Radial glial cells, proliferating periventricular cells, and microglia might contribute to successful structural repair in the cerebral cortex of the lizard Gallotia galloti

Romero-Aleman, M. M.; Monzon-Mayor, M; Yanes, C.; Lang, Dirk

doi:10.1016/j.expneurol.2004.03.014

Cited by 43 publications

(36 citation statements)

References 40 publications

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“…In regeneration-competent systems such as the rat peripheral nerve, GS activity decreases after axotomy (Politis and Miller, 1985). In contrast, the GS expression increases in the regenerating lizard cerebral cortex (Romero-Alemán et al, 2004), and also in the fish cerebellum (Zupanc et al, 2006). Thus, the patterns of GS expression and/or activity in both systems are diverse.…”

Section: Identification Of Neuron-like Cells In the On-otrmentioning

confidence: 85%

Expression of neuronal markers, synaptic proteins, and glutamine synthetase in the control and regenerating lizard visual system

Romero-Aleman

Monzon-Mayor

Santos

et al. 2010

J of Comparative Neurology

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Spontaneous regrowth of retinal ganglion cell (RGC) axons occurs after optic nerve (ON) transection in the lizard Gallotia galloti. To gain more insight into this event we performed an immunohistochemical study on selected neuron and glial markers, which proved useful for analyzing the axonal regrowth process in different regeneration models. In the control lizards, RGCs were beta-III tubulin- (Tuj1) and HuCD-positive. The vesicular glutamate transporter-1 (VGLUT1) preferentially stained RGCs and glial somata rather than synaptic layers. In contrast, SV2 and vesicular GABA/glycine transporter (VGAT) labeling was restricted to both plexiform layers. Strikingly, the strong expression of glutamine synthetase (GS) in both Müller glia processes and macroglial somata revealed a high glutamate metabolism along the visual system. Upregulation of Tuj1 and HuCD in the surviving RGCs was observed at all the timepoints studied (1, 3, 6, 9, and 12 months postlesion). The significant rise of Tuj1 in the optic nerve head and optic tract (OTr) by 1 and 6 months postlesion, respectively, suggests an increase of the beta-III tubulin transport and incorporation into newly formed axons. Persistent Tuj1(+) and SV2(+) puncta and swellings were abnormally observed in putative degenerating/dystrophic fibers. Unexpectedly, neuron-like cells of obscure significance were identified in the control and regenerating ON-OTr. We conclude that: 1) the persistent upregulation of Tuj1 and HuCD favors the long-lasting axonal regrowth process; 2) the latter succeeded despite the ectopia and dystrophy of some regrowing fibers; and 3) maintenance of the glutamate-glutamine cycle contributes to the homeostasis and plasticity of the system.

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Section: Identification Of Neuron-like Cells In the On-otrmentioning

confidence: 85%

Expression of neuronal markers, synaptic proteins, and glutamine synthetase in the control and regenerating lizard visual system

Romero-Aleman

Monzon-Mayor

Santos

et al. 2010

J of Comparative Neurology

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“…Parvalbumin has been used to label amacrine cells in the vertebrate retina (Hamano et al, 1990;Casini et al, 1998;Weruaga et al, 2000;Mack et al, 2004) and HuC-D is a marker for RNA-binding neuronal proteins (HuC and HuD) that are highly conserved among vertebrates (Saito et al, 2004). In the G. galloti brain, tomato lectin, vimentin and GFAP have been previously used to detect microglia (Romero-Alemán et al, 2004) and astrocytes (Monzón-Mayor et al, 1990), respectively.…”

Section: Introductionmentioning

confidence: 99%

Distribution of neurotrophin‐3 during the ontogeny and regeneration of the lizard (Gallotia galloti) visual system

