Retinal differentiation in syngnathids: comparison in the developmental rate and acquisition of retinal structures in altricial and precocial fish species

Álvarez-Hernán, Guadalupe; Andrade, J.P.; Escarabajal-Blázquez, Laura; Blasco, Manuel; Solana-Fajardo, Jorge; Martı́n-Partido, Gervasio; Francisco-Morcillo, Javier

doi:10.1007/s00435-019-00447-3

Cited by 11 publications

(7 citation statements)

References 81 publications

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“…Furthermore, ontogenetic events that are restricted to the embryonic retina in precocial bird species such as cell death ( Cook et al, 1998 ; Marín-Teva et al, 1999 ; Francisco-Morcillo et al, 2014 ) are detected in the altricial bird retina during the first week of life ( Álvarez-Hernán et al, 2021b ). A high abundance of proliferative progenitors has been also described in the retina of altricial newly hatched fish ( Evans and Browman, 2004 ; Bejarano-Escobar et al, 2014 ; Pavón-Muñoz et al, 2016 ; Álvarez-Hernán et al, 2019 ) and new-borns of altricial mammals ( Palatroni et al, 1990 ). In contrast, newly hatched individuals of C. coturnix present a functional visual system with a totally differentiated retina in which mitotic activity is almost absent, as has been previously shown in the precocial retina of G. gallus ( Fischer and Reh, 2000 ; Álvarez-Hernán et al, 2021a ).…”

Section: Discussionmentioning

confidence: 93%

Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development

et al. 2022

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During development of the vertebrate retina, mitotic activity is defined as apical when is located at the external surface of the neuroepithelium or as non-apical when is found in more internal regions. Apical mitoses give rise to all retinal cell types. Non-apical mitoses are linked to committed horizontal cell precursors that subsequently migrate vitreo-sclerally, reaching their final position in the outer surface of the inner nuclear layer, where they differentiate. Previous studies have suggested differences in the timing of retinal maturation between altricial and precocial bird species. In the present study we analyze qualitatively and quantitatively the mitotic activity in the developing retina of an altricial (zebra finch, Taeniopygia guttata) and a precocial (Japanese quail, Coturnix coturnix) bird species. We found that pHisH3-immunoreactive apical and non-apical mitoses were abundant in the T. guttata retina at the hatching stage. In contrast, pHisH3 immunoreactivity almost disappeared from the quail retina at the embryonic day 10 (E10). Furthermore, we also found that the onset of the appearance of non-apical mitoses occurred at later stages in the altricial bird species than in the precocial one. The disappearance of apical mitoses and the spatiotemporal distribution of non-apical mitoses followed central to peripheral and dorsal to ventral gradients, similar to gradients of cell differentiation described in the retina of birds. Therefore, these results suggest that retinal neurogenesis is active at the hatching stage in T. guttata, and that horizontal cell differentiation is delayed in the altricial bird species compared to the precocial one. Together, this study reveals important insights into the timing differences that regulate bird retinal maturation and provides a better understanding of the evolution of avian altriciality and precociality.

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Section: Discussionmentioning

confidence: 93%

Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development

et al. 2022

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“…The vertebrate retina contains six well-known types of neurons – ganglion, amacrine, horizontal, bipolar, cone, and rod cells. Much is known about the intrinsic programs (mainly coded by transcription factors, but also by extrinsic factors such as growth factors) which are involved in retinogenesis and in the maintenance of neuronal phenotypes ( Álvarez-Hernán et al, 2013 , 2018 , 2019 , 2020 ; Xiang, 2013 ; Bejarano-Escobar et al, 2014 , 2015 ). Furthermore, several phases of cell death have been reported to occur during development of the vertebrate retina ( Cook et al, 1998 ; Knabe et al, 2000 ; Péquignot et al, 2003 ; Francisco-Morcillo et al, 2004 , 2014 ; Rodríguez-Gallardo et al, 2005 ; Chavarría et al, 2007 , 2013 ; Valenciano et al, 2009 ; Bejarano-Escobar et al, 2011 , 2013 ).…”

Section: Sa-β-gal Staining In the Developing Embryomentioning

confidence: 99%

Is Senescence-Associated β-Galactosidase a Reliable in vivo Marker of Cellular Senescence During Embryonic Development?

