Investigation of the migration path for new rod photoreceptors in the adult cichlid fish retina (original) (raw)
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Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas
Journal of Chemical Neuroanatomy, 2010
We studied the pattern of cell proliferation and its relation with photoreceptor differentiation in the embryonic and postembryonic retina of two elasmobranchs, the lesser spotted dogfish (Scyliorhinus canicula) and the brown shyshark (Haploblepharus fuscus). Cell proliferation was studied with antibodies raised against proliferating cell nuclear antigen (PCNA) and phospho-histone-H3, and early photoreceptor differentiation with an antibody raised against rod opsin. As regards the spatiotemporal distribution of PCNA-immunoreactive cells, our results reveal a gradual loss of PCNA that coincides in a spatiotemporal sequence with the gradient of layer maturation. The presence of a peripheral growth zone containing pure-proliferating retinal progenitors (the ciliary marginal zone) in the adult retina matches with the general pattern observed in other groups of gnathostomous fishes. However, in the shark retina the generation of new cells is not restricted to the ciliary marginal zone but also occurs in retinal areas that contain differentiated cells: (1) in a transition zone that lies between the pureproliferating ciliary marginal zone and the central (layered) retina; (2) in the differentiating central area up to prehatching embryos where large amounts of PCNA-positive cells were observed even in the inner and outer nuclear layers; (3) and in the retinal pigment epithelium of prehatching embryos. Rod opsin immunoreactivity was observed in both species when the outer plexiform layer begins to be recognized in the central retina and, as we previously observed in trout, coincided temporally with the weakening in PCNA labelling.
The embryogenesis of rod photoreceptors in the teleost fish retina, Haplochromis burtoni
Developmental Brain Research, 1998
Development of the retina, like that of other tissues, occurs via an orderly sequence of cell division and differentiation, producing the functional retina. In teleost fish, however, cell division and differentiation in the retina continue throughout the life of the animal in two distinct ways. Stem cells in a circumferential germinal zone at the periphery of the retina give rise to all retinal cell types and progenitor Ž . cells located throughout the retina in the outer nuclear layer ONL produce new rod photoreceptors. These processes in adult retina recapitulate in space the embryonic events responsible for forming the retina. Analysis of these events in an African cichlid fish, Haplochromis burtoni, confirmed that cone photoreceptors differentiate first, followed by rod photoreceptors. Correspondingly, at the margin of the eye, cone photoreceptors differentiate nearer to the margin than do rods. Control of photoreceptor production is not understood. Here we present the time of appearance and distribution pattern of GABA and vimentin which are candidates for the control of retinal cell division and differentiation. Antibody staining reveals that both GABA and vimentin exhibit unique patterns of expression during embryonic retinal development. Vimentin immunoreactivity is evident throughout the retina in a spoke-like pattern between developmental Days 4 and 7, as both cone and rod photoreceptors are being formed. GABA is expressed in horizontal cells between Days 5 and 7, corresponding to the onset of rod differentiation in time and in position within the retina. Moreover, the wave of GABAergic staining in the horizontal cells parallels the wave of rod differentiation across the embryonic retina of H. burtoni. Thus, GABA may play a role in the development of rod photoreceptors. q
Neuroscience, 2007
In the retina of many lower vertebrates, the arrangement of cells, in particular of cone photoreceptors, is highly regular. The data presented in this report show that in the retina of a cichlid fish (Astatotilapia burtoni) the regular arrangement is not restricted to cone photoreceptors and their synaptic terminals but can be found in elements of the inner retina as well. A variety of immunocytochemical and other markers was used in combination with confocal microscopy on whole-mount preparations and tangential sections. Nearest neighbor analysis was performed and density recovery profiles as auto-and cross-correlograms were generated. Cells displaying a regular arrangement of their synaptic processes in matching radial register to each other were identified for each major retinal neuronal cell type except ganglion cells (i.e. photoreceptors, horizontal cells, bipolar cells, and amacrine cells). The precise location of some of the corresponding cell bodies was not as regular but still non-random, however there was no spatial cross-correlation between cell bodies of different types. The radial processes of Müller glial cells displayed a distribution correlating to the arrangement of photoreceptors and neurons. Thus, for one Müller glial cell I found two PKC-positive cone bipolar cells, a spatially corresponding grid of parvalbumin-positive amacrine cell processes, one H1 horizontal cell, and two pairs of double cones. There was no evidence among ganglion cells matching this pattern, possibly due to the lack of suitable markers. Although many other cell types do not follow this matching regular mosaic arrangement, a basic columnar building block can be postulated for the retina at least in cichlid fish. This suggests a functional radial unit from photoreceptors to the inner plexiform layer.
