Retinal axon regeneration in the lizardGallotia galloti in the presence of CNS myelin and oligodendrocytes

Lang, Dirk; Monzon-Mayor, M; Bandtlow, Christine E.; Stuermer, Claudia A. O.

doi:10.1002/(sici)1098-1136(199805)23:1<61::aid-glia6>3.0.co;2-7

Cited by 29 publications

(38 citation statements)

References 48 publications

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“…Another possibility is that the regrowing axons do not express the set of receptors required for detection of these guidance cues. This is an intriguing possibility, supported by our previous observation that regenerating RGC axons in G. galloti are apparently insensitive to myelin-associated axon growth inhibitors (Lang et al, 1998). The glial scar that forms at the transection site in the lizard optic nerve also does not appear to form a barrier for the regenerating RGC axons.…”

Section: Discussionmentioning

confidence: 76%

“…In the lizard Gallotia galloti, the regenerative response of RGCs after optic nerve transection (ONS) is characterized by two peculiarities: first, according to our earlier in vitro observations, outgrowth of RGC axons from lizard retinal explants following a conditioning nerve lesion sets in much later than in fish or amphibian retinal explants, where vigorous axon outgrowth occurs 1 week after optic nerve lesion (Murray, 1976;Stuermer, 1988a,b). Second, RGC axons in G. galloti were shown to regenerate in the presence of inhibitory oligodendrocytes and myelin, and NIs do not induce permanent growth cone collapse of lizard RGC axons in vitro (Lang et al, 1998). This stands in contrast to findings for most other neuronal cell types, where NIs inhibit neurite growth and induce growth cone collapse (Fawcett et al, 1989;Bandtlow et al, 1990;Bastmeyer et al, 1991;Moorman and Hume, 1993;Lang et al, 1995).…”

Section: Introductionmentioning

confidence: 94%

“…RGC axon regeneration through the optic nerve has also been demonstrated in three species of reptiles (Rio et al, 1989;Beazley et al, 1997;Lang et al, 1998), which occupy an intermediate position on the evolutionary scale between fish and amphibians on the one hand, and birds and mammals on the other. In the lizard Gallotia galloti, the regenerative response of RGCs after optic nerve transection (ONS) is characterized by two peculiarities: first, according to our earlier in vitro observations, outgrowth of RGC axons from lizard retinal explants following a conditioning nerve lesion sets in much later than in fish or amphibian retinal explants, where vigorous axon outgrowth occurs 1 week after optic nerve lesion (Murray, 1976;Stuermer, 1988a,b).…”

Section: Introductionmentioning

confidence: 94%

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Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal ganglion cells

Lang¹,

Romero-Aleman²,

Arbelo-Galvan³

et al. 2002

J. Neurobiol.

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Using anterograde tracing with HRPand antibodies (ABs) against neurofilaments, we show that regrowth of retinal ganglion cell (RGC) axons in the lizard Gallotia galloti commences only 2 months after optic nerve transection (ONS) and continues over at least 9 months. This is unusually long when compared to RGC axon regeneration in fish or amphibians. Following ONS, lizard RGCs up-regulate the immediate early gene C-JUN for 9 months or longer, indicating their reactive state. In keeping with the in vivo data, axon outgrowth from lizard retinal explants is increased above control levels from 6 weeks, reaches its maximum as late as 3 months, and remains elevated for at least 1 year after ONS. By means of BrdU incorporation assays and antiproliferating cell nuclear antigen immunohistochemistry, we show that the late axon outgrowth is not derived from new RGCs that might have arisen in reaction to ONS: no labeled cells were detected in lizard retinas at 0.5, 1, 1.5, 3, 6, and 12 months after ONS. Conversely, numbers of RGCs undergoing apoptosis were too low to be detectable in TUNEL assays at any time after ONS. These results demonstrate that retinal axon regeneration in G. galloti is due to axon regrowth from the resident population of RGCs, which remain in a reactive state over an extended time interval. Neurogenesis does not appear to be involved in RGC axon regrowth in G. galloti.

