1):19–34PubMedCrossRef Mills SL, Massey SC (1999) AII amacrine cells limit scotopic acuity in central macaque retina: a confocal analysis of calretinin labeling. J Comp Neurol 411(1):19–34PubMedCrossRef
38.
go back to reference Weymouth AE, Vingrys AJ (2008) Rodent electroretinography: methods for extraction and interpretation of rod and cone responses. Prog Retin Eye Res 27(1):1–44PubMedCrossRef Weymouth AE, Vingrys AJ (2008) Rodent electroretinography: methods for extraction and interpretation of rod and cone responses. Prog Retin Eye Res 27(1):1–44PubMedCrossRef
39.
go back to reference Akula JD, Mocko JA, Moskowitz A, Hansen RM, Fulton AB (2007) The oscillatory potentials of the dark-adapted electroretinogram in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48(12):5788–5797PubMedCrossRef Akula JD, Mocko JA, Moskowitz A, Hansen RM, Fulton AB (2007) The oscillatory potentials of the dark-adapted electroretinogram in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48(12):5788–5797PubMedCrossRef
40.
go back to reference Fulton AB, Hansen RM, Moskowitz A, Barnaby AM (2005) Multifocal ERG in subjects with a history of retinopathy of prematurity. Doc Ophthalmol 111(1):7–13PubMedCrossRef Fulton AB, Hansen RM, Moskowitz A, Barnaby AM (2005) Multifocal ERG in subjects with a history of retinopathy of prematurity. Doc Ophthalmol 111(1):7–13PubMedCrossRef
41.
go back to reference Reynaud X, Hansen RM, Fulton AB (1995) Effect of prior oxygen exposure on the electroretinographic responses of infant rats. Invest Ophthalmol Vis Sci 36(10):2071–2079PubMed Reynaud X, Hansen RM, Fulton AB (1995) Effect of prior oxygen exposure on the electroretinographic responses of infant rats. Invest Ophthalmol Vis Sci 36(10):2071–2079PubMed
42.
go back to reference Daniele LL, Sauer B, Gallagher SM, Pugh EN Jr, Philp NJ (2008) Altered visual function in monocarboxylate transporter 3 (Slc16a8) knockout mice. Am J Physiol 295(2):C451–C457CrossRef Daniele LL, Sauer B, Gallagher SM, Pugh EN Jr, Philp NJ (2008) Altered visual function in monocarboxylate transporter 3 (Slc16a8) knockout mice. Am J Physiol 295(2):C451–C457CrossRef
43.
go back to reference Yu DY, Cringle SJ (2001) Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog Retin Eye Res 20(2):175–208PubMedCrossRef Yu DY, Cringle SJ (2001) Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog Retin Eye Res 20(2):175–208PubMedCrossRef
44.
go back to reference Cringle SJ, Yu PK, Su EN, Yu DY (2006) Oxygen distribution and consumption in the developing rat retina. Invest Ophthalmol Vis Sci 47(9):4072–4076PubMedCrossRef Cringle SJ, Yu PK, Su EN, Yu DY (2006) Oxygen distribution and consumption in the developing rat retina. Invest Ophthalmol Vis Sci 47(9):4072–4076PubMedCrossRef
45.
go back to reference 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(4):480–498PubMedCrossRef 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(4):480–498PubMedCrossRef
46.
go back to reference Fulton AB, Hansen RM, Moskowitz A (2008) The cone electroretinogram in retinopathy of prematurity. Invest Ophthalmol Vis Sci 49(2):814–819PubMedCrossRef Fulton AB, Hansen RM, Moskowitz A (2008) The cone electroretinogram in retinopathy of prematurity. Invest Ophthalmol Vis Sci 49(2):814–819PubMedCrossRef
47.
go back to reference Lachapelle P, Dembinska O, Rojas LM, Benoit J, Almazan G, Chemtob S (1999) Persistent functional and structural retinal anomalies in newborn rats exposed to hyperoxia. Can J Physiol Pharmacol 77(1):48–55PubMedCrossRef Lachapelle P, Dembinska O, Rojas LM, Benoit J, Almazan G, Chemtob S (1999) Persistent functional and structural retinal anomalies in newborn rats exposed to hyperoxia. Can J Physiol Pharmacol 77(1):48–55PubMedCrossRef
48.
