Quantitative evaluation of the distribution of proliferating cells in the adult retina in three cyprinid species

Abstract

In the present study, a descriptive and quantitative analysis of all the proliferating cell populations present in the normal adult retina of three cyprinid species (goldfish, zebrafish, and tench) is reported. Evaluation of cell proliferation was performed in proliferating cell nuclear antigen (PCNA)-labeled tissue sections as well as in single-cell suspensions analyzed by flow cytometry. Our results show that the neural progenitors of the inner nuclear layer (INL) of cyprinids continue dividing in adulthood in uninjured retinas. These cells are probably related to the generation of rods in normal retinal growth, as well as in the production of any retinal cell type in regenerating processes. The distributions of both these cells and their presumptive progeny, the rod precursors, differ from one species to another, being homogeneous in zebrafish, displaced to the periphery in goldfish and to the temporal pole in tench. With regard to the cell apposition at the retinal periphery, it seems to be symmetrical in goldfish and zebrafish, based on a homogeneous extension of the peripheral growth zone (PGZ), but asymmetrical in tench, where it presents a significantly lower extension in the ventral retina. The flow cytometry analyses indicate that, overall, the proportion of proliferating cells is significantly greater in zebrafish retina despite the fact that body growth rate is lower in zebrafish than the other two species.

Eye development and retinal differentiation in an altricial fish species, the senegalese sole (Solea senegalensis, Kaup 1858)

“…The differentiation process in the fish retina can be analyzed by monitoring the chronotopographical appearance of the layered retinal structure and functional synapses, the arrest of proliferative activity, or the appearance of a variety of neurochemical macromolecules selectively expressed by retinal cell types (Sandy and Blaxter, '80; Sharma and Ungar, '80; Vecino et al, '93; Kvenseth et al, '96; de Miguel Villegas et al, '97; Hagedorn et al, '98; Doldán et al, '99; Hu and Easter, '99; Helvik et al, 2001; Peterson et al, 2001; Mader and Cameron, 2004; Candal et al, 2005a, 2008; Arenzana et al, 2006; Kitambi and Malicki, 2008; Bejarano‐Escobar et al, 2009). Proliferating cell nuclear antigen (PCNA), an antigen expressed in the nuclei of cells during DNA replication, has previously been used to identify proliferating precursor cells in the teleost fish retina (Mack and Fernald, '97; Velasco et al, 2001; Cid et al, 2002; Candal et al, 2005a; Bernardos et al, 2007; Thummel et al, 2008; Bejarano‐Escobar et al, 2009). Thus, PCNA immunoreactivity has been observed in the juvenile and adult fish retina in different neurogenic niches, such as a neuroepithelial cell population located in the marginal edge of the retina that is called the circumferential germinal zone (CGZ), and proliferative cells located in the microenvironment around some Müller glia and in the outer nuclear layer (ONL) (Julian et al, '98; Otteson et al, 2001; Cid et al, 2002; Raymond et al, 2006; Bernardos et al, 2007; Thummel et al, 2008; Bejarano‐Escobar et al, 2009).…”

“…Proliferating cell nuclear antigen (PCNA), an antigen expressed in the nuclei of cells during DNA replication, has previously been used to identify proliferating precursor cells in the teleost fish retina (Mack and Fernald, '97; Velasco et al, 2001; Cid et al, 2002; Candal et al, 2005a; Bernardos et al, 2007; Thummel et al, 2008; Bejarano‐Escobar et al, 2009). Thus, PCNA immunoreactivity has been observed in the juvenile and adult fish retina in different neurogenic niches, such as a neuroepithelial cell population located in the marginal edge of the retina that is called the circumferential germinal zone (CGZ), and proliferative cells located in the microenvironment around some Müller glia and in the outer nuclear layer (ONL) (Julian et al, '98; Otteson et al, 2001; Cid et al, 2002; Raymond et al, 2006; Bernardos et al, 2007; Thummel et al, 2008; Bejarano‐Escobar et al, 2009). Electron microscopy has commonly been used to verify the presence of morphological synapses in the plexiform layers during fish retinal development (Schmitt and Dowling, '99).…”

Ontogeny of ultraviolet‐sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss)

“…This population of cells had been identified in larval fish (Hagedorn and Fernald, 1992;Johns, 1982). Subsequent to Julian et al's (1998) description, these proliferative events have been demonstrated in the retina of other adult teleosts (Cid et al, 2002;Otteson et al, 2001;Vihtelic and Hyde, 2000). This feature appears to exist in other salmonids (Ahlbert, 1976).…”

Light-induced degeneration and microglial response in the retina of an epibenthonic pigmented teleost: age-dependent photoreceptor susceptibility to cell death

“…We performed immunohistochemical detection of PCNA, an antigen expressed in the nuclei of cells during DNA replication, that has previously been used to identify proliferating precursor cells in the teleost fish retina (Mack and Fernald, 1997;Velasco et al, 2001;Cid et al, 2002;Candal et al, 2005;Bernardos et al, 2007;BejaranoEscobar et al, 2009;Bejarano-Escobar et al, 2010), and to investigate whether cell proliferation is affected by the incidence of constant high intensity light in experimental animals. Many PCNA-positive nuclei were found in the ciliary marginal zone (CMZ) in both control and experimental tench (Fig.8A,C,E).…”