Spatiotemporal Pattern of Doublecortin Expression in the Retina of the Sea Lamprey

Abstract

Despite the importance of doublecortin (DCX) for the development of the nervous system, its expression in the retina of most vertebrates is still unknown. The key phylogenetic position of lampreys, together with their complex life cycle, with a long blind larval stage and an active predator adult stage, makes them an interesting model to study retinal development. Here, we studied the spatiotemporal pattern of expression of DCX in the retina of the sea lamprey. In order to characterize the DCX expressing structures, the expression of acetylated α-tubulin (a neuronal marker) and cytokeratins (glial marker) was also analyzed. Tract-tracing methods were used to label ganglion cells. DCX immunoreactivity appeared initially in photoreceptors, ganglion cells and in fibers of the prolarval retina. In larvae smaller than 100 mm, DCX expression was observed in photoreceptors, in cells located in the inner nuclear and inner plexiform layers (IPLs) and in fibers coursing in the nuclear and IPLs, and in the optic nerve (ON). In retinas of premetamorphic and metamorphic larvae, DCX immunoreactivity was also observed in radially oriented cells and fibers and in a layer of cells located in the outer part of the inner neuroblastic layer (INbL) of the lateral retina. Photoreceptors and fibers ending in the outer limitans membrane (OLM) showed DCX expression in adults. Some retinal pigment epithelium cells were also DCX immunoreactive. Immunofluorescence for α-tubulin in premetamorphic larvae showed coexpression in most of the DCX immunoreactive structures. No cells/fibers were found showing DCX and cytokeratins colocalization. The perikaryon of mature ganglion cells is DCX negative. The expression of DCX in sea lamprey retinas suggests that it could play roles in the migration of cells that differentiate in the metamorphosis, in the establishment of connections of ganglion cells and in the development of photoreceptors. Our results also suggest that the radial glia and retinal pigment epithelium cells of lampreys are neurogenic. Comparison of our observations with those reported in gnathostomes reveals similarities and interesting differences probably due to the peculiar development of the sea lamprey retina.

Organization of alpha‐transducin immunoreactive system in the brain and retina of larval and young adult Sea Lamprey (Petromyzon marinus), and their relationship with other neural systems

“…Our results suggest that primitive rods adapted to perceive dim light are the first photoreceptors to appear during ontogeny of extant lampreys. Moreover, the retina appears highly modified during the long burrowing blind larval life (De Miguel, Rodicio & Anadón, ; Anadón, Meléndez‐Ferro, Pérez‐Costas, Pombal & Rodicio, ; Villar‐Cheda, Abalo, Anadón & Rodicio, ; Abalo, Villar‐Cerviño, Villar‐Cheda, Anadón & Rodicio, ; Fernández‐López et al, ). The “duplex” retina only develops during metamorphosis, the time of maturation of lamprey eyes for the adult life (Villar‐Cheda et al, ).…”

The stepwise development of the lamprey visual system and its evolutionary implications

“…(A) Overview showing retinal development in the early larva (left), late larva (centre) and adult (right). Drawings are based on eye sections from Fernández‐López et al () for the early larva, Villar‐Cheda et al () for the late larva and Zeiss et al () for the adult. The boxed regions are magnified in B and C. (B) Retinal structure in the late larva.…”

Distinct Features of Doublecortin as a Marker of Neuronal Migration and Its Implications in Cancer Cell Mobility

“…DCX is expressed in the brain of several species and has consequently been studied for its involvement in neurogenesis, cellular movement, wound healing, and neuronal plasticity. It is expressed in the retinas of chick, rat, shark, and most recently the sea lamprey (Wakabayashi et al, 2008 ; Kim and Sun, 2012 ; Sanchez-Farias and Candal, 2015 ; Fernandez-Lopez et al, 2016 ). It is also expressed in short-lived annual fish (teleost Nothobranchius furzeri ) (Tozzini et al, 2012 ), the zebra finch ( Taeniopygia guttata ; Itoh et al, 2006 ), in rat retinal pigment epithelium (RPE) cells in vitro (Engelhardt et al, 2005 ), as well as in immature and adult neurons in the cerebellum of guinea pig, cat, dog, and primates (Couillard-Despres et al, 2005 ; Ocbina et al, 2006 ; De Nevi et al, 2013 ).…”