go back to reference Dembinska O, Rojas LM, Varma DR, Chemtob S, Lachapelle P (2001) Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats. Invest Ophthalmol Vis Sci 42(5):1111–1118PubMed Dembinska O, Rojas LM, Varma DR, Chemtob S, Lachapelle P (2001) Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats. Invest Ophthalmol Vis Sci 42(5):1111–1118PubMed
49.
go back to reference 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(7):2481–2490PubMed 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(7):2481–2490PubMed
50.
go back to reference 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(4):404–417PubMedCrossRef 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(4):404–417PubMedCrossRef
51.
go back to reference Kalloniatis M, Tomisich G (1999) Amino acid neurochemistry of the vertebrate retina. Prog Retin Eye Res 18(6):811–866PubMedCrossRef Kalloniatis M, Tomisich G (1999) Amino acid neurochemistry of the vertebrate retina. Prog Retin Eye Res 18(6):811–866PubMedCrossRef
52.
go back to reference Fletcher EL, Kalloniatis M (1996) Neurochemical architecture of the normal and degenerating rat retina. J Comp Neurol 376(3):343–360PubMedCrossRef Fletcher EL, Kalloniatis M (1996) Neurochemical architecture of the normal and degenerating rat retina. J Comp Neurol 376(3):343–360PubMedCrossRef
53.
go back to reference Kalloniatis M, Marc RE, Murry RF (1996) Amino acid signatures in the primate retina. J Neurosci 16(21):6807–6829PubMed Kalloniatis M, Marc RE, Murry RF (1996) Amino acid signatures in the primate retina. J Neurosci 16(21):6807–6829PubMed
54.
go back to reference Marc RE, Murry RF, Fisher SK, Linberg KA, Lewis GP, Kalloniatis M (1998) Amino acid signatures in the normal cat retina. Invest Ophthalmol Vis Sci 39(9):1685–1693PubMed Marc RE, Murry RF, Fisher SK, Linberg KA, Lewis GP, Kalloniatis M (1998) Amino acid signatures in the normal cat retina. Invest Ophthalmol Vis Sci 39(9):1685–1693PubMed
55.
go back to reference Robin LN, Kalloniatis M (1992) Interrelationship between retinal ischaemic damage and turnover and metabolism of putative amino acid neurotransmitters, glutamate and GABA. Doc Ophthalmol 80(4):273–300PubMedCrossRef Robin LN, Kalloniatis M (1992) Interrelationship between retinal ischaemic damage and turnover and metabolism of putative amino acid neurotransmitters, glutamate and GABA. Doc Ophthalmol 80(4):273–300PubMedCrossRef
56.
go back to reference Bui BV, Vingrys AJ, Kalloniatis M (2003) Correlating retinal function and amino acid immunocytochemistry following post-mortem ischemia. Exp Eye Res 77(2):125–136PubMedCrossRef Bui BV, Vingrys AJ, Kalloniatis M (2003) Correlating retinal function and amino acid immunocytochemistry following post-mortem ischemia. Exp Eye Res 77(2):125–136PubMedCrossRef
57.
go back to reference Bui BV, Vingrys AJ, Wellard JW, Kalloniatis M (2004) Monocarboxylate transport inhibition alters retinal function and cellular amino acid levels. Eur J Neurosci 20(6):1525–1537PubMedCrossRef Bui BV, Vingrys AJ, Wellard JW, Kalloniatis M (2004) Monocarboxylate transport inhibition alters retinal function and cellular amino acid levels. Eur J Neurosci 20(6):1525–1537PubMedCrossRef
58.
go back to reference Fletcher EL, Kalloniatis M (1997) Neurochemical development of the degenerating rat retina. J Comp Neurol 388(1):1–22PubMedCrossRef Fletcher EL, Kalloniatis M (1997) Neurochemical development of the degenerating rat retina. J Comp Neurol 388(1):1–22PubMedCrossRef
59.
go back to reference Fletcher EL, Kalloniatis M (1997) Localisation of amino acid neurotransmitters during postnatal development of the rat retina. J Comp Neurol 380(4):449–471PubMedCrossRef Fletcher EL, Kalloniatis M (1997) Localisation of amino acid neurotransmitters during postnatal development of the rat retina. J Comp Neurol 380(4):449–471PubMedCrossRef
60.
