Conditional müller cell ablation causes independent neuronal and vascular pathologies in a novel transgenic model

Journal of Neuroscience

Volumn 32, Issue 45, 2012, Pages 15715-15727

  Shen, Weiyong ^a   Fruttiger, Marcus ^b   Zhu, Ling ^a   Chung, Sook H ^a   Barnett, Nigel L ^c,d   Kirk, Joshua K ^a   Lee, SoRa ^a   Coorey, Nathan J ^a   Killingsworth, Murray ^e   Sherman, Larry S ^f   Gillies, Mark C ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c QUEENSLAND EYE INSTITUTE   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; PIGMENT EPITHELIUM DERIVED FACTOR; VASCULOTROPIN A;

A WAVE; ADULT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B WAVE; BLOOD RETINA BARRIER; BLOOD VESSEL PERMEABILITY; CELL LOSS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; FEMALE; FLUORESCENCE ANGIOGRAPHY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MICROSCOPY; MOUSE; MUELLER CELL; NICK END LABELING; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DETACHMENT; RETINA DISEASE; RETINA NEOVASCULARIZATION; RETINAL TELANGIECTASIA; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOOD-RETINAL BARRIER; CILIARY NEUROTROPHIC FACTOR; EYE PROTEINS; MICE; MICE, TRANSGENIC; NERVE GROWTH FACTORS; NEUROGLIA; PHOTORECEPTOR CELLS; RETINA; RETINAL NEOVASCULARIZATION; RETINAL TELANGIECTASIS; RETINAL VESSELS; SERPINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84868519037     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2841-12.2012     Document Type: Article

References (47)

