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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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. |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0153422</identifier><identifier>PMID: 27144443</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>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</subject><ispartof>PloS one, 2016-05, Vol.11 (5), p.e0153422-e0153422</ispartof><rights>2016 Camarata et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Camarata et al 2016 Camarata et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-b4aa5ebddf40ca7c907f0166334da1db77d9b995129205be8584387711e335f03</citedby><cites>FETCH-LOGICAL-c526t-b4aa5ebddf40ca7c907f0166334da1db77d9b995129205be8584387711e335f03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4856328/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4856328/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27144443$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Camarata, Troy</creatorcontrib><creatorcontrib>Howard, Alexis</creatorcontrib><creatorcontrib>Elsey, Ruth M</creatorcontrib><creatorcontrib>Raza, Sarah</creatorcontrib><creatorcontrib>O'Connor, Alice</creatorcontrib><creatorcontrib>Beatty, Brian</creatorcontrib><creatorcontrib>Conrad, Jack</creatorcontrib><creatorcontrib>Solounias, Nikos</creatorcontrib><creatorcontrib>Chow, Priscilla</creatorcontrib><creatorcontrib>Mukta, Saima</creatorcontrib><creatorcontrib>Vasilyev, Aleksandr</creatorcontrib><title>Postembryonic Nephrogenesis and Persistence of Six2-Expressing Nephron Progenitor Cells in the Reptilian Kidney</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>New nephron formation (nephrogenesis) ceases in mammals around birth and is completely absent in adults. 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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. 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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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27144443</pmid><doi>10.1371/journal.pone.0153422</doi><oa>free_for_read</oa></addata></record> |
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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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