Cell movement and cell cycle dynamics in the retina of the adult teleost Haplochromis burtoni
The Journal of Comparative Neurology, 1997
The authors analyzed the pattern of neurogenesis, the time frame of cell movement, and the cell cycle kinetics of a population of stem cells located in the outer nuclear layer in the retina of the adult teleost Haplochromis burtoni. These stem cells continue to give rise to new rod photoreceptors throughout life. The new rods move vitread after the last cell division. The authors investigated events during cell division and cell differentiation by using one marker that labels dividing cells transiently (proliferating cell nuclear antigen) along with another marker that labels dividing cells permanently (bromodeoxyuridine). The bulk of cell movement does not occur within 24 hours after S-phase labeling but is clearly underway 12 hours later, shortly after mitosis. The cell cycle length was estimated to be approximately 25 hours. The distribution of labeled cells at various times after S-phase suggests that new rods are generated by asymmetric cell division, that is, one of the daughter cells moves after mitosis and becomes postmitotic, while the other daughter cell remains in place and reenters the cell cycle. The proliferation patterns across the retina suggest that the location of areas of mitotic activity changes over time. The authors hypothesize that local extracellular factors control the rate of cell division in a given area, thereby keeping the overall rod density constant.
Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss)
The Journal of Comparative Neurology, 2003
In order to facilitate emerging models of retinal development, we developed electroretinogram and in situ hybridization protocols to examine the ontogeny of photoreceptors in the retina of a land-locked salmonid, the rainbow trout (Oncorhynchus mykiss). We cloned cDNA fragments corresponding to the rod opsin and each of the four cone opsin gene families, which we utilized to produce riboprobes. We established the specificity of the in situ hybridization protocol by examining subcellular signal localization and through double-labeling experiments. We confirm the assumption that the accessory corner cones in the square mosaic are the ultraviolet wavelength-sensitive (UVS) cone photoreceptor (i.e., they express an SWS1 opsin) and observed UVS cones throughout the retina of small trout. Larger fish have a decrease in sensitivity to short wavelength light stimuli and the distribution of UVS cones in the mature retina is limited to the dorsal-temporal quadrant. These larger fish also possess differentiated UVS cones in the peripheral germinal zone (PGZ), including within areas peripheral to mature retina lacking UVS cones. These data are consistent with the loss of putative UVS cones from the PGZ of a migratory salmonid of another genus, and thus the disappearance of UVS cones appears to be general to the Family Salmonidae, regardless of life history strategy. The generation, differentiation, and subsequent loss of UVS cones in the smolt PGZ is a dramatic example of the supposition that the mechanisms of PGZ development recapitulate the retinal embryogenesis of that species.
The Journal of Comparative Neurology, 1985
The organization of retinofugal projections was studied in a cichlid fish 'by labelling small groups of retinal ganglion cell axons with either horseradish peroxidase or cobaltous lysine. Two major findings resulted from these (experiments. First, optic tract axons show a greater degree of pathway diversity than was previously appreciated, and this pathway diversity is related to the target nuclei of groups of axons. The most striking example is the formation of the medial optic tract. Fibers that will become the medial optic tract move abruptly away from their neighbors, at about the level of the optic chiasm, and coalesce at the dorsomedial edge of the marginal optic tract. The medial optic tract projects to the thalamus, the dorsal pretectum, and the deep layer of the optic tectum. The axial optic tract is a group of fibers which segregates from 1,he most medial portion of the marginal optic tract, at about the level of the optic chiasm. The axial tract stays medial to the marginal optic tract for a few hundred microns and then curves laterally to rejoin the marginal optic tract. At least some axial trat axons terminate in the suprachiasmatic nucleus. Within the marginal optic tract, retinal ganglion cell axons from a given retinal quadrant are always segregated into at least two groups. The smaller group projects to the superficial pretectal nucleus. The larger group projects to the superficial layer of the optic tectum.
