Reactive gliosis in the adult zebrafish retina

Experimental Eye Research

Volumn 143, Issue , 2016, Pages 98-109

  Thomas, Jennifer L ^a,b   Ranski, Alexandra H ^a   Morgan, Gregory W ^a,c   Thummel, Ryan ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

5 Fluorouracil; M ller glia; Ouabain; Photoreceptor; Regeneration

Indexed keywords

FLUOROURACIL; ANTINEOPLASTIC ANTIMETABOLITE; CYCLINE; GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; GLIA CELL; GLIOSIS; MUELLER CELL; NEUROPROTECTION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; REGENERATION; RETINA; ZEBRA FISH; ANIMAL; APOPTOSIS; CELL PROLIFERATION; CYTOLOGY; DARK ADAPTATION; DRUG EFFECTS; INTRAVITREAL DRUG ADMINISTRATION; LIGHT; MACROGLIA; METABOLISM; PATHOPHYSIOLOGY; PHOTORECEPTOR CELL; PHYSIOLOGY; RADIATION RESPONSE; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; TUNEL ASSAY;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CELL PROLIFERATION; DARK ADAPTATION; EPENDYMOGLIAL CELLS; FLUOROURACIL; GLIOSIS; GREEN FLUORESCENT PROTEINS; IN SITU NICK-END LABELING; INTRAVITREAL INJECTIONS; LIGHT; PHOTORECEPTOR CELLS, VERTEBRATE; PROLIFERATING CELL NUCLEAR ANTIGEN; REAL-TIME POLYMERASE CHAIN REACTION; STEM CELLS; ZEBRAFISH;

EID: 84948783777     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.09.017     Document Type: Article

References (66)

