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Antón Barreiro-Iglesias
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Barreiro-Iglesias, A. Proliferative Activity in Zebrafish Retina. Encyclopedia. Available online: https://encyclopedia.pub/entry/16719 (accessed on 01 December 2023).
Barreiro-Iglesias A. Proliferative Activity in Zebrafish Retina. Encyclopedia. Available at: https://encyclopedia.pub/entry/16719. Accessed December 01, 2023.
Barreiro-Iglesias, Antón. "Proliferative Activity in Zebrafish Retina" Encyclopedia, https://encyclopedia.pub/entry/16719 (accessed December 01, 2023).
Barreiro-Iglesias, A.(2021, December 03). Proliferative Activity in Zebrafish Retina. In Encyclopedia. https://encyclopedia.pub/entry/16719
Barreiro-Iglesias, Antón. "Proliferative Activity in Zebrafish Retina." Encyclopedia. Web. 03 December, 2021.
Proliferative Activity in Zebrafish Retina
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This entry is adapted from the peer-reviewed paper 10.3390/ijms222111715

Researchers performed a systematic and comparative study of the constitutive proliferative activity of the retina from early developing (2 days post-fertilisation) to aged (up to 3–4 years post-fertilisation) zebrafish. 

Zebrafish Retina neurogenic proliferative

1. Introduction

Neurogenesis is the process by which neural progenitor cells give rise to mature neurons and glial cells. Early in development, the central nervous system (CNS) is formed from a highly active neurogenic neuroepithelium. As development progresses, proliferative and neurogenic activities are gradually lost in most CNS regions, and, in postnatal life, neurogenic activity is restricted to specific regions called neurogenic niches [1][2]. Moreover, the presence of postnatal neurogenic activity in the CNS was also progressively lost during vertebrate evolution (reviewed in [3][4][5][6][7][8]). Accordingly, different vertebrate species show different postnatal/adult proliferative and neurogenic rates and different numbers of neurogenic niches in the CNS, which are more abundant in teleost fishes (reviewed in [3][4][5][6][7][8][9]). Some postnatal constitutive and/or inducible (e.g., during regeneration) neurogenic niches are found in the retina of vertebrates. These include the ciliary marginal zone (CMZ), which is a circumferential ring of cells located in the peripheral retina [10][11][12][13][14][15]; the Müller glial cells of the inner nuclear layer (INL) of the central retina [12][16][17][18][19]; the retinal pigment epithelium (RPE; [20][21][22]), a pseudostratified region at the junction between the retina and the ciliary body [23]; and the pigmented and non-pigmented epithelium of the ciliary body [24][25][26][27][28]. The proliferative and neurogenic capacities of each of these retinal neurogenic niches varies in different vertebrate species (reviewed in [19][29][30][31]). In fishes, all retinal cell types, except rod photoreceptors, are generated within the CMZ and incorporated to the most peripheral region of the central retina (so that older cells remain in the central retina and new cells become located successively in more peripheral positions). Instead, rod photoreceptors are continuously generated from Müller glia in the central retina.
Based on studies in teleost species, it is largely assumed that the retina of fishes, in contrast to mammals, has continuous proliferative activity throughout life and that this (together with tissue stretching) is partially responsible for continuous eye growth, even during adulthood. This idea emerges in relevant articles on this topic during the last decades: “Fish retinas differ fundamentally from those of other vertebrates because they continue to grow throughout the life of the animal, both by adding new neurons and by stretching existing retinal tissue” [32]; “In fish and amphibia, retinal stem cells located in the periphery of the retina, the ciliary marginal zone (CMZ), produce new neurons in the retina throughout life” [33]; “The retina of many fish and amphibians grows throughout life, roughly matching the overall growth of the animal. The new retinal cells are continually added at the anterior margin of the retina, in a circumferential zone of cells” [34]; “The retinas of lower vertebrates grow throughout life from retinal stem cells (RSCs) and retinal progenitor cells (RPCs) at the rim of the retina” [35]; “In the retina of teleost fish, cell addition continues throughout life involving proliferation and axonal growth” [36], to name a few. However, studies in the sea lamprey, Petromyzon marinus, and the catshark, Scyliorhinus canicula, revealed the loss of proliferative activity in the retina of adult individuals of these ancient vertebrate groups [37][38]. This raised the possibility that continuous proliferative activity throughout life in the retina was a derived characteristic of modern teleost fishes and not the ancestral character common to all fish groups [38].

