Analysis of the morphogenesis and cell proliferation in the retina of a pleuronectiform fish, the turbot psetta maxima (Pleuronectiformes: Teleostei)

Abstract

The morphogenesis and cell proliferation in the retina of turbot (Psetta maxima, Pleuronectiformes: Teleostei) from embryo through metamorphosis have been examined by using proliferating cell nuclear antigen (PCNA)-immunohistochemistry and general histological procedures. In the embryonic retina, cell proliferation and spatial cell reorganization form the anlage of the pigment epithelium and neural retina. Neurogenesis begins around hatching in the temporal retina, dorsal to the optic nerve exit, and then a wave of cell differentiation spreads to the nasal retina to yield a laminated retina by the end of the prolarval turbot stage. Germinal zones in the differentiated retina persist as a rim at the retinal margin, as well as surrounding the optic fissure in premetamorphic and metamorphic turbot larvae. In these zones, progenitor cells with different morphologies show a similar spatial arrangement, which suggests that they have a similar retinogenic potential. During metamorphosis, asymmetric proliferative activity in turbot germinal zones is associated with a marked expansion of the retinal tissue. Scattered stem cells in the laminated retina, related to the lineage of rod photoreceptors, were also observed both in large premetamorphic larvae and metamorphic turbots. The proliferative activity of these cells increases considerably during metamorphosis, when rod photoreceptors become morphologically differentiated.

Retinal development in the gilthead seabream Sparus aurata

“…The study reported here shows that the maturation of one of the sensory organs, the eye, also occurs during this period. When hatched, the neuroretina of many species of fishes has a neuroepithelial appearance without any layering, as has been described in other altricial fish species such as the Atlantic halibut Hippoglossus hippoglossus (L. 1758) (Helvik et al, 2001a, b), S. maximus (Doldán et al, 1999;Cid et al, 2013), S. senegalensis (Bejarano-Escobar et al, 2010) and T. tinca (Bejarano-Escobar et al, 2009). On the contrary, in precocial species of fishes, the individual skips the larval period and exits the egg in a juvenile state.…”

“…When hatched, the neuroretina of many species of fishes has a neuroepithelial appearance without any layering, as has been described in other altricial fish species such as the Atlantic halibut Hippoglossus hippoglossus (L. 1758) (Helvik et al , 2001 a , b ), S . maximus (Doldán et al , ; Cid et al , ), S . senegalensis (Bejarano‐Escobar et al , ) and T .…”

“…There is high variability in the development of the fish retina, both intra and interspecifically (Evans & Browman, ). Thus, while altricial fish species, such as the turbot Scophthalmus maximus (L. 1758) (Doldán et al , ; Cid et al , ), the tench Tinca tinca (L. 1758) (Bejarano‐Escobar et al , ) or the Senegalese sole Solea senegalensis Kaup 1858 (Bejarano‐Escobar et al , ) hatch with an undifferentiated retina and do not complete retinal development until late in larval life, precocial fish species, such as the brown trout Salmo trutta L. 1758 (Candal et al , , ), the small spotted catshark Scyliorhinus canicula (L. 1758) (Ferreiro‐Galve et al , 2008, 2010 a , b , 2012; Bejarano‐Escobar et al , 2012 a , 2013) or the brown banded bamboo shark Chiloscyllium punctatum Müller & Henle 1838 (Harahush et al , ) complete their retinal development before hatching. Detailed comparative studies of additional species of fishes, examining maturational features such as histogenesis and cell differentiation, should advance understanding of interspecific differences.…”

Proliferative events and apoptotic remodelling in retinal development of common toad (Bufo bufo)

“…All the cells in which the chromosomes were clearly visible were counted as mitotic figures, whereas pycnotic bodies with nuclei showing chromatin fragmentation or its collapse were considered apoptotic cells. As a control, the observations of mitotic figures have been matched with the immunohistochemistry for Proliferating Cell Nuclear Antigen (PCNA), an established marker for cells in active proliferation (Kurki et al, ; Cid et al, ); while the trend of apoptotic cells was compared to the protein levels of fragmented nuclear poly (ADP‐ribose) polymerase‐1 (PARP‐1), a molecule involved in several programmed cell death paths (Duriez and Shah, ; Chaitanya et al, ).…”

Morphogenesis of the saccus vasculosus of turbot Scophthalmus maximus: assessment of cell proliferation and distribution of parvalbumin and calretinin during ontogeny

“…Overall, development is slow in S . maximus during the embryonic and larval period, and it has been shown that brain and sensory organs achieve a mature appearance and reorganize during metamorphosis (Briñón et al , ; de Miguel et al , ; Prego et al , ; Doldán et al , ; Cid et al , ). This study provides a description of the morphological changes that take place in the developing SV in S .…”