1. Bailey T.J., Fossum S.L., Fimbel S.M., Montgomery J.E., Hyde D.R. The inhibitor of phagocytosis, O-phospho-L-serine, suppresses muller glia proliferation and cone cell regeneration in the light-damaged zebrafish retina. Exp. Eye Res. 2010, 91:601-612.
2. Berindan-Neagoe I., Braicu C., Pileczki V., Cojocneanu Petric R., Miron N., Balacescu O., Iancu D., Ciuleanu T. 5-Fluorouracil potentiates the anti-cancer effect of oxaliplatin on Colo320 colorectal adenocarcinoma cells. J. Gastrointest. Liver Dis. JGLD 2013, 22:37-43.
3. Bernardos R.L., Raymond P.A. GFAP transgenic zebrafish. Gene Expr. Patterns GEP 2006, 6:1007-1013.
4. Bignami A., Dahl D. The radial glia of muller in the rat retina and their response to injury. An immunofluorescence study with antibodies to the glial fibrillary acidic (GFA) protein. Exp. Eye Res. 1979, 28:63-69.
5. Bringmann A., Pannicke T., Grosche J., Francke M., Wiedemann P., Skatchkov S.N., Osborne N.N., Reichenbach A. Muller cells in the healthy and diseased retina. Prog. Retinal Eye Res. 2006, 25:397-424.
6. Bringmann A., Reichenbach A., Wiedemann P. Pathomechanisms of cystoid macular edema. Ophthalmic Res. 2004, 36:241-249.
7. Bringmann A., Wiedemann P. Involvement of muller glial cells in epiretinal membrane formation. Graefe's Arch. Clin. Exp. Ophthalmol. = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie 2009, 247:865-883.
8. Bringmann A., Wiedemann P. Muller glial cells in retinal disease. Ophthalmologica. J. Int. d'ophtalmologie. Int. J. Ophthalmol. Z. fur Augenheilkd. 2012, 227:1-19.
9. Das A.V., Mallya K.B., Zhao X., Ahmad F., Bhattacharya S., Thoreson W.B., Hegde G.V., Ahmad I. Neural stem cell properties of muller glia in the mammalian retina: regulation by notch and Wnt signaling. Dev. Biol. 2006, 299:283-302.
10. Dyer M.A., Cepko C.L. Control of muller glial cell proliferation and activation following retinal injury. Nat. Neurosci. 2000, 3:873-880.
11. Egensperger R., Maslim J., Bisti S., Hollander H., Stone J. Fate of DNA from retinal cells dying during development: uptake by microglia and macroglia (Muller cells). Brain research. Dev. Brain Res. 1996, 97:1-8.
12. Failli A., Legitimo A., Orsini G., Castagna M., Spisni R., Miccoli P., Consolini R. Antiproliferative effects of 5-fluorouracil and oxaliplatin in colon cancer cell lines: comparison of three different cytotoxicity assays. J. Biol. Regul. Homeost. Agents 2013, 27:275-284.
13. Faktorovich E.G., Steinberg R.H., Yasumura D., Matthes M.T., LaVail M.M. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature 1990, 347:83-86.
14. Faktorovich E.G., Steinberg R.H., Yasumura D., Matthes M.T., LaVail M.M. Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J. Neurosci. Off. J. Soc. Neurosci. 1992, 12:3554-3567.
15. Fausett B.V., Gumerson J.D., Goldman D. The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J. Neurosci. Off. J. Soc. Neurosci. 2008, 28:1109-1117.
16. Fimbel S.M., Montgomery J.E., Burket C.T., Hyde D.R. Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J. Neurosci. Off. J. Soc. Neurosci. 2007, 27:1712-1724.
17. Ganesh B.S., Chintala S.K. Inhibition of reactive gliosis attenuates excitotoxicity-mediated death of retinal ganglion cells. PloS One 2011, 6:e18305.
18. Garcia M., Vecino E. Role of muller glia in neuroprotection and regeneration in the retina. Histol. Histopathol. 2003, 18:1205-1218.
19. Giannelli S.G., Demontis G.C., Pertile G., Rama P., Broccoli V. Adult human muller glia cells are a highly efficient source of rod photoreceptors. Stem Cells 2011, 29:344-356.
20. Grosche J., Hartig W., Reichenbach A. Expression of glial fibrillary acidic protein (GFAP), glutamine synthetase (GS), and Bcl-2 protooncogene protein by muller (glial) cells in retinal light damage of rats. Neurosci. Lett. 1995, 185:119-122.
21. Hollander H., Makarov F., Dreher Z., van Driel D., Chan-Ling T.L., Stone J. Structure of the macroglia of the retina: sharing and division of labour between astrocytes and muller cells. J. Comp. Neurol. 1991, 313:587-603.
22. Inman D.M., Horner P.J. Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucoma. Glia 2007, 55:942-953.
23. Karl M.O., Reh T.A. Studying the generation of regenerated retinal neuron from muller glia in the mouse eye. Methods Mol. Biol. 2012, 884:213-227.
