Postembryonic Nephrogenesis and Persistence of Six2-Expressing Nephron Progenitor Cells in the Reptilian Kidney

New nephron formation (nephrogenesis) ceases in mammals around birth and is completely absent in adults. In contrast, postembryonic nephrogenesis is well documented in the mesonephric kidneys of fishes and amphibians. The transient mesonephros in reptiles (including birds) and mammals is replaced by...

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Veröffentlicht in:PloS one 2016-05, Vol.11 (5), p.e0153422-e0153422
Hauptverfasser: Camarata, Troy, Howard, Alexis, Elsey, Ruth M, Raza, Sarah, O'Connor, Alice, Beatty, Brian, Conrad, Jack, Solounias, Nikos, Chow, Priscilla, Mukta, Saima, Vasilyev, Aleksandr
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container_volume 11
creator Camarata, Troy
Howard, Alexis
Elsey, Ruth M
Raza, Sarah
O'Connor, Alice
Beatty, Brian
Conrad, Jack
Solounias, Nikos
Chow, Priscilla
Mukta, Saima
Vasilyev, Aleksandr
description New nephron formation (nephrogenesis) ceases in mammals around birth and is completely absent in adults. In contrast, postembryonic nephrogenesis is well documented in the mesonephric kidneys of fishes and amphibians. The transient mesonephros in reptiles (including birds) and mammals is replaced by the metanephros during embryogenesis. Thus, one may speculate that postembryonic nephrogenesis is restricted to the mesonephric kidney. Previous reports have suggested the metanephros of non-avian reptiles (hereafter reptiles) may continually form nephrons throughout life. We investigated the presence of adult nephrogenesis in reptiles by examining adult kidneys from several species including Trachemys scripta, Chrysemys picta, Boa constrictor, Tupinambis tegu, Anolis carolinensis, and Alligator mississipiensis among others. We found that all major reptilian groups (Testudines, Crocodylia, and Squamates) showed the presence of adult nephrogenesis. The total amount of nephrogenesis varied greatly between species with turtles displaying the highest density of nephrogenesis. In contrast, we were unable to detect adult nephrogenesis in monotremes, and in the iguanid A. carolinensis. Nephron progenitor cells express the transcription factor Six2, which in mammals, becomes downregulated as the progenitor cell population is exhausted and nephrogenesis ends. Using the alligator as a model, we were able to detect Six2-positive cap mesenchyme cells in the adult kidney, which spatially correlated with areas of nephrogenesis. These results suggest that the metanephric kidney of reptiles has maintained the ability to continually grow new nephrons during postembryonic life, a process lost early in mammalian evolution, likely due to the persistence of a Six2-expressing progenitor cell population.
doi_str_mv 10.1371/journal.pone.0153422
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subjects Adults
Alligator mississippiensis
Amphibia
Amphibians
Animals
Anolis carolinensis
Aquatic reptiles
Biology and Life Sciences
Birds
Boa constrictor
Cells (biology)
Chrysemys picta
Crocodylia
Embryogenesis
Embryonic growth stage
Gene expression
Homeostasis
Kidneys
Mammals
Medicine
Medicine and Health Sciences
Mesenchyme
Morphogenesis
Morphology
Nephrons
Nephrons - growth & development
Osteopathic medicine
Progenitor cells
Reptiles
SIX gene family
Squamata
Stem cells
Stem Cells - cytology
Testudines
Trachemys scripta
Trans-Activators - metabolism
Tupinambis teguixim
Turtles
title Postembryonic Nephrogenesis and Persistence of Six2-Expressing Nephron Progenitor Cells in the Reptilian Kidney
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