go back to reference Kalloniatis M, Fletcher EL (1993) Immunocytochemical localization of the amino acid neurotransmitters in the chicken retina. J Comp Neurol 336(2):174–193PubMedCrossRef Kalloniatis M, Fletcher EL (1993) Immunocytochemical localization of the amino acid neurotransmitters in the chicken retina. J Comp Neurol 336(2):174–193PubMedCrossRef
61.
go back to reference Kalloniatis M, Napper GA (2002) Retinal neurochemical changes following application of glutamate as a metabolic substrate. Clin Exp Optom 85(1):27–36PubMedCrossRef Kalloniatis M, Napper GA (2002) Retinal neurochemical changes following application of glutamate as a metabolic substrate. Clin Exp Optom 85(1):27–36PubMedCrossRef
62.
go back to reference Napper GA, Kalloniatis M (1999) Neurochemical changes following postmortem ischemia in the rat retina. Vis Neurosci 16(6):1169–1180PubMedCrossRef Napper GA, Kalloniatis M (1999) Neurochemical changes following postmortem ischemia in the rat retina. Vis Neurosci 16(6):1169–1180PubMedCrossRef
63.
go back to reference Sun D, Bui BV, Vingrys AJ, Kalloniatis M (2007) Alterations in photoreceptor-bipolar cell signaling following ischemia/reperfusion in the rat retina. J Comp Neurol 505(1):131–146PubMedCrossRef Sun D, Bui BV, Vingrys AJ, Kalloniatis M (2007) Alterations in photoreceptor-bipolar cell signaling following ischemia/reperfusion in the rat retina. J Comp Neurol 505(1):131–146PubMedCrossRef
64.
go back to reference Sun D, Kalloniatis M (2004) Quantification of amino acid neurochemistry secondary to NMDA or betaxolol application. Clin Experiment Ophthalmol 32(5):505–517PubMedCrossRef Sun D, Kalloniatis M (2004) Quantification of amino acid neurochemistry secondary to NMDA or betaxolol application. Clin Experiment Ophthalmol 32(5):505–517PubMedCrossRef
65.
go back to reference Sun D, Vingrys AJ, Kalloniatis M (2007) Metabolic and functional profiling of the ischemic/reperfused rat retina. J Comp Neurol 505(1):114–130PubMedCrossRef Sun D, Vingrys AJ, Kalloniatis M (2007) Metabolic and functional profiling of the ischemic/reperfused rat retina. J Comp Neurol 505(1):114–130PubMedCrossRef
66.
go back to reference Sun D, Vingrys AJ, Kalloniatis M (2007) Metabolic and functional profiling of the normal rat retina. J Comp Neurol 505(1):92–113PubMedCrossRef Sun D, Vingrys AJ, Kalloniatis M (2007) Metabolic and functional profiling of the normal rat retina. J Comp Neurol 505(1):92–113PubMedCrossRef
67.
go back to reference Marc RE, Jones BW (2003) Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol 28(2):139–147PubMedCrossRef Marc RE, Jones BW (2003) Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol 28(2):139–147PubMedCrossRef
68.
go back to reference Marc RE, Jones BW, Anderson JR, Kinard K, Marshak DW, Wilson JH et al (2007) Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci 48(7):3364–3371PubMedCrossRef Marc RE, Jones BW, Anderson JR, Kinard K, Marshak DW, Wilson JH et al (2007) Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci 48(7):3364–3371PubMedCrossRef
69.
go back to reference Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22(5):607–655PubMedCrossRef Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22(5):607–655PubMedCrossRef
70.
go back to reference Marc RE, Murry RF, Fisher SK, Linberg KA, Lewis GP (1998) Amino acid signatures in the detached cat retina. Invest Ophthalmol Vis Sci 39(9):1694–1702PubMed Marc RE, Murry RF, Fisher SK, Linberg KA, Lewis GP (1998) Amino acid signatures in the detached cat retina. Invest Ophthalmol Vis Sci 39(9):1694–1702PubMed
71.
go back to reference Tout S, Chan-Ling T, Hollander H, Stone J (1993) The role of Muller cells in the formation of the blood-retinal barrier. Neuroscience 55(1):291–301PubMedCrossRef Tout S, Chan-Ling T, Hollander H, Stone J (1993) The role of Muller cells in the formation of the blood-retinal barrier. Neuroscience 55(1):291–301PubMedCrossRef
72.
