Abstract
Besides being a marker of various somatic stem cells in mammals, prominin-1 (CD133) plays a role in maintaining the photoreceptor integrity since mutations in the PROM1 gene are linked with retinal degeneration. In spite of that, little information is available regarding its distribution in eyes of non-mammalian vertebrates endowed with high regenerative abilities. To address this subject, prominin-1 cognates were isolated from axolotl, zebrafish and chicken, and their retinal compartmentalization was investigated and compared to that of their mammalian orthologue. Interestingly, prominin-1 transcripts—except for the axolotl—were not strictly restricted to the outer nuclear layer (i.e., photoreceptor cells), but they also marked distinct subdivisions of the inner nuclear layer (INL). In zebrafish, where the prominin-1 gene is duplicated (i.e., prominin-1a and prominin-1b), a differential expression was noted for both paralogues within the INL being localized either to its vitreal or scleral subdivision, respectively. Interestingly, expression of prominin-1a within the former domain coincided with Pax-6–positive cells that are known to act as progenitors upon injury-induced retino-neurogenesis. A similar, but minute population of prominin-1–positive cells located at the vitreal side of the INL was also detected in developing and adult mice. In chicken, however, prominin-1–positive cells appeared to be aligned along the scleral side of the INL reminiscent of zebrafish prominin-1b. Taken together our data indicate that in addition to conserved expression of prominin-1 in photoreceptors, significant prominin-1–expressing non-photoreceptor retinal cell populations are present in the vertebrate eye that might represent potential sources of stem/progenitor cells for regenerative therapies.
Highlights
Vision is one of the most important sensory modality channelling information into the brain through a specialized set of photoreceptors coupled to a chain of second and third order neuronal cells
PROM1 (PROML1; prominin-1) encodes for the prototype of a family of cholesterolbinding pentaspan membrane glycoproteins conserved throughout the animal kingdom [3,4,5,6]
In order to get more insights into the spatiotemporal expression pattern of prominin-1 within the retina of three distinct classes of non-mammalian vertebrate model organisms, we identified cognates of this gene from axolotl, zebrafish and chick and localized their expression using a nonradioactive in situ hybridization (ISH) technique, and compared them to the murine eye model
Summary
Vision is one of the most important sensory modality channelling information into the brain through a specialized set of photoreceptors coupled to a chain of second and third order neuronal cells. Numerous diseases might lead to degenerative alteration of this neuronal circuitry, the most common cause of blindness is the primary degeneration of photoreceptor cells. These pathologies are often of inheritable nature, e.g. retinitis pigmentosa [1] and achromatopsia [2]. Previous studies have revealed that prominin-1 (CD133) is highly enriched in precursor structures of mammalian rod photoreceptive disks, i.e. plasma membrane evaginations growing out at the base of the outer segment from the connecting cilium [7]. The importance of prominin-1 for the photoreceptor cell architecture and integrity ( that of rods) has been established from four distinct lines of observation. Prominin-1 appears to be a key player in maintenance of the integrity of photoreceptors from insects to mammals in spite of the significantly distinct organizing principles of their visual organs [16]
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