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Variations in the proliferative activity of the peripheral retina correlate with postnatal ocular growth in squamate reptiles.

ABSTRACT: The retina is a complex, multilayered tissue responsible for the perception of visual stimuli from the environment. Contrary to mammals, the capacity for postnatal eye growth in fish and amphibians, and to a lower extent in birds, is coordinated with a progenitor population residing in the ciliary marginal zone (CMZ) at the retinal peripheral margin. However, little is known about embryonic retinogenesis and postnatal retinal growth in squamates (lizards, snakes), despite their exceptional array of ecologies and ocular morphologies. Here, we address this gap by performing the first large-scale study assessing both ontogenetic and adult changes in the stem/progenitor activity of the squamate peripheral retina. Our study reveals for the first time that squamates exhibit a source of proliferating progenitors persisting post embryogenesis in a newly identified retinociliary junction anteriorly adjacent to the retina. This region is strikingly similar to the vertebrate CMZ by its peripheral location and pseudostratified nature, and shares a common pattern of slow-cycling cells, spatial differentiation gradient, and response to postnatal ocular growth. Additionally, its proliferative activity varies considerably among squamate species, in correlation with embryonic and postnatal differences in eye size and growth. Together our data indicate that squamates possess a proliferative peripheral retina that acts as a source of progenitors to compensate, at least in part, for postnatal ocular growth. Our findings also highlight the remarkable variation in activity and location of vertebrate retinal progenitors, indicating that the currently accepted scenario of reduced CMZ activity over the course of evolution is too simplistic.

SUBMITTER: Eymann J

PROVIDER: S-EPMC6766921 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The retina is a complex tissue responsible for both detection and primary processing of visual stimuli. Although all vertebrate retinas share a similar, multi-layered organization, the ability to regenerate individual retinal cells varies tremendously, being extremely limited in mammals and birds when compared to anamniotes such as fish and amphibians. However, little is yet known about damage response and regeneration of retinal tissues in "non-classical" squamate reptiles (lizards, snakes), which occupy a key phylogenetic position within amniotes and exhibit unique regenerative features in many tissues. Here, we address this gap by establishing and characterizing a model of excitotoxic retinal damage in bearded dragon lizard (Pogona vitticeps). We particularly focus on identifying, at the cellular and molecular level, a putative endogenous cellular source for retinal regeneration, as diverse self-repair strategies have been characterized in vertebrates using a variety of retinal injury and transgenic models. Our findings reveal for the first time that squamates hold the potential for postnatal retinal regeneration following acute injury. Although no changes occur in the activity of physiologically active progenitors recently identified at the peripheral retinal margin of bearded dragon, two distinct successive populations of proliferating cells at central retina respond to neurotoxin treatment. Following an initial microglia response, a second source of proliferating cells exhibit common hallmarks of vertebrate Müller glia (MG) activation, including cell cycle re-entry, dedifferentiation into a progenitor-like phenotype, and re-expression of proneural markers. The observed lizard glial responses, although not as substantial as in anamniotes, appear more robust than the absent or neonatal-limited regeneration reported without exogenous stimulation in other amniotes. Altogether, these results help to complete our evolutionary understanding of regenerative potential of the vertebrate retina, and further highlight the major importance of glial cells in retinal regeneration. Furthermore, our work offers a new powerful vertebrate model to elucidate the developmental and evolutionary bases of retinal regeneration within amniotes. Such new understanding of self-repair mechanisms in non-classical species endowed with regenerative properties may help designing therapeutic strategies for vertebrate retinal diseases.

Project description:Transposable elements (TEs) are highly abundant in the genome and capable of mobility, two properties that make them particularly prone to transfer horizontally between organisms. Although the impact of horizontal transfer (HT) of TEs is well recognized in prokaryotes, the frequency of this phenomenon and its contribution to genome evolution in eukaryotes remain poorly appreciated. Here, we provide evidence that a DNA transposon called SPIN has colonized the genome of 17 species of reptiles representing nearly every major lineage of squamates, including 14 families of lizards, snakes, and amphisbaenians. Slot blot analyses indicate that SPIN has amplified to high copy numbers in most of these species, ranging from 2,000-28,000 copies per haploid genome. In contrast, we could not detect the presence of SPIN in any of the turtles (seven species from seven families) and crocodiles (four species) examined. Genetic distances between SPIN sequences from species belonging to different squamate families are consistently very low (average = 0.1), considering the deep evolutionary divergence of the families investigated (most are >100 My diverged). Furthermore, these distances fall below interfamilial distances calculated for two genes known to have evolved under strong functional constraint in vertebrates (RAG1, average = 0.24 and C-mos, average = 0.27). These data, combined with phylogenetic analyses, indicate that the widespread distribution of SPIN among squamates is the result of at least 13 independent events of HTs. Molecular dating and paleobiogeographical data suggest that these transfers took place during the last 50 My on at least three different continents (North America, South America and, Africa). Together, these results triple the number of known SPIN transfer events among tetrapods, provide evidence for a previously hypothesized transoceanic movement of SPIN transposons during the Cenozoic, and further underscore the role of HT in the evolution of vertebrate genomes.

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Variations in the proliferative activity of the peripheral retina correlate with postnatal ocular growth in squamate reptiles.

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