1. Abukawa H, Tomi M, Kiyokawa J, Hori S, Kondo T, Terasaki T, Hosoya K (2009) Modulation of retinal capillary endothelial cells by Müller glial cell-derived factors. Mol Vis 15:451-457.
2. Ali TK, Al-Gayyar MM, Matragoon S, Pillai BA, Abdelsaid MA, Nussbaum JJ, El-Remessy AB (2011) Diabetes-induced peroxynitrite impairs the balance of pro-nerve growth factor and nerve growth factor, and causes neurovascular injury. Diabetologia 54:657-668.
3. 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.
4. Barber AJ, Gardner TW, Abcouwer SF (2011) The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci 52:1156-1163.
5. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P, Skatchkov SN, Osborne NN, Reichenbach A (2006) Müller cells in the healthy and diseased retina. Prog Retin Eye Res 25:397-424.
6. Bringmann A, Iandiev I, Pannicke T, Wurm A, Hollborn M, Wiedemann P, Osborne NN, Reichenbach A (2009) Cellular signaling and factors in-volvedinMüller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res 28:423-451.
7. Bui BV, Armitage JA, Vingrys AJ (2002) Extraction and modelling of oscillatory potentials. Doc Ophthalmol 104:17-36.
8. Cayouette M, Gravel C (1997) Adenovirus-mediated gene transfer of ciliary neurotrophic factor can prevent photoreceptor degeneration in the retinal degeneration (rd) mouse. Hum Gene Ther 8:423-430.
9. Charbel Issa P, Troeger E, Finger R, Holz FG, Wilke R, Scholl HP (2010) Structure-function correlation of the human central retina. PLoS One 5:e12864.
10. Dubois-Dauphin M, Poitry-Yamate C, de Bilbao F, Julliard AK, Jourdan F, Donati G (2000) Early postnatal Müller cell death leadstoretinal but not optic nerve degeneration in NSE-Hu-Bcl-2 transgenic mice. Neurosci-ence 95:9-21.
11. Dyer MA, Cepko CL (2000) Control of Müller glial cell proliferation and activation following retinal injury. Nat Neurosci 3:873-880.
12. Erickson KK, Sundstrom JM, Antonetti DA (2007) Vascular permeability in ocular disease and the role of tight junctions. Angiogenesis 10:103-117.
13. Fletcher EL, Phipps JA, Ward MM, Puthussery T, Wilkinson-Berka JL (2007) Neuronal and glial cell abnormality as predictors of progression of diabetic retinopathy. Curr Pharm Des 13:2699-2712.
14. Gass JD (1999) Müller cell cone, an overlooked part of the anatomy of the fovea centralis: hypotheses concerning its role inthe pathogenesisof mac-ular hole and foveomacualr retinoschisis. Arch Ophthalmol 117:821-823.
15. Gass JD, Blodi BA (1993) Idiopathic juxtafoveolar retinal telangiectasis. Update of classification and follow-up study. Ophthalmology 100:1536-1546.
16. Ghosh A, Manrique-Hoyos N, Voigt A, Schulz JB, Kreutzfeldt M, Merkler D, Simons M (2011) Targeted ablation of oligodendrocytes triggers axonal damage. PLoS One 6:e22735.
17. Guidolin D, Vacca A, Nussdorfer GG, Ribatti D (2004) A new image analysis method based on topological and fractal parameters to evaluate the angiostatic activity of docetaxel by using the Matrigel assay in vitro. Mi-crovasc Res 67:117-124.
18. Hammes HP, Federoff HJ, Brownlee M (1995) Nerve growth factor prevents both neuroretinal programmed cell death and capillary pathology in experimental diabetes. Mol Med 1:527-534.
19. Jorge R, Costa RA, Calucci D, Scott IU (2007) Intravitreal bevacizumab (Avastin) associated with the regression of subretinal neovascularization in idiopathic juxtafoveolar retinal telangiectasis. Graefe's Arch Clin Exp OPhthalmol 245:1045-1048.
20. Karlstetter M, Ebert S, Langmann T (2010) Microglia in the healthy and degenerating retina: insights from novel mouse models. Immunobiology 215:685-691.
21. Kovach JL, Rosenfeld PJ (2009) Bevacizumab (avastin) therapy for idio-pathic macular telangiectasia type II. Retina 29:27-32.
22. LaVail MM, Unoki K, Yasumura D, Matthes MT, Yancopoulos GD, Steinberg RH (1992) Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc Natl Acad Sci U S A 89:11249-11253.
23. Liang WC, Wu X, Peale FV, Lee CV, Meng YG, Gutierrez J, Fu L, Malik AK, Gerber HP, Ferrara N, Fuh G (2006) Cross-species vascular endothelial growth factor (VEGF)-blocking antibodies completely inhibit the growth of human tumor xenografts and measure the contribution of stromal VEGF. J Biol Chem 281:951-961.
24. Matsuoka M, Ogata N, Otsuji T, Nishimura T, Takahashi K, Matsumura M (2004) Expression of pigment epithelium derived factor and vascular endothelial growth factor in choroidal neovascular membranes and pol-ypoidal choroidal vasculopathy. Br J Ophthalmol 88:809-815.
25. Maxwell F, Maxwell IH, Glode LM (1987) Cloning, sequence determination, and expression in transfected cells of the coding sequence for the tox 176 attenuated diphtheria toxin A chain. Mol Cell Biol 7:1576-1579.