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Section: Discussionmentioning

confidence: 76%

Section: Introductionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 94%

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Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal ganglion cells

Lang¹,

Romero-Aleman²,

Arbelo-Galvan³

et al. 2002

J. Neurobiol.

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“…Adult lizards were anaesthetised on ice before being lesioned according to Lang et al (1998). Briefly, an unilateral incision was made along the margin of the largest supraocular osteodermal plaque to expose and cut the ON.…”

Section: Methodsmentioning

confidence: 99%

“…However, whereas autonomic innervation has been reported in the CP of several lizard species (Nguyen-Legros 1978), the pecten is devoid of innervation (Brach 1977;Ehinger 1967). As regrowth of the axons of retinal ganglion cells (RGCs) occurs after optic nerve (ON) injury in the lizard Gallotia galloti (Lang et al 1998(Lang et al , 2002, the nutrition of the surviving RGCs should be maintained during regeneration.…”

Section: Introductionmentioning

confidence: 99%

Ontogeny of the conus papillaris of the lizard Gallotia galloti and cellular response following transection of the optic nerve: an immunohistochemical and ultrastructural study

et al. 2011

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Spontaneous regrowth of the axons of retinal ganglion cells (RGC) occurs after unilateral optic nerve transection (ONT) in the lizard Gallotia galloti. We have performed an immunohistochemical and ultrastructural study of the conus papillaris (CP) of this lizard during ontogeny and after ONT in order to characterize its cell subpopulations, innervation and putative blood-brain barrier (BBB) and to evaluate changes occurring throughout regeneration. Proliferating PCNA(+) cells were abundant between embryonic stage 33 (E33) and hatching. From E33, we observed Pax2(+)/GS(+) glial cells in the primitive CP, which became increasingly pigmented and vascularised from E35. Conal astrocytes coexpressing Pax2 with vimentin and/or GFAP were identified from E37-E38. GluT-1(+)/LEA(+)/Pax2(-) endothelial cells (ECs) formed a continuous endothelium with tight junctions and luminal and abluminal microfolds. In adults, the peripheral blood vessels showed a thinner calibre, stronger GluT-1 staining and more abundant microfolds than those of the central CP indicating the higher specialization involved during transport within the former. Occasional pericytes, abundant Pax2(+) pigment cells, LEA(+) microglia/macrophages, unmyelinated Tuj1(+) nerve fibres and SV2(+) synaptic vesicles were also observed in the perivascular zone. After ONT, the expression of GluT-1 and p75(NTR) persisted in ECs, suggesting the preservation/early recovery of the BBB. Relevant ultrastructural alterations were observed at 0.5 months postlesion, although, by 3 months, the CP had recovered the ultrastructure of controls indicating tissue recovery. Abnormal newly formed blood vessels had developed in the CP-optic nerve junction. Thus, the CP is a central nervous system structure whose regenerating capacity might be key for the nutritional support of regenerating RGCs in G. galloti.

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Failure to restore vision after optic nerve regeneration in reptiles: Interspecies variation in response to axotomy

Dunlop

Tee

Stirling

et al. 2004

J of Comparative Neurology

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Optic nerve regeneration within the reptiles is variable. In a snake, Viper aspis, and the lizard Gallotia galloti, regeneration is slow, although some retinal ganglion cell (RGC) axons eventually reach the visual centers (Rio et al. [1989] Brain Res 479:151-156; Lang et al. [1998] Glia 23:61-74). By contrast, in a lizard, Ctenophorus ornatus, numerous RGC axons regenerate rapidly to the visual centers, but unless animals are stimulated visually, the regenerated projection lacks topography and animals remain blind via the experimental eye (Beazley et al. [2003] J. Neurotrauma 20:1263-1269). V. aspis, G. galloti, and C. ornatus belong respectively to the Serpentes, Lacertidae, and Agamidae within the Eureptilia, the major modern group of living reptiles comprising the Squamata (snakes, lizards, and geckos) and the Crocodyllia. Here we have extended the findings on Eureptilia to include two geckos (Gekkonidae), Cehyra variegata and Nephrurus stellatus. We also examined a turtle, Chelodina oblonga, the Testudines being the sole surviving representatives of the Parareptilia, the more ancient reptilian group. In all three species, visually elicited behavioral responses were absent throughout regeneration, a result supported electrophysiologically; axonal tracing revealed that only a small proportion of RGC axons crossed the lesion and none entered the contralateral optic tract. RGC axons failed to reach the chiasm in C. oblonga, and in G. variegata, and N. stellatus RGC axons entered the opposite optic nerve; a limited ipsilateral projection was seen in G. variegata. Our results support a heterogeneous response to axotomy within the reptiles, each of which is nevertheless dysfunctional.

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Retinal axon regeneration in the lizardGallotia galloti in the presence of CNS myelin and oligodendrocytes

Cited by 29 publications

References 48 publications

Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal ganglion cells

Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal ganglion cells

Ontogeny of the conus papillaris of the lizard Gallotia galloti and cellular response following transection of the optic nerve: an immunohistochemical and ultrastructural study

Failure to restore vision after optic nerve regeneration in reptiles: Interspecies variation in response to axotomy

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