Photoreceptor Differentiation during Retinal Development, Growth, and Regeneration in a Metamorphic Vertebrate

Abstract

To test the hypothesis that growth and regeneration of the adult retina involves a mechanistic recapitulation of retinal development, the patterns of photoreceptor differentiation were investigated in the developing retina, as well as growing and regenerating adult retina, of a metamorphic vertebrate, the winter flounder. Only one opsin, of type RH2 (a "green" cone opsin), was expressed in premetamorphic (developing) retina, and a corresponding middle-wavelength visual pigment was observed. In premetamorphic retinas there was no evidence for any other cone opsins or pigments, rods, rod opsin expression, or rod visual pigment. In contrast, a rod opsin (RH1) and three cone opsins (SWS2, RH2, and LWS) were expressed in postmetamorphic (adult) retina, and these opsins were consistent with the observed repertoire of visual pigments. During postmetamorphic retinal growth and regeneration, cones were always produced before rods, but the different cone types were apparently produced simultaneously, suggesting that cone differentiation mechanisms might change after metamorphosis. The results support the hypothesis that photoreceptor differentiation during growth and regeneration of the adult retina involves a recapitulation of mechanisms that control the sequence of photoreceptor production during retinal development.

Intra-retinal variation of opsin gene expression in the guppy (Poecilia reticulata)

“…It is possible that LWS S180r is expressed in more cone cells or in a different region of the retina at a different life history stage, as only adults were surveyed in this study. Opsin gene expression and regional cone abundance vary during ontogeny in a diversity of fish including cichlids , winter flounder (Mader and Cameron, 2004), salmonids and zebrafish (Takechi and Kawamura, 2005;Allison et al, 2010).…”

In ovo thyroxine exposure alters later UVS cone loss in juvenile rainbow trout

“…In goldfish, RH1 appears first, followed by LWS, RH2, SWS2 and SWS1 opsins (Raymond et al, 1995;Stenkamp et al, 1996). Eel and winter flounder (a flatfish), both species considered to undergo true metamorphosis, express only RH2 during the premetamorphic stage, whereas SWS2 expression appeared only after metamorphosis in juveniles (Mader and Cameron, 2004;Cottrill et al, 2009). In juvenile flatfish, RH1 and LWS expression also appeared after metamorphosis (Mader and Cameron, 2004).…”

Neurogenesis in the Fish Retina

“…Postmetamorphic flounder have two additional cone pigments, red-and blue-sensitive pigments selectively expressed in specific cone photoreceptors, and a rhodopsin pigment expressed in rods. In addition, the green-sensitive pigment is expressed in a cone photoreceptor type that is different in morphology from the green-sensitive cones of premetamorphic flounder (Mader and Cameron, 2004). Metamorphosis in Atlantic halibut is accompanied by similar changes, although some red-and blue-sensitive photoreceptors are present in the premetamorphic retina (Helvik et al, 2001).…”

“…This hypothesis is also consistent with a wealth of anatomical studies aimed at comparative description of regenerated versus native retina. For example, all retinal cell types are present in regenerated zebrafish retina (Cameron and Carney, 2000), the full and appropriate complement of opsins and visual pigments is reestablished (Cameron et al, 1997;Mader and Cameron, 2004), though incorrectly patterned , and regenerated ganglion cells display normal dendritic arbors (Cameron et al, 1999).…”