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Development and Role of Retinal Glia in Regeneration of Ganglion Cells Following Retinal Br J Ophthalmol: First Published As 10.1136/Bjo.80.5.458 on 1 May 1996

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Development and Role of Retinal Glia in Regeneration of Ganglion Cells Following Retinal Br J Ophthalmol: First Published As 10.1136/Bjo.80.5.458 on 1 May 1996 458 British Journal ofOphthalmology 1996; 80: 458-464 Development and role of retinal glia in regeneration of ganglion cells following retinal Br J Ophthalmol: first published as 10.1136/bjo.80.5.458 on 1 May 1996. Downloaded from injury Robert E MacLaren Abstract normally inhibitory to axonal growth.4-6 Aims/background-Recent observations Thirdly, the re-extending axon must negotiate have shown that the glial scar resulting an inhibitory gliotic barrier formed by reactive from a surgical lesion of the immature astrocytes around the lesion site.7-9 Finally, retina differs from elsewhere in the central one must consider re-navigation to appropriate nervous system, in that it permits the targets and reformation of functional neural through growth and reconnection ofregen- connections.10 erating axons. This study in the opossum In the mammalian visual system, success has examines in detail the development and been achieved in overcoming all of these reaction to injury ofretinal glia at different factors. Specific molecules have been identified developmental stages, and specifically that can promote the survival of axotomised examines the distribution of the gliosis ganglion cells: brain derived neurotrophic related inhibitory molecule, chondroitin factor3; inhibitors of protease and microgliaS; sulphate proteoglycan (CSPG), maing and, as yet undetermined, factors present in comparisons with a control site ofgliosis in peripheral nerves.1 To connect to central the cerebral cortex. targets, ganglion cell axons also need to Methods-A linear slit was cut into the traverse the thickly myelinated optic nerve, but retina or cortex with a fine tungsten this too can be overcome, either by the anti- probe. After a variable time delay, body mediated blocking of myelin associated immunocytochemistry of the resulting inhibitory factors,12 or by simply bypassing the gliosis was employed to detect astrocytes optic nerve altogether with a surgically inserted with glial fibrillary acidic protein (GFAP), peripheral nerve graft.13 14 By connecting the Muller cells with vimentin, and CSPG other end of the graft to the colliculus, these with CS-56 antibodies. GFAP was also latter experiments have also demonstrated the http://bjo.bmj.com/ used at different ages to examine the ability for regenerating ganglion cells to reform normal development of astrocytes in the functional connections'5 and to restore the retina ofthis species. light reflex.'6 Results-Astrocytes entered the retina 12 In contrast with peripheral nerve grafting, days after birth (P12), closely associated our experiments focus on the possibility of with blood vessels in the nerve fibre layer. regeneration through the existing visual path- In experiments at all ages studied, cellular ways. In lower vertebrates, ganglion cells can on September 27, 2021 by guest. Protected copyright. continuity was re-established across the regenerate back along a cut optic nerve and lesioned retina, which did not result in a reform topographic maps in the tectum, lead- significant astrocyte proliferation or ing to a return of vision.17 It is highly likely, CSPG expression. In contrast, cortical therefore, that successful return of vision in injury led to the development of a cystic mammals would also require correct re-estab- cavity surrounded by astrocytes and lishment oftopographic maps in central targets, CSPG. MuIler cells expressed GFAP but which would be more likely if regeneration not CSPG in the lesioned retina. could simply repeat the sequence of events Conclusion-Successful regrowth of that normally occur during development. 18 ganglion cells through a retinal lesion may Formerly, we described the capacity for retinal be partly the result ofthe scarcity ofastro- ganglion cells to regrow through a surgical cytes in the retina, which results in mini- lesion in the developing mammalian retina mal gliosis, or of their apparent inability (opossum) and re-navigate appropriately at the to express inhibitory molecules. optic chiasm.12 20 Ofparticular interest in those (BrJ Ophthalmol 1996; 80: 458-464) experiments was the observation that regrowing ganglion cells passed directly through the gliotic scar in the retina; a phenomenon not The failure of axons to regenerate in the observed elsewhere in the CNS, where gliotic central nervous system (CNS) of mammals is scars usually form a barrier impenetrable to Department ofHuman multifactorial. Firstly, the lesioned neurons regrowing axons.21 22 Anatomy, University need to be provided with appropriate trophic Further investigation into the structure of of Oxford, South Parks factors in order to in Road, Oxford prevent programmed cell glia the retina and the gliotic reaction to a OX1 3QX death and to facilitate re-extension of an surgical insult may therefore help in our under- R E MacLaren axon. 1-3 Secondly, the re-extending axon must standing ofmechanisms important for success- Accepted for publication be allowed to pass unimpeded through the ful regeneration of axotomised ganglion cells. 