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Development of astroglia heterogeneously expressing Pax2, vimentin and GFAP during the ontogeny of the optic pathway of the lizard (Gallotia galloti): an immunohistochemical and ultrastructural study

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Abstract

The successful regrowth of retinal ganglion cell (RGC) axons after optic nerve (ON) axotomy in Gallotia galloti indicates a permissive role of the glial environment. We have characterised the astroglial lineage of the lizard optic pathway throughout its ontogeny (embryonic stage 30 [E30] to adults) by using electron microscopy and immunohistochemistry to detect the proliferation marker PCNA (proliferating cell nuclear antigen), the transcription factor Pax2 and the gliofilament proteins vimentin (Vim) and GFAP (glial fibrillary acidic protein). PCNA+ cells were abundant until E39, with GFAP+/PCNA+ astrocytes being observed between E37 and hatching. Proliferation diminished markedly afterwards, being undetectable in the adult optic pathway. Müller glia of the central retina expressed Pax2 from E37 and their endfeet accumulated Vim from E33 and GFAP from E37 onwards. Astrocytes were absent in the avascular lizard retina, whereas abundant Pax2+ astrocytes were observed in the ON from E30. A major subpopulation of these astrocytes coexpressed Vim from E35 and also GFAP from E37 onwards; thus the majority of mature astrocytes coexpressed Pax2/Vim/GFAP. The astrocytes were ultrastructurally identified by their gliofilaments, microtubules, dense bodies, desmosomes and glycogen granules, which preferentially accumulated in cell processes. Astrocytes in the adult ON coexpressed both gliofilaments and presented desmosomes indicating a reinforcement of the ON structure; this is physiologically necessary for local adaptation to mechanical forces linked to eye movement. We suggest that astrocytes forming this structural scaffold facilitate the regrowth of RGCs after ON transection.

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Abbreviations

CN:

Caudal optic nerve

CPONJ:

Conus papillaris-optic nerve junction

CR:

Central retina

GFAP:

Glial fibrillary acidic protein

INL:

Inner nuclear layer

MN:

Mid optic nerve

OCh:

Optic chiasm

ON:

Optic nerve

ONH:

Optic nerve head

OTr:

Optic tract

PCNA:

Proliferating cell nuclear antigen

PR:

Peripheral retina

RGC:

Retinal ganglion cell

RONJ:

Retina-optic nerve junction

Vim:

Vimentin

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Acknowledgements

The technical assistance of the Electron Microscopy Services of the University of La Laguna (ULL) and the University of Las Palmas de Gran Canaria (ULPGC) are greatly appreciated.

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Authors and Affiliations

  1. Department of Cellular Biology, Faculty of Biology, University of La Laguna, 38206, Tenerife, Canary Islands, Spain

    M. Nieves Casañas, Elena Santos, Carmen Yanes, Raquel Viñoly & M. Carmen Alfayate

  2. Department of Morphology (Cellular Biology), Faculty of Health Sciences, University of Las Palmas of Gran Canaria, C/ Dr. Pasteur s/n. A.C. 550, 35016, Las Palmas, Canary Islands, Spain

    Elena Santos, Maria M. Romero-Alemán & Maximina Monzón-Mayor

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  1. M. Nieves Casañas
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  2. Elena Santos
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  6. M. Carmen Alfayate
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Correspondence to Elena Santos.

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This work was supported by the Spanish Ministry of Education (Research Project BFU2007-67139) and the Regional Canary Islands Government (ACIISI, Research Project SolSubC200801000281; Project ULPAPD-08/01-4).

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Fig. S1

Panoramic views of the retina (a, b) and optic nerve-optic tract (ON-OTr; c, d) of adult (Ad) lizards immunolabelled for vimentin (Vim) and glial fibrillary acidic protein (GFAP). a, b Immunofluorescence labelling for Vim (a) and immunoperoxidase staining for GFAP (b) in the retina. Müller glia endfeet are weakly Vim+ in the central (CR) compared with the peripheral retina (PR), whereas they show homogeneous GFAP labelling along the entire retina (l lens). c, d Immunoperoxidase staining for Vim (c) and GFAP (d) in the ON-OTr. Note intense Vim staining in the caudal nerve (CN) and strong GFAP staining in the midnerve (MN). Bars 250 μm (JPEG 90 kb)

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Casañas, M.N., Santos, E., Yanes, C. et al. Development of astroglia heterogeneously expressing Pax2, vimentin and GFAP during the ontogeny of the optic pathway of the lizard (Gallotia galloti): an immunohistochemical and ultrastructural study. Cell Tissue Res 345, 295–311 (2011). https://doi.org/10.1007/s00441-011-1211-9

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