Mera-Rodríguez

Álvarez-Hernán

Gañán

et al. 2021

Front. Cell Dev. Biol.

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During vertebrate embryonic development, cellular senescence occurs at multiple locations. To date, it has been accepted that when there has been induction of senescence in an embryonic tissue, β-galactosidase activity is detectable at a pH as high as 6.0, and this has been extensively used as a marker of cellular senescence in vivo in both whole-mount and cryosections. Such senescence-associated β-galactosidase (SA-β-GAL) labeling appears enhanced in degenerating regions of the vertebrate embryo that are also affected by programmed cell death. In this sense, there is a strong SA-β-GAL signal which overlaps with the pattern of cell death in the interdigital tissue of the developing limbs, and indeed, many of the labeled cells detected go on to subsequently undergo apoptosis. However, it has been reported that β-GAL activity at pH 6.0 is also enhanced in healthy neurons, and some retinal neurons are strongly labeled with this histochemical technique when they begin to differentiate during early embryonic development. These labeled early post-mitotic neurons also express other senescence markers such as p21. Therefore, the reliability of this histochemical technique in studying senescence in cells such as neurons that undergo prolonged and irreversible cell-cycle arrest is questionable because it is also expressed in healthy post-mitotic cells. The identification of new biomarkers of cellular senescence would, in combination with established markers, increase the specificity and efficiency of detecting cellular senescence in embryonic and healthy mature tissues.

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“…It has been proposed that structures that become postmitotic late in development become more enlarged that structures that are born earlier, that is, that the telencephalon in vertebrates tends to be disproportionally large because neurogenesis in this region is generally Early vs. delayed and extended telencephalic neurogenesis in birds has been related to precociality vs. altriciality (Charvet and Striedter 2011). The altricial-precocial spectrum describes the degree of morphological maturation of offspring at the moment of hatching (Álvarez-Hernán et al 2019). In fish, precocial species hatch at an advanced stage of development, while altricial species hatch at a less developed stage.…”

Section: Telencephalic Proliferation Across Evolution: the Origin Of Adult Neurogenesismentioning

confidence: 99%

Characterization of neurogenic niches in the telencephalon of juvenile and adult sharks

Docampo-Seara¹,

Pereira-Guldrís²,

Sánchez-Farías³

et al. 2020

Brain Struct Funct

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Neurogenesis is a multistep process by which progenitor cells become terminally differentiated neurons. Adult neurogenesis has gathered increasing interest with the aim of developing new cell-based treatments for neurodegenerative diseases in humans. Active sites of adult neurogenesis exist from fish to mammals, although in the adult mammalian brain the number and extension of neurogenic areas is considerably reduced in comparison to non-mammalian vertebrates and they become mostly reduced to the telencephalon. Much of our understanding in this field is based in studies on mammals and zebrafish, a modern bony fish. The use of the cartilaginous fish Scyliorhinus canicula (representative of basal gnathostomes) as a model expands the comparative framework to a species that shows highly neurogenic activity in the adult brain. In this work, we studied the proliferation pattern in the telencephalon of juvenile and adult specimens of S. canicula using antibodies against the proliferation marker proliferating cell nuclear antigen (PCNA). We have characterized proliferating niches using stem cell markers (Sex determining region Y-box 2), glial markers (glial fibrillary acidic protein, brain lipid binding protein and glutamine synthase), intermediate progenitor cell markers (Dlx2 and Tbr2) and markers for migrating neuroblasts (Doublecortin). Based in the expression pattern of these markers, we demonstrate the existence of different cell subtypes within the PCNA immunoreactive zones including non-glial stem cells, glial progenitors, intermediate progenitor-like cells and migratory neuroblasts, which were widely distributed in the ventricular zone of the pallium, suggesting that the main progenitor types that constitute the neurogenic niche in mammals are already present in cartilaginous fishes.

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Retinal differentiation in syngnathids: comparison in the developmental rate and acquisition of retinal structures in altricial and precocial fish species

Cited by 11 publications

References 81 publications

Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development

Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development

Is Senescence-Associated β-Galactosidase a Reliable in vivo Marker of Cellular Senescence During Embryonic Development?

Characterization of neurogenic niches in the telencephalon of juvenile and adult sharks

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