26. Mitamura T, Higashiyama S, Taniguchi N, Klagsbrun M, Mekada E (1995) Diphtheria toxin bindstothe epidermal growth factor (EGF)-like domain of human heparin-binding EGF-like growth factor/diphtheria toxin receptor and inhibits specifically its mitogenic activity. J Biol Chem 270: 1015-1019.
27. Miyahara S, Kiryu J, Yamashiro K, Miyamoto K, Hirose F, Tamura H, Katsuta H, Nishijima K, Tsujikawa A, Honda Y (2004) Simvastatin inhibits leukocyte accumulation and vascular permeability in the retinas of rats with streptozotocin-induced diabetes. Am J Pathol 164:1697-1706.
28. Mohan N, Monickaraj F, Balasubramanyam M, Rema M, Mohan V (2012) Imbalanced levels of angiogenic and angiostatic factors in vitreous, plasma and postmortem retinal tissue of patients with proliferative diabetic retinopathy. J Diabetes Complications.
29. Morimoto H, Bonavida B (1992) Diphtheria toxin- and Pseudomonas A toxin-mediated apoptosis. ADP ribosylation of elongation factor-2 is required for DNA fragmentation and cell lysis and synergy with tumor necrosis factor-alpha. J Immunol 149:2089-2094.
30. Moxon-Lester L, Takamoto K, Colditz PB, Barnett NL (2009) S-adenosyl-L-methionine restores photoreceptor function following acute retinal ischemia. Visual neuroscience 26:429-441.
31. Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923-926.
32. Ooto S, Hangai M, Takayama K, Arakawa N, Tsujikawa A, Koizumi H, Oshima S, Yoshimura N (2011) High-resolution photoreceptor imaging in idiopathic macular telangiectasia type 2 using adaptive optics scanning laser ophthalmoscopy. Invest Ophthalmol Vis Sci 52:5541-5550.
33. Powner MB, Gillies MC, Tretiach M, Scott A, Guymer RH, Hageman GS, Fruttiger M (2010) Perifoveal Müller cell depletion in a case of macular telangiectasia type 2. Ophthalmology 117:2407-2416.
34. Rhee KD, Ruiz A, Duncan JL, Hauswirth WW, Lavail MM, Bok D, Yang XJ (2007) Molecular and cellular alterations induced by sustained expression of ciliary neurotrophic factor in a mouse model of retinitis pigmen-tosa. Invest Ophthalmol Vis Sci 48:1389-1400.
35. Rich KA, Figueroa SL, Zhan Y, Blanks JC (1995) Effects of Müller cell disruption on mouse photoreceptor cell development. Exp Eye Res 61:235-248.
36. Sallo FB, Leung I, Chung M, Wolf-Schnurrbusch UE, Dubra A, Williams DR, Clemons T, Pauleikhoff D, Bird AC, Peto T (2011) Retinal crystals in type 2 idiopathic macular telangiectasia. Ophthalmology 118:2461-2467.
37. Shen WY, Lai CM, Graham CE, Binz N, Lai YK, Eade J, Guidolin D, Ribatti D, Dunlop SA, Rakoczy PE (2006) Long-term global retinal microvascular changes in a transgenic vascular endothelial growth factor mouse model. Diabetologia 49:1690-1701.
38. Shen W, Li S, Chung SH, Gillies MC (2010) Retinal vascular changes after glial disruption in rats. J Neurosci Res 88:1485-1499.
39. Sieving PA, Caruso RC, Tao W, Coleman HR, Thompson DJ, Fullmer KR, Bush RA (2006) Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proc Natl Acad Sci U S A 103:3896-3901.
40. Vázquez-Chona FR, Clark AM, Levine EM (2009) Rlbp1 promoter drives robust Müller glial GFP expressionintransgenic mice. Invest Ophthalmol Vis Sci 50:3996-4003.
41. Walsh N, Valter K, Stone J (2001) Cellular and subcellular patterns of expression of bFGF and CNTF in the normal and light stressed adult rat retina. Exp Eye Res 72:495-501.
42. Willis CL, Nolan CC, Reith SN, Lister T, Prior MJ, Guerin CJ, Mavroudis G, Ray DE (2004) Focal astrocyte loss is followed by microvascular damage, with subsequent repair of the blood-brain barrier in the apparent absence of direct astrocytic contact. Glia 45:325-337.
43. Willis CL, Taylor GL, Ray DE (2007) Microvascular P-glycoprotein expression at the blood-brain barrier following focal astrocyte loss and at the fenestrated vasculature of the area postrema. Brain Res 1173:126-136.
44. Wu M, Yang S, Elliott MH, Fu D, Wilson K, Zhang J, Du M, Chen J, Lyons T (2012) Oxidative and Endoplasmic Reticulum Stresses Mediate Apopto-sis Inducedby Modified LDL inHuman Retinal Müller Cells. Invest Oph-thalmol Vis Sci 53:4595-4604.
45. Wu S, Wu Y, Capecchi MR (2006) Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development 133:581-590.
46. Yannuzzi LA, Bardal AM, Freund KB, Chen KJ, Eandi CM, Blodi B (2006) Idiopathic macular telangiectasia. Arch Ophthalmol 124:450-460.
47. Zhang K, Hopkins JJ, Heier JS, Birch DG, Halperin LS, Albini TA, Brown DM, Jaffe GJ, Tao W, Williams GA (2011) Ciliary neurotrophic factor delivered by encapsulated cell intraocular implants for treatment of geographic atrophy in age-related macular degeneration. Proc Natl Acad Sci U S A 108:6241-6245.