19 January 1996 CNS tissue; the myelin of oligodendrocytes is The aims of the experiments described in this Development and role ofretinal glia in regeneration ofganglion cells following retinal injury 459 paper are therefore threefold. Firstly, to exam- washing off the primary solutions. In the ine the normal and comparative histology of double labelling experiments, both primary retinal glial cells in the adult opossum. antibodies were added together in the same Br J Ophthalmol: first published as 10.1136/bjo.80.5.458 on 1 May 1996. Downloaded from Secondly, to observe the development of astro- solution, but the secondaries were added cytes in the retina of this species, and to cor- sequentially: goat anti-rabbit for 1 hour, a 30 relate this with the known critical postnatal minute block with 4% NGS, then goat anti- period (up to P12) in which regrowth of gan- mouse for 1 hour. All secondaries were washed glion cells through a retinal lesion is known to off with three rinses of PBS and the slides occur. Finally, to compare the gliotic reaction coverslipped with Aquamount (BDH, UK) of the retina to another CNS site (cortex), mounting medium. looking specifically for immunoreactivity for In selected cases, the penultimate wash con- chondroitin-6-sulphate proteoglycan (CSPG), tained a 0-001% solution of 4',6-diamidino-2- a molecule expressed by reactive astrocytes phenylindole (DAPI: Sigma), a DNA groove and which is known to be inhibitory to axonal binding protein that gives a blue fluorescence growth.8 to all cell nuclei. Specimens were photo- graphed with appropriate filters under a Leica fluorescence microscope with single, double, Materials and methods or triple exposures. Control sections (with The opossum Monodelphis domestica was used primary or secondaries omitted) confirmed for this study. The advantage of using the specificity of all the immunolabelling metatherian (marsupial) mammals lies in their described. predominantly postnatal CNS development. Five adult animals were in the experimental Whereas in rodents, ganglion cell genesis and group undergoing either a retinal (n=5) or central retinal connections are virtually com- cortical (n=2) lesion; three neonates under- plete at birth,23 24 in the opossum these events went a retinal lesion only (P7, P10, and P15). occur almost entirely postnatally.25 26 Thus, Sterile surgery was performed under an the investigation and experimental manipula- inhaled anaesthetic (halothane 5%) in oxygen, tion of factors common to the developing delivered via a face mask in an open circuit. A visual system of all mammals can be made in fine tungsten probe was employed to make the postnatal opossum without the need for surgical lesions in the temporal retina using intrauterine surgery. As a rough guide, CNS a method previously described in detail.20 development at 2 weeks old in this species is Briefly, this involved passing the sharp tung- comparable with a 1 day old mouse or rat.27 sten probe through the lateral part ofthe globe At various postnatal ages Monodelphis pups behind and parallel to the ora serrata. With the were detached from the maternal teats and probe held in place as a cutting edge inter- killed by anaesthesia with ether. The brain, nally, a sharpened pair of forceps was then base of skull, orbit, and overlying cranium scored along the outside of the globe, giving http://bjo.bmj.com/ were dissected free from the mandible and the two instruments a scissor-like action. This immediately frozen in OCT (Sigma, UK) at resulted in a slit cut in the retina from inside to -200C. Cryostat sections were then taken at out, minimising damage to the sclera and lens. 12 pm through the optic nerve and optic nerve For cortical lesions, a small burr hole was head and collected onto 5% gelatinised slides. made over the parietal bone (lateral to the After a period of 15 minutes of air drying, the superior sagittal sinus) and a similar probe sections were fixed with 4% paraformaldehyde inserted to a depth of 5 mm into and perpen- on September 27, 2021 by guest. Protected copyright. for a further 20 minutes, washed three times in dicular to the underlying parietal cortex. This pH 7-4 phosphate buffered saline (PBS), and probe was then swept through an arc laterally incubated overnight at 4°C with primary anti- to an angle of about 45 degrees and then bodies as follows: slowly withdrawn, thus lesioning the under- GFAP (polyclonal rabbit IgG, Dako, UK or lying cortical tissue in a similar fashion to the monoclonal GA-5 mouse IgG, Sigma, UK) retina. The skin was closed with 6/0 silk and diluted 1:500 in PBS with 1% bovine serum the animals survived for a variable period of albumin (BSA) and 4% normal goat serum 3-90 days (mostly 7-8 days), before being (NGS). killed with an intraperitoneal injection of bar- Vimentin (monoclonal mouse IgG, Dako) biturate. The eyes and lesioned areas of cortex diluted 1:500 in PBS with 1% BSA and 4% were marked for orientation and removed NGS.
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