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Gordon Fain, Matthew Toomey, Ala Morshedian, Gabriel Pollock, Rikard Frederiksen, Jennifer Enright, Steve McCormick, Carter Cornwall, Joseph Corbo; Cambrian origin of the rhodopsin/porphyropsin switch. Invest. Ophthalmol. Vis. Sci. 2017;58(8):5605.
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Lamprey are jawless vertebrates, which diverged from jawed vertebrates (fishes, amphibians, reptiles, and mammals) during the Cambrian period (~500 Mya). Lamprey are also anadromous, migrating between freshwater and marine environments during their life cycle. In the 1950s, Wald detected vitamin A1-based rhodopsin in juvenile lamprey but red-shifted vitamin A2-based porphyropsin in adults. Here, we sought to ask the question: do lampreys use the same mechanism of A1-to-A2 conversion (expression of the enzyme, CYP27C1) as fresh-water jawed vertebrates?
Single-cell measurements were made from sea lamprey (Petromyzon marinus) photoreceptors with suction-electrode recording. Photoreceptors were also studied by microspectrophotometry. HPLC, PCR, and in situ hybridization were used to characterize retinoid content and CYP27C1 gene expression.
Juvenile lamprey rods and cones resemble those of adults. Rods respond to single photons, have longer integration times, and are 70-80 times more sensitive than cones. Spectral sensitivity and microspectrophotometry show that both juveniles and adults have only one spectral class of rod and one cone with best-fitting λmax’s for juveniles of 504 nm (rods) and 551 nm (cones); and for adults of 522 nm (rods) and 592 nm (cones). HPLC shows that vitamin A2 is present in adult eyes but not in those of juveniles. Quantitative PCR for expression of the vitamin A1 3,4-dehydrogenase CYP27C1 gene indicates that levels are significantly higher in the adult RPE compared to juvenile. In situ hybridization shows that the CYP27C1 transcript localizes to the adult RPE and is not detected in the juvenile eye.
Lamprey rods and cones respond to light in a nearly identical fashion in juvenile and adult forms, with one spectral class of rod and one cone having predominantly A2-based pigments in fresh-water adults and A1-based pigments in marine juveniles. Lamprey convert vitamin A1 to vitamin A2 with the same enzyme used by jawed vertebrates, the 3,4-dehydrogenase CYP27C1. Moreover in both lamprey and jawed vertebrates, this enzyme is localized to the RPE. We conclude that porphyropsin and the mechanism of converting A1 to A2 were present in the retina before jawed and jawless vertebrates diverged, not long after the origin of chordates during the Cambrian radiation.
This is an abstract that was submitted for the 2017 ARVO Annual Meeting, held in Baltimore, MD, May 7-11, 2017.
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