24. LaVail M.M., Faktorovich E.G., Hepler J.M., Pearson K.L., Yasumura D., Matthes M.T., Steinberg R.H. Basic fibroblast growth factor protects photoreceptors from light-induced degeneration in albino rats. Ann. N. Y. Acad. Sci. 1991, 638:341-347.
25. Lewis G.P., Chapin E.A., Luna G., Linberg K.A., Fisher S.K. The fate of muller's glia following experimental retinal detachment: nuclear migration, cell division, and subretinal glial scar formation. Mol. Vis. 2010, 16:1361-1372.
26. Lewis G.P., Erickson P.A., Guerin C.J., Anderson D.H., Fisher S.K. Changes in the expression of specific muller cell proteins during long-term retinal detachment. Exp. Eye Res. 1989, 49:93-111.
27. Lewis G.P., Fisher S.K. Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression. Int. Rev. Cytol. 2003, 230:263-290.
28. Liu B., Hunter D.J., Rooker S., Chan A., Paulus Y.M., Leucht P., Nusse Y., Nomoto H., Helms J.A. Wnt signaling promotes muller cell proliferation and survival after injury. Investig. Ophthalmol. Vis. Sci. 2013, 54:444-453.
29. Longley D.B., Harkin D.P., Johnston P.G. 5-fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer 2003, 3:330-338.
30. Lu X., Deng Q., Li H., Suo Z. Altered characteristics of cancer stem/initiating cells in a breast cancer cell line treated with persistent 5-FU chemotherapy. Exp. Ther. Med. 2011, 2:821-826.
31. Lu Y.B., Iandiev I., Hollborn M., Korber N., Ulbricht E., Hirrlinger P.G., Pannicke T., Wei E.Q., Bringmann A., Wolburg H., Wilhelmsson U., Pekny M., Wiedemann P., Reichenbach A., Kas J.A. Reactive glial cells: increased stiffness correlates with increased intermediate filament expression. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2011, 25:624-631.
32. Masai I., Yamaguchi M., Tonou-Fujimori N., Komori A., Okamoto H. The hedgehog-PKA pathway regulates two distinct steps of the differentiation of retinal ganglion cells: the cell-cycle exit of retinoblasts and their neuronal maturation. Development 2005, 132:1539-1553.
33. McGillem G.S., Dacheux R.F. Rabbit retinal muller cells undergo antigenic changes in response to experimentally induced proliferative vitreoretinopathy. Exp. Eye Res. 1999, 68:617-627.
34. McUsic A.C., Lamba D.A., Reh T.A. Guiding the morphogenesis of dissociated newborn mouse retinal cells and hES cell-derived retinal cells by soft lithography-patterned microchannel PLGA scaffolds. Biomaterials 2012, 33:1396-1405.
35. Morris A.C., Schroeter E.H., Bilotta J., Wong R.O., Fadool J.M. Cone survival despite rod degeneration in XOPS-mCFP transgenic zebrafish. Investig. Ophthalmol. Vis. Sci. 2005, 46:4762-4771.
36. Nakazawa T., Takeda M., Lewis G.P., Cho K.S., Jiao J., Wilhelmsson U., Fisher S.K., Pekny M., Chen D.F., Miller J.W. Attenuated glial reactions and photoreceptor degeneration after retinal detachment in mice deficient in glial fibrillary acidic protein and vimentin. Investig. Ophthalmol. Vis. Sci. 2007, 48:2760-2768.
37. Negishi K. 5-Fluorouracil reduces proliferating cell nuclear antigen immunoreactive cells in goldfish retina. Neurosci. Res. 1994, 19:21-29.
38. Newman E., Reichenbach A. The muller cell: a functional element of the retina. Trends Neurosci. 1996, 19:307-312.
39. Newman E.A. Inward-rectifying potassium channels in retinal glial (muller) cells. J. Neurosci. Off. J. Soc. Neurosci. 1993, 13:3333-3345.
40. Nickerson P.E., McLeod M.C., Myers T., Clarke D.B. Effects of epidermal growth factor and erythropoietin on muller glial activation and phenotypic plasticity in the adult mammalian retina. J. Neurosci. Res. 2011, 89:1018-1030.
41. Okada M., Matsumura M., Ogino N., Honda Y. Muller cells in detached human retina express glial fibrillary acidic protein and vimentin. Graefe's Arch. Clin. Exp. Ophthalmol. = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie 1990, 228:467-474.
42. Olson K.B., Greene J.R. Evaluation of 5-fluorouracil in the treatment of cancer. J. Natl. Cancer Inst. 1960, 25:133-140.
43. Paulson O.B., Newman E.A. Does the release of potassium from astrocyte endfeet regulate cerebral blood flow?. Science 1987, 237:896-898.
44. Poitry-Yamate C.L., Poitry S., Tsacopoulos M. Lactate released by muller glial cells is metabolized by photoreceptors from mammalian retina. J. Neurosci. Off. J. Soc. Neurosci. 1995, 15:5179-5191.