go back to reference Chan-Ling T, Stone J (1992) Degeneration of astrocytes in feline retinopathy of prematurity causes failure of the blood-retinal barrier. Invest Ophthalmol Vis Sci 33(7):2148–2159PubMed Chan-Ling T, Stone J (1992) Degeneration of astrocytes in feline retinopathy of prematurity causes failure of the blood-retinal barrier. Invest Ophthalmol Vis Sci 33(7):2148–2159PubMed
73.
go back to reference Pow DV, Robinson SR (1994) Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60(2):355–366PubMedCrossRef Pow DV, Robinson SR (1994) Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60(2):355–366PubMedCrossRef
74.
go back to reference Kalloniatis M, Napper GA (1996) Glutamate metabolic pathways in displaced ganglion cells of the chicken retina. J Comp Neurol 367(4):518–536PubMedCrossRef Kalloniatis M, Napper GA (1996) Glutamate metabolic pathways in displaced ganglion cells of the chicken retina. J Comp Neurol 367(4):518–536PubMedCrossRef
75.
go back to reference Napper GA, Pianta MJ, Kalloniatis M (2001) Localization of amino acid neurotransmitters following in vitro ischemia and anoxia in the rat retina. Vis Neurosci 18(3):413–427PubMedCrossRef Napper GA, Pianta MJ, Kalloniatis M (2001) Localization of amino acid neurotransmitters following in vitro ischemia and anoxia in the rat retina. Vis Neurosci 18(3):413–427PubMedCrossRef
76.
go back to reference Chan-Ling T, McLeod DS, Hughes S, Baxter L, Chu Y, Hasegawa T et al (2004) Astrocyte-endothelial cell relationships during human retinal vascular development. Invest Ophthalmol Vis Sci 45(6):2020–2032PubMedCrossRef Chan-Ling T, McLeod DS, Hughes S, Baxter L, Chu Y, Hasegawa T et al (2004) Astrocyte-endothelial cell relationships during human retinal vascular development. Invest Ophthalmol Vis Sci 45(6):2020–2032PubMedCrossRef
77.
go back to reference Zhang Y, Stone J (1997) Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38(9):1653–1666PubMed Zhang Y, Stone J (1997) Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38(9):1653–1666PubMed
78.
go back to reference Penn JS, Thum LA, Rhem MN, Dell SJ (1988) Effects of oxygen rearing on the electroretinogram and GFA-protein in the rat. Invest Ophthalmol Vis Sci 29(11):1623–1630PubMed Penn JS, Thum LA, Rhem MN, Dell SJ (1988) Effects of oxygen rearing on the electroretinogram and GFA-protein in the rat. Invest Ophthalmol Vis Sci 29(11):1623–1630PubMed
79.
go back to reference Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev 2(3):185–193CrossRef Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev 2(3):185–193CrossRef
80.
81.
go back to reference Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456(7223):745–749PubMedCrossRef Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA (2008) Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 456(7223):745–749PubMedCrossRef
82.
go back to reference Gordon GR, Mulligan SJ, MacVicar BA (2007) Astrocyte control of the cerebrovasculature. Glia 55(12):1214–1221PubMedCrossRef Gordon GR, Mulligan SJ, MacVicar BA (2007) Astrocyte control of the cerebrovasculature. Glia 55(12):1214–1221PubMedCrossRef
83.
go back to reference Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314–1318PubMedCrossRef Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308(5726):1314–1318PubMedCrossRef
84.
go back to reference Lee JE, Liang KJ, Fariss RN, Wong WT (2008) Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Invest Ophthalmol Vis Sci 49(9):4169–4176PubMedCrossRef Lee JE, Liang KJ, Fariss RN, Wong WT (2008) Ex vivo dynamic imaging of retinal microglia using time-lapse confocal microscopy. Invest Ophthalmol Vis Sci 49(9):4169–4176PubMedCrossRef
85.
