Peripapillary glial cells in the chick retina: A special glial cell type expressing astrocyte, radial glia, neuron, and oligodendrocyte markers throughout development

Abstract

Peripapillary glial cells of the chick are a special type of glia, not only because of their position, forming a boundary between the retina on one side and the optic nerve head (ONH) and the pecten on the other, but also because although they have the same orientation and similar shape as the retinal Müller cell (a type of radial glia) and express common markers for these cells and astrocytes, they do not express glutamine synthetase (GS) or carbonic anhydrase C (CA-C), enzymes intensely expressed by Müller cells and astrocytes. In this study, we present further molecular characterization of these cells, using immunohistochemistry techniques. We show that peripapillary glial cells express a novel neuron antigen, 3BA8, that in the adult retina is located only in one neuron type (the amacrine cell) and in the inner plexiform layer (IPL). They also express an antigen specific to myelin and oligodendrocytes, MOSP, and a glial antigen, 3CB2, expressed by radial glia and astrocytes throughout the CNS. The study of the developmental expression of these three antigens in the peripapillary glial cell territory shows different spatiotemporal labeling patterns: 3CB2 and 3BA8 are expressed much earlier (embryonic days E3 and E5, respectively) than MOSP (E12), and during a developmental window (E6-E10) 3BA8 labels the peripapillary glial cells intensely and does not label the ONH or the optic nerve (ON), which are labeled later. The expression of 3CB2 is much more intense in the peripapillary glial cells than in Müller cells from early stages of development up to E16, and the expression of MOSP starts earlier in the peripapillary glial cells than in the Müller cells and is maintained with much higher intensity in the peripapillary glial cells throughout development. These findings show that Müller and peripapillary glial cells follow independent courses of differentiation, which together with the fact that the peripapillary glial cells express molecules typical of neurons, oligodendrocytes, radial glia, and astrocytes are evidence that peripapillary glial cells are a unique type of glia in the CNS.

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

“…The glial subpopulations of the ON and ONH are heterogeneous intra-and inter-specifically within vertebrates (Dávila et al 1987;Lillo et al 2002;Quesada et al 2004;Triviño et al 1996). This seems also to apply to the CP of G. galloti.…”

“…The conus papillaris (CP) is a highly vascularised and pigmented structure typical of the reptilian eye; it projects from the optic nerve head (ONH) into the vitreous chamber and is homologous to the avian pecten oculi (Quesada et al 2004;Wolburg et al 1999) whose main function is the nutrition of the avian avascular retina (Braekevelt 1989;Wolburg et al 1999). 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).…”

Comparative Anatomy of the Optic Nerve Head and Inner Retina in Non-Primate Animal Models Used for Glaucoma Research

“…This group of animals includes the rabbit [4,10], quail , and chicken [4]. In these species, the optic nerve head contains neuronal tissue and astrocytes in addition to oligodendroglia cells [11-13]. …”

“…Similar to the rabbit, partly myelinated axons are localized in the nerve fiber layer in both the quail and the chicken retina [70,71]. Subsequently, oligodendrocytes are located throughout the avian retina with a distinct central-to-peripheral gradient [70,72]. The number of ganglion cells in the avian retina is high and is about twice that of primates (quail: 2,000,000 ganglion cells [73]; chicken: 2,400,000 ganglion cells [74]).…”

Characterization of the antigenic phenotype of αB-crystallin-expressing peripapillary glial cells in the developing chick retina

“…Although Müller cells help in the migration of immature neurons during retinal development, they remain in the retina after migration of ganglion cells ceases. A subpopulation of Müller cells, called peripapillary glial cells (PPGCs), are located adjacent to the optic nerve head (ONH) in the chicken retina [5-7]. PPGCs have a similar shape to Müller cells and bear bidirectional processes; the vitread processes extend toward the vitreous body, and the ventricular processes protrude toward the subretinal space.…”