2. Current Studies

It is largely assumed that the retina of fishes shows continuous and active proliferation and neurogenesis throughout life. This assumption is based on previous work in teleost models in which the presence of proliferating cells was only studied in juveniles or young adults, in animals in which the precise age was not defined or known by the authors of the study, or without performing quantitative comparisons between all life stages or ages. This feature of throughout-life neurogenesis does not apply to lampreys or cartilaginous fishes, in which proliferative activity is virtually absent in adult animals [37][38]. Moreover, some of the previous studies on teleost fishes provided qualitative descriptions that also suggested a loss of proliferating cells with age. For example, Johns and Fernald [39] reported that, when studying African cichlid and goldfish juveniles and adults, the dividing cells in the ONL were easier to demonstrate in younger fish. In zebrafish, Marcus et al. [40] also indicated that the number of BrdU labelled cells was greater in the CMZ and central retina of embryos than in young adults (6–8 mpf). A recent study by Van Houcke et al. [41] showed a decline in the cell proliferation (PCNA+ cells) in the zebrafish CMZ from 6 to 48 mpf. However, the proliferation within the central retina of zebrafish was not quantified over time. Besides, the assessment of progenitor cell proliferation relied only on PCNA expression, which, despite its use, can lead to the overestimation of proliferation in aged animals (see the Introduction).
Here, researchers obtained quantitative data comparing the cell cycle progression (PCNA+ cells/section) and mitotic activity (pH3+ cells/section) in both the CMZ and the central zebrafish retina at different ages and covering all major life stages. Results show that there is a drastic decline in proliferative activity from 2 to 7 dpf, a continuous reduction in the number of proliferating cells in sexually maturing and old animals, and that cells undergoing mitosis are virtually absent in old animals. This is in good agreement with previous reports of a drastic decrease in cell proliferation in early larvae (between the 3 dpf and 4 dpf; [40]) and with reports of a significant proliferation decrease in early adulthood (6–12 mpf), with very reduced proliferation rates at the mid (18–24 mpf) and late (36–38 mpf) adult stages [41]. As expected, the number of PCNA+ cells reported in the CMZ by Van Houcke et al. [41] was higher than that of pH3+ cells in this region at similar life stages (present results) since the latter are only a fraction of the number of cells progressing through the cell cycle. Results in zebrafish reveal a similar pattern to that reported in lampreys and sharks showing a loss of the proliferating and mitotic cells in the adult retina [37][38]. However, it seems that retinal proliferative activity is maintained at a higher rate in adult zebrafish than in adult lampreys (no PCNA+ cells; [37]) or sharks (very few PCNA+ cells and almost no pH3+ cells; [38]).
Unlike previous reports on the proliferation in the zebrafish retina, the new systematic analysis allowed unveiling the occurrence of a secondary wave of proliferation during sexual maturation (i.e., from 1.5 to 3 mpf) affecting both the CMZ and the central retina. Only a study by Bernardos et al. [17] provided a qualitative description indicating that BrdU+ cells in the ONL were observed in higher numbers in 1 to 2 mpf animals than in 7 dpf animals. This increase in the cell proliferation at 1.5 mpf (present results) did not reach the levels of the early developing (2 dpf) period, but it was significantly higher than in the 7 dpf specimens. This secondary wave of proliferation could be related to an earlier peak of cell death that occurs in the retina (especially in the ONL) of 7 dpf zebrafish [42]. This increase in cell proliferation could allow for the replacement of the cells lost during this critical period in which fish transition from acquiring nutrition from their yolk to active feeding. This secondary wave of proliferation could also be related to retinal adaptations that might be needed for sexual behaviours, especially since the integration of multi-sensory information between olfaction and vision has been implicated in mating-like behaviours in zebrafish [43]. However, current data have only implicated dopaminergic interplexiform and retinal ganglion cells in this olfacto–visual centrifugal pathway [43], which would not explain why proliferation and neurogenesis are needed in the ONL (see below). Future studies should decipher whether this secondary wave of proliferation is only needed to replace lost retinal cells or if it is related to retinal adaptations needed for sexual (or adult) behaviours in zebrafish.
By looking at the distribution of the proliferating/mitotic cells in the cell layers of the central retina at different ages, researchers observed that, in early developing 4 dpf specimens, the numbers of pH3+ and PCNA+ cells were higher in the INL, whereas, in older animals, they were more abundant in the ONL. Previous studies have shown that the progenitor cells of the central retina (Müller glia) in juvenile/adult goldfish [39][44][45] and in juvenile zebrafish [17][46][47][48] generate new rods, which indicates that the higher cell proliferation and mitotic activity researchers observed in the ONL of juvenile and adult zebrafish is related to rod generation. As far as researchers are aware, the generation of other retinal cell types from the INL and ONL progenitors of the un-injured juvenile/adult teleost retina has not been reported, although injury-induced proliferating Müller glial cells can regenerate all the retinal cell types, including cones [17][46][47][48], which has led to the suggestion that the neuronal progenitors produced by Müller glia are multipotent and can revert to an earlier lineage under the influence of certain microenvironmental signals [17][46][47][49]. The zebrafish retina presents five main types of photoreceptors (four cones and one rod), and the five types of photoreceptors are generated during early development [50][51]. Perhaps one or more of these photoreceptor types are specifically needed for mating/courtship/adult behaviours and could be generated in extra numbers during sexual maturation, which could explain the secondary wave of cell proliferation researchers detected in zebrafish juveniles. Since, during courtship and spawning, female zebrafish discriminate between the sexes using visual cues in which the male yellow colouration is critical [51], it is tempting to hypothesise that specific cones might be needed at this life stage. However, microenviromental signals other than retinal injury driving cone generation from progenitors in the central retina have not been experimentally assessed. Future work should attempt to study whether cones could also be generated from these dividing progenitor cells of the central retina, especially during the previously undetected secondary wave of proliferation at the time of sexual maturation.

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