go back to reference Davies MH, Stempel AJ, Powers MR (2008) MCP-1 deficiency delays regression of pathologic retinal neovascularization in a model of ischemic retinopathy. Invest Ophthalmol Vis Sci 49(9):4195–4202PubMedCrossRef Davies MH, Stempel AJ, Powers MR (2008) MCP-1 deficiency delays regression of pathologic retinal neovascularization in a model of ischemic retinopathy. Invest Ophthalmol Vis Sci 49(9):4195–4202PubMedCrossRef
86.
go back to reference Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, Kuziel WA et al (2003) An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9(11):1390–1397PubMedCrossRef Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, Kuziel WA et al (2003) An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat Med 9(11):1390–1397PubMedCrossRef
87.
go back to reference El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C et al (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13(4):432–438PubMedCrossRef El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C et al (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13(4):432–438PubMedCrossRef
88.
go back to reference Yoshida S, Yoshida A, Ishibashi T, Elner SG, Elner VM (2003) Role of MCP-1 and MIP-1alpha in retinal neovascularization during postischemic inflammation in a mouse model of retinal neovascularization. J Leukoc Biol 73(1):137–144PubMedCrossRef Yoshida S, Yoshida A, Ishibashi T, Elner SG, Elner VM (2003) Role of MCP-1 and MIP-1alpha in retinal neovascularization during postischemic inflammation in a mouse model of retinal neovascularization. J Leukoc Biol 73(1):137–144PubMedCrossRef
89.
go back to reference Biber K, Neumann H, Inoue K, Boddeke HW (2007) Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci 30(11):596–602PubMedCrossRef Biber K, Neumann H, Inoue K, Boddeke HW (2007) Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci 30(11):596–602PubMedCrossRef
90.
go back to reference Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev 8(1):57–69CrossRef Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev 8(1):57–69CrossRef
91.
go back to reference Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27(10):2596–2605PubMedCrossRef Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27(10):2596–2605PubMedCrossRef
92.
go back to reference Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM et al (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9(7):917–924PubMedCrossRef Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM et al (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9(7):917–924PubMedCrossRef
93.
go back to reference Danser AH, van den Dorpel MA, Deinum J, Derkx FH, Franken AA, Peperkamp E et al (1989) Renin, prorenin, and immunoreactive renin in vitreous fluid from eyes with and without diabetic retinopathy. J Clin Endocrinol Metab 68(1):160–167PubMedCrossRef Danser AH, van den Dorpel MA, Deinum J, Derkx FH, Franken AA, Peperkamp E et al (1989) Renin, prorenin, and immunoreactive renin in vitreous fluid from eyes with and without diabetic retinopathy. J Clin Endocrinol Metab 68(1):160–167PubMedCrossRef
94.
go back to reference Moravski CJ, Kelly DJ, Cooper ME, Gilbert RE, Bertram JF, Shahinfar S et al (2000) Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension 36(6):1099–1104PubMed Moravski CJ, Kelly DJ, Cooper ME, Gilbert RE, Bertram JF, Shahinfar S et al (2000) Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension 36(6):1099–1104PubMed
95.
go back to reference Wilkinson-Berka JL, Fletcher EL (2004) Angiotensin and bradykinin: targets for the treatment of vascular and neuro-glial pathology in diabetic retinopathy. Curr Pharm Des 10(27):3313–3330PubMedCrossRef Wilkinson-Berka JL, Fletcher EL (2004) Angiotensin and bradykinin: targets for the treatment of vascular and neuro-glial pathology in diabetic retinopathy. Curr Pharm Des 10(27):3313–3330PubMedCrossRef
96.
go back to reference Berka JL, Stubbs AJ, Wang DZ, DiNicolantonio R, Alcorn D, Campbell DJ et al (1995) Renin-containing Muller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci 36(7):1450–1458PubMed Berka JL, Stubbs AJ, Wang DZ, DiNicolantonio R, Alcorn D, Campbell DJ et al (1995) Renin-containing Muller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci 36(7):1450–1458PubMed
97.
go back to reference Sarlos S, Wilkinson-Berka JL (2005) The renin-angiotensin system and the developing retinal vasculature. Invest Ophthalmol Vis Sci 46(3):1069–1077PubMedCrossRef Sarlos S, Wilkinson-Berka JL (2005) The renin-angiotensin system and the developing retinal vasculature. Invest Ophthalmol Vis Sci 46(3):1069–1077PubMedCrossRef
98.
