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Size variations in synaptic terminals among different types of photoreceptors and across the zebrafish retina.

ABSTRACT: Photoreceptor synaptic terminals are responsible for transmitting visual information to downstream neurons. In vertebrate retinas, photoreceptor synaptic terminals are of different sizes and structures. The molecular mechanisms that underlie photoreceptor synaptic development are not clearly understood. Here, we have systematically examined the size variations in the synaptic terminals of cone and rod photoreceptors in the adult zebrafish retina. We reveal that the average cone pedicle sizes expand in the order of UV, blue, green, and red cones, echoing the increasing maximally sensitive wavelengths of the opsins expressed in the corresponding cone types. In addition, rod spherules are smaller than all cone pedicles. The terminals of each photoreceptor type also display distinct regional variations across the retina and between males and females. These findings establish the basis for using the zebrafish retina to study the molecular mechanisms that regulate the sizes and structures of photoreceptor terminals for proper visual functions.

SUBMITTER: Park JS

PROVIDER: S-EPMC9918681 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Size variations in synaptic terminals among different types of photoreceptors and across the zebrafish retina.

Park Jong-Su JS Wei Xiangyun X

Experimental eye research 20221230

Photoreceptor synaptic terminals are responsible for transmitting visual information to downstream neurons. In vertebrate retinas, photoreceptor synaptic terminals are of different sizes and structures. The molecular mechanisms that underlie photoreceptor synaptic development are not clearly understood. Here, we have systematically examined the size variations in the synaptic terminals of cone and rod photoreceptors in the adult zebrafish retina. We reveal that the average cone pedicle sizes exp ...[more]

PMID: 36587757

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Project description:BackgroundThe multiplex, lattice mosaic of cone photoreceptors in the adult fish retina is a compelling example of a highly ordered epithelial cell pattern, with single cell width rows and columns of cones and precisely defined neighbor relationships among different cone types. Cellular mechanisms patterning this multiplex mosaic are not understood. Physical models can provide new insights into fundamental mechanisms of biological patterning. In earlier work, we developed a mathematical model of photoreceptor cell packing in the zebrafish retina, which predicted that anisotropic mechanical tension in the retinal epithelium orients planar polarized adhesive interfaces to align the columns as cone photoreceptors are generated at the retinal margin during post-embryonic growth.MethodsWith cell-specific fluorescent reporters and in vivo imaging of the growing retinal margin in transparent juvenile zebrafish we provide the first view of how cell packing, spatial arrangement, and cell identity are coordinated to build the lattice mosaic. With targeted laser ablation we probed the tissue mechanics of the retinal epithelium.ResultsWithin the lattice mosaic, planar polarized Crumbs adhesion proteins pack cones into a single cell width column; between columns, N-cadherin-mediated adherens junctions stabilize Müller glial apical processes. The concentration of activated pMyosin II at these punctate adherens junctions suggests that these glial bands are under tension, forming a physical barrier between cone columns and contributing to mechanical stress anisotropies in the epithelial sheet. Unexpectedly, we discovered that the appearance of such parallel bands of Müller glial apical processes precedes the packing of cones into single cell width columns, hinting at a possible role for glia in the initial organization of the lattice mosaic. Targeted laser ablation of Müller glia directly demonstrates that these glial processes support anisotropic mechanical tension in the planar dimension of the retinal epithelium.ConclusionsThese findings uncovered a novel structural feature of Müller glia associated with alignment of photoreceptors into a lattice mosaic in the zebrafish retina. This is the first demonstration, to our knowledge, of planar, anisotropic mechanical forces mediated by glial cells.

Project description:BackgroundDevelopment of a functional retina depends on regulated differentiation of several types of neurons and generation of a highly complex network between the different types of neurons. In addition, each type of retinal neuron includes several distinct morphological types. Very little is known about the mechanisms responsible for generating this diversity of retinal neurons, which may also display specific patterns of regional distribution.ResultsIn a screen in zebrafish, using a trapping vector carrying an engineered yeast Gal4 transcription activator and a UAS:eGFP reporter cassette, we have identified two transgenic lines of zebrafish co-expressing eGFP and Gal4 in specific subsets of retinal bipolar cells. The eGFP-labelling facilitated analysis of axon terminals within the inner plexiform layer of the adult retina and showed that the fluorescent bipolar cells correspond to previously defined morphological types. Strong regional restriction of eGFP-positive bipolar cells to the central part of the retina surrounding the optic nerve was observed in adult zebrafish. Furthermore, we achieved specific ablation of the labelled bipolar cells in 5 days old larvae, using a bacterial nitroreductase gene under Gal4-UAS control in combination with the prodrug metronidazole. Following prodrug treatment, nitroreductase expressing bipolar cells were efficiently ablated without affecting surrounding retina architecture, and recovery occurred within a few days due to increased generation of new bipolar cells.ConclusionThis report shows that enhancer trapping can be applied to label distinct morphological types of bipolar cells in the zebrafish retina. The genetic labelling of these cells yielded co-expression of a modified Gal4 transcription activator and the fluorescent marker eGFP. Our work also demonstrates the potential utility of the Gal4-UAS system for induction of other transgenes, including a bacterial nitroreductase fusion gene, which can facilitate analysis of bipolar cell differentiation and how the retina recovers from specific ablation of these cells.

Dataset Information

Size variations in synaptic terminals among different types of photoreceptors and across the zebrafish retina.

Publications

Size variations in synaptic terminals among different types of photoreceptors and across the zebrafish retina.

Similar Datasets

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