Santos

Monzon-Mayor

Romero-Aleman

et al. 2007

Developmental Neurobiology

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We have previously described the spontaneous regeneration of retinal ganglion cell axons after optic nerve (ON) transection in the adult Gallotia galloti. As neurotrophin-3 (NT-3) is involved in neuronal differentiation, survival and synaptic plasticity, we performed a comparative immunohistochemical study of NT-3 during the ontogeny and regeneration (after 0.5, 1, 3, 6, 9, and 12 months postlesion) of the lizard visual system to reveal its distribution and changes during these events. For characterization of NT-3(+) cells, we performed double labelings using the neuronal markers HuC-D, Pax6 and parvalbumin (Parv), the microglial marker tomato lectin or Lycopersicon esculentum agglutinin (LEA), and the astroglial markers vimentin (Vim) and glial fibrillary acidic protein (GFAP). Subpopulations of retinal and tectal neurons were NT-3(+) from early embryonic stages to adulthood. Nerve fibers within the retinal nerve fiber layer, both plexiform layers and the retinorecipient layers in the optic tectum (OT) were also stained. In addition, NT-3(+)/GFAP(+) and NT-3(+)/Vim(+) astrocytes were detected in the ON, chiasm and optic tract in postnatal and adult lizards. At 1 month postlesion, abundant NT-3(+)/GFAP(+) astrocytes and NT-3(-)/LEA(+) microglia/macrophages were stained in the lesioned ON, whereas NT-3 became downregulated in the experimental retina and OT. Interestingly, at 9 and 12 months postlesion, the staining in the experimental retina resembled that in control animals, whereas bundles of putative regrown fibers showed a disorganized staining pattern in the OT. Altogether, we demonstrate that NT-3 is widely distributed in the lizard visual system and its changes after ON transection might be permissive for the successful axonal regrowth.

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“…Work in frogs, lizards, salamanders and fish suggests that neural stem/progenitor cells at the ventricle react to CNS injury by increasing proliferation and neurogenesis, and might be the origin of regenerated neurons (Endo et al, 2007;Font et al, 2001;Kaslin et al, 2008;Kirsche and Kirsche, 1961;Parish et al, 2007;Tanaka and Ferretti, 2009;Zupanc and Clint, 2003). However, the experimental evidence for this notion is indirect: it relies on the observation of upregulated proliferation and neurogenesis after lesion in the ventricular zone and enhanced migration of newborn neurons to the lesion site (Endo et al, 2007;Font et al, 2001;Kaslin et al, 2008;Kirsche, 1965;Romero-Aleman et al, 2004;Zupanc and Ott, 1999). In addition, removal of the constitutive proliferation zones in the carp optic tectum prevents restoration of the tissue architecture (Kirsche and Kirsche, 1961).…”

Section: Introductionmentioning

confidence: 99%

“…In many nonmammalian species, RG persist into adulthood and therefore could be a source of adult-born neurons (Kaslin et al, 2008). In salamanders, lizards and bony fishes, it has been suggested, but not shown, that ventricular RG might be the source of regenerated neurons in the lesioned brain and spinal cord (Berg et al, 2010;Echeverri and Tanaka, 2002;Parish et al, 2007;Reimer et al, 2008;Romero-Aleman et al, 2004). Very recently it has been shown by viral lineage-tracing in the zebrafish telencephalon that RG can indeed act as constitutive neural stem cells in the uninjured brain (Rothenaigner et al, 2011).…”

Section: Newly Generated Neurons Derive From Radial Glialmentioning

confidence: 99%

Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors

et al. 2011

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SUMMARYSevere traumatic injury to the adult mammalian CNS leads to life-long loss of function. By contrast, several non-mammalian vertebrate species, including adult zebrafish, have a remarkable ability to regenerate injured organs, including the CNS. However, the cellular and molecular mechanisms that enable or prevent CNS regeneration are largely unknown. To study brain regeneration mechanisms in adult zebrafish, we developed a traumatic lesion assay, analyzed cellular reactions to injury and show that adult zebrafish can efficiently regenerate brain lesions and lack permanent glial scarring. Using Cre-loxP-based genetic lineage-tracing, we demonstrate that her4.1-positive ventricular radial glia progenitor cells react to injury, proliferate and generate neuroblasts that migrate to the lesion site. The newly generated neurons survive for more than 3 months, are decorated with synaptic contacts and express mature neuronal markers. Thus, regeneration after traumatic lesion of the adult zebrafish brain occurs efficiently from radial glia-type stem/progenitor cells.

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Radial glial cells, proliferating periventricular cells, and microglia might contribute to successful structural repair in the cerebral cortex of the lizard Gallotia galloti

Cited by 43 publications

References 40 publications

Expression of neuronal markers, synaptic proteins, and glutamine synthetase in the control and regenerating lizard visual system

Expression of neuronal markers, synaptic proteins, and glutamine synthetase in the control and regenerating lizard visual system

Distribution of neurotrophin‐3 during the ontogeny and regeneration of the lizard (Gallotia galloti) visual system

Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors

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