Developmental Brain Research, 1983
Key words: retina --fish development --neuronal death --NOR development --retinopetal innervation -transcellular HRP-labelling Adult patterns and the development of the nucleus of origin of centrifugal innervation of the retina, the nucleus olfacto-retinalis (NOR), were studied with horseradish peroxidase in 2 cichlid fish species. In the adults large and small cells within the nuclear boundaries can be distinguished by their cytoarchitecture and their HRP-labelling. The NOR is already formed at hatching (5.5 days postspawning) but cannot be filled by HRP injections into one eye until 2 days later. The number of labelled neurons increases steadily until adult cell density is reached. Later larval stages show that the NOR neurons also increase in size. The two cell types found in the adult can first be distinguished at around 30 days post-spawning. Early unilateral enucleation reduces the density of the small cells in the contralateral NOR. In spite of different environmental constraints on the growth of the larvae, the NOR develops in a similar way in both species but always somewhat later in the substrate-spawner than in the mouth-brooder. The centrifugal innervation of bird (isthmo-optic nucleus, ION) and fish (NOR) retinae starts at comparable developmental stages of the retina, but no cell death as found in the developing ION in birds occurs in the developing NOR in fish. It is suggested that this is due to the constant adjustment of the NOR to the ever increasing cell numbers in the fish retina. The NOR is thus the only known centrifugally projecting nucleus in vertebrates which lacks extensive degenerating patterns during early development. The known LH-RH immunoreactivity, the two cell types, the early development, and the projection to the retina of the NOR in cichlid fish resemble closely characteristics of the ganglion of the terminalis nerve of other piscine species.
Patterns of rod proliferation in deep-sea fish retinae
Vision research, 1995
In a sample of 37 species of deep-sea fish species from the sea floor of the Porcupine Seabight and the Gobal spur (North Atlantic) we investigated the overall structure of the retina with special respect for the organization of rods, their length and their arrangement in multiple banks. Using an immunocytochemical marker for cell proliferation (PCNA) we studied the mechanisms of rod proliferation, and, by means of serial section reconstruction followed their integration into the existing population of rods. Furthermore, in three different species we have observed growth related changes in retinal thickness, rod density and proliferation activity. We found evidence for two different principles for the organization of rods in these deep-sea fish retinae. In the first group of species represented by Nematonurus armatus and Coryphaenoides guentheri we found rods to be rather short (20-30 microns) and arranged in three and more banks. In these species rod proliferation occurred in a sin...
Rod Outer Segment Renewal in the Retinae of Deep-sea Fish
Vision Research, 1996
Outer segment renewal involves the synthesis of disc material in the photoreceptor inner segments, the shedding of the tips of the photoreceptor outer segments, and their phagocytosis by the retinal pigment epithelial cells. It has been suggested that in the retinae of deep-sea fish no renewal of outer segments may take place. In order to assess enter segment renewal in deep-sea fish retinae we counted (i) pericilim'y vesicles in rod inner segments as a parameter for disc-synthesis activity and (ii) phagosomes in retinal pigment epithelial cells as a parameter of shedding and phagocytosis in 12 species of deep-sea fish with multibank or single bank retinae. We also measured the lengths of rod outer segments in order to evaluate the balance between synthesis and phagocytotic activity. In four of these species (Syr.
Investigative Ophthalmology & Visual Science, 2004
Fish grow throughout life, including enlargement of eye and retina. Retinal growth involves several mechanisms of adjustment, such as cell addition and dendritic growth. To discover possible other means with which the animals adjust to changing eye size, the distribution of displaced amacrine cells (DACs) and ganglion cells (GCs) was analyzed in the retina of three sizes of a South American cichlid, the blue arcara Aequidens pulcher. DACs were identified by staining with antibodies specific for the calcium-binding protein parvalbumin. They were also weakly positive for staining against choline acetyl transferase (ChaT). GCs were labeled retrogradely with rhodamine dextran. Densities for both DACs and GCs were lower in the retinas of large fish. To distinguish changes due to eye size from specific adjustments, the proportions of DACs to GCs were examined, rather than the absolute cell densities, in various retinal regions in cryostat sections and wholemount preparations from fish of the three sizes. The analyses suggest that, in small and large fish, DACs and GCs were produced in similar proportions (ratio of DACs to GCs, approximately 0.62) in the retinal periphery where new retinal tissue was added by the germinal zone. However, in the central retina of large fish, this proportion was shifted toward GCs (DAC-GC ratio as low as 0.25). During growth of the eye, the proportion of DACs in the ganglion cell layer decreases, indicating that these cells are eliminated from the ganglion cell layer by some unknown mechanism.