45. Pollak J., Wilken M.S., Ueki Y., Cox K.E., Sullivan J.M., Taylor R.J., Levine E.M., Reh T.A. ASCL1 reprograms mouse muller glia into neurogenic retinal progenitors. Development 2013, 140:2619-2631.
46. Ponsioen T.L., van Luyn M.J., van der Worp R.J., Nolte I.M., Hooymans J.M., Los L.I. In vitro phagocytosis of collagens by immortalised human retinal muller cells. Graefe's Arch. Clin. Exp. Ophthalmol. = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie 2007, 245:82-92.
47. Qin Z., Kidd A.R., Thomas J.L., Poss K.D., Hyde D.R., Raymond P.A., Thummel R. FGF signaling regulates rod photoreceptor cell maintenance and regeneration in zebrafish. Exp. Eye Res. 2011, 93:726-734.
48. Sahel J.A., Albert D.M., Lessell S. Proliferation of retinal glia and excitatory amino acids. Ophtalmol. organe de la Societe francaise d'ophtalmologie 1990, 4:13-16.
49. Sethi C.S., Lewis G.P., Fisher S.K., Leitner W.P., Mann D.L., Luthert P.J., Charteris D.G. Glial remodeling and neural plasticity in human retinal detachment with proliferative vitreoretinopathy. Investig. Ophthalmol. Vis. Sci. 2005, 46:329-342.
50. Sherpa T., Fimbel S.M., Mallory D.E., Maaswinkel H., Spritzer S.D., Sand J.A., Li L., Hyde D.R., Stenkamp D.L. Ganglion cell regeneration following whole-retina destruction in zebrafish. Dev. Neurobiol. 2008, 68:166-181.
51. Strzalka W., Ziemienowicz A. Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Ann. Bot. 2011, 107:1127-1140.
52. Thomas J.L., Nelson C.M., Luo X., Hyde D.R., Thummel R. Characterization of multiple light damage paradigms reveals regional differences in photoreceptor loss. Exp. Eye Res. 2012, 97:105-116.
53. Thomas J.L., Thummel R. A novel light damage paradigm for use in retinal regeneration studies in adult zebrafish. J. Vis. Exp. JoVE 2013, e51017.
54. Thummel R., Kassen S.C., Enright J.M., Nelson C.M., Montgomery J.E., Hyde D.R. Characterization of muller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp. Eye Res. 2008, 87:433-444.
55. Thummel R., Kassen S.C., Montgomery J.E., Enright J.M., Hyde D.R. Inhibition of muller glial cell division blocks regeneration of the light-damaged zebrafish retina. Dev. Neurobiol. 2008, 68:392-408.
56. Tiwari M. Antimetabolites: established cancer therapy. J. Cancer Res. Ther. 2012, 8:510-519.
57. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. Off. J. Soc. Neurosci. 1996, 16:877-885.
58. Ulbricht E., Pannicke T., Hollborn M., Raap M., Goczalik I., Iandiev I., Hartig W., Uhlmann S., Wiedemann P., Reichenbach A., Bringmann A., Francke M. Proliferative gliosis causes mislocation and inactivation of inwardly rectifying K(+) (kir) channels in rabbit retinal glial cells. Exp. Eye Res. 2008, 86:305-313.
59. Van Triest B., Pinedo H.M., Giaccone G., Peters G.J. Downstream molecular determinants of response to 5-fluorouracil and antifolate thymidylate synthase inhibitors. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol./ESMO 2000, 11:385-391.
60. Vazquez-Chona F.R., Swan A., Ferrell W.D., Jiang L., Baehr W., Chien W.M., Fero M., Marc R.E., Levine E.M. Proliferative reactive gliosis is compatible with glial metabolic support and neuronal function. BMC Neurosci. 2011, 12:98.
61. Vihtelic T.S., Hyde D.R. Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J. Neurobiol. 2000, 44:289-307.
62. Wan J., Zheng H., Xiao H.L., She Z.J., Zhou G.M. Sonic hedgehog promotes stem-cell potential of muller glia in the mammalian retina. Biochem. Biophys. Res. Commun. 2007, 363:347-354.
63. Wen R., Song Y., Cheng T., Matthes M.T., Yasumura D., LaVail M.M., Steinberg R.H. Injury-induced upregulation of bFGF and CNTF mRNAS in the rat retina. J. Neurosci. Off. J. Soc. Neurosci. 1995, 15:7377-7385.
64. Westerfield The Zebrafish Book: a Guide for the Laboratory Use of Zebrafish (Danio rerio) 1995, Univ. of Oregon Press., Eugene, OR.
65. Xue L., Ding P., Xiao L., Hu M., Hu Z. Nestin, a new marker, expressed in muller cells following retinal injury. Can. J. Neurol. Sci. 2010, 37:643-649.
66. Yafai Y., Iandiev I., Lange J., Yang X.M., Wiedemann P., Bringmann A., Eichler W. Basic fibroblast growth factor contributes to a shift in the angioregulatory activity of retinal glial (Muller) cells. PloS One 2013, 8:e68773.