go back to reference Yokota H, Nagaoka T, Mori F, Hikichi T, Hosokawa H, Tanaka H et al (2007) Prorenin levels in retinopathy of prematurity. Am J Ophthalmol 143(3):531–533PubMedCrossRef Yokota H, Nagaoka T, Mori F, Hikichi T, Hosokawa H, Tanaka H et al (2007) Prorenin levels in retinopathy of prematurity. Am J Ophthalmol 143(3):531–533PubMedCrossRef
99.
go back to reference Lonchampt M, Pennel L, Duhault J (2001) Hyperoxia/normoxia-driven retinal angiogenesis in mice: a role for angiotensin II. Invest Ophthalmol Vis Sci 42(2):429–432PubMed Lonchampt M, Pennel L, Duhault J (2001) Hyperoxia/normoxia-driven retinal angiogenesis in mice: a role for angiotensin II. Invest Ophthalmol Vis Sci 42(2):429–432PubMed
100.
go back to reference Wilkinson-Berka JL (2004) Diabetes and retinal vascular disorders: role of the renin-angiotensin system. Expert Rev Mol Med 6(15):1–18PubMedCrossRef Wilkinson-Berka JL (2004) Diabetes and retinal vascular disorders: role of the renin-angiotensin system. Expert Rev Mol Med 6(15):1–18PubMedCrossRef
101.
go back to reference Nagai N, Noda K, Urano T, Kubota Y, Shinoda H, Koto T et al (2005) Selective suppression of pathologic, but not physiologic, retinal neovascularization by blocking the angiotensin II type 1 receptor. Invest Ophthalmol Vis Sci 46(3):1078–1084PubMedCrossRef Nagai N, Noda K, Urano T, Kubota Y, Shinoda H, Koto T et al (2005) Selective suppression of pathologic, but not physiologic, retinal neovascularization by blocking the angiotensin II type 1 receptor. Invest Ophthalmol Vis Sci 46(3):1078–1084PubMedCrossRef
102.
go back to reference Wilkinson-Berka JL, Tan G, Jaworski K, Miller AG (2009) Identification of a retinal aldosterone system and the protective effects of mineralocorticoid receptor antagonism on retinal vascular pathology. Circ Res 104(1):124–133PubMedCrossRef Wilkinson-Berka JL, Tan G, Jaworski K, Miller AG (2009) Identification of a retinal aldosterone system and the protective effects of mineralocorticoid receptor antagonism on retinal vascular pathology. Circ Res 104(1):124–133PubMedCrossRef
103.
go back to reference Satofuka S, Ichihara A, Nagai N, Koto T, Shinoda H, Noda K et al (2007) Role of nonproteolytically activated prorenin in pathologic, but not physiologic, retinal neovascularization. Invest Ophthalmol Vis Sci 48(1):422–429PubMedCrossRef Satofuka S, Ichihara A, Nagai N, Koto T, Shinoda H, Noda K et al (2007) Role of nonproteolytically activated prorenin in pathologic, but not physiologic, retinal neovascularization. Invest Ophthalmol Vis Sci 48(1):422–429PubMedCrossRef
104.
go back to reference Sarlos S, Rizkalla B, Moravski CJ, Cao Z, Cooper ME, Wilkinson-Berka JL (2003) Retinal angiogenesis is mediated by an interaction between the angiotensin type 2 receptor, VEGF, and angiopoietin. Am J Pathol 163(3):879–887PubMed Sarlos S, Rizkalla B, Moravski CJ, Cao Z, Cooper ME, Wilkinson-Berka JL (2003) Retinal angiogenesis is mediated by an interaction between the angiotensin type 2 receptor, VEGF, and angiopoietin. Am J Pathol 163(3):879–887PubMed
Metadata
Title
The significance of neuronal and glial cell changes in the rat retina during oxygen-induced retinopathy
Authors
Erica L. Fletcher
Laura E. Downie
Kate Hatzopoulos
Kirstan A. Vessey
Michelle M. Ward
Chee L. Chow
Michael J. Pianta
Algis J. Vingrys
Michael Kalloniatis
Jennifer L. Wilkinson-Berka
Publication date
01-02-2010
Publisher
Springer-Verlag
Published in
Documenta Ophthalmologica / Issue 1/2010
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-009-9193-6

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