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      Peroxiredoxin1, a novel regulator of pronephros development, influences retinoic acid and Wnt signaling by controlling ROS levels

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          Abstract

          Peroxiredoxin1 (Prdx1) is an antioxidant enzyme belonging to the peroxiredoxin family of proteins. Prdx1 catalyzes the reduction of H 2O 2 and alkyl hydroperoxide and plays an important role in different biological processes. Prdx1 also participates in various age-related diseases and cancers. In this study, we investigated the role of Prdx1 in pronephros development during embryogenesis. Prdx1 knockdown markedly inhibited proximal tubule formation in the pronephros and significantly increased the cellular levels of reactive oxygen species (ROS), which impaired primary cilia formation. Additionally, treatment with ROS (H 2O 2) severely disrupted proximal tubule formation, whereas Prdx1 overexpression reversed the ROS-mediated inhibition in proximal tubule formation. Epistatic analysis revealed that Prdx1 has a crucial role in retinoic acid and Wnt signaling pathways during pronephrogenesis. In conclusion, Prdx1 facilitates proximal tubule formation during pronephrogenesis by regulating ROS levels.

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          Most cited references 37

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          Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates.

          The evolutionarily conserved planar cell polarity (PCP) pathway (or noncanonical Wnt pathway) drives several important cellular processes, including epithelial cell polarization, cell migration and mitotic spindle orientation. In vertebrates, PCP genes have a vital role in polarized convergent extension movements during gastrulation and neurulation. Here we show that mice with mutations in genes involved in Bardet-Biedl syndrome (BBS), a disorder associated with ciliary dysfunction, share phenotypes with PCP mutants including open eyelids, neural tube defects and disrupted cochlear stereociliary bundles. Furthermore, we identify genetic interactions between BBS genes and a PCP gene in both mouse (Ltap, also called Vangl2) and zebrafish (vangl2). In zebrafish, the augmented phenotype results from enhanced defective convergent extension movements. We also show that Vangl2 localizes to the basal body and axoneme of ciliated cells, a pattern reminiscent of that of the BBS proteins. These data suggest that cilia are intrinsically involved in PCP processes.
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            Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells.

            Hydrogen peroxide is widely viewed as the main second messenger in redox signaling, and it has been proposed that deactivation of the antioxidant peroxiredoxin (Prdx) enzymes allows free peroxide to accumulate and directly oxidize target proteins (the floodgate model). We assessed the role of cytosolic Prdxs 1 and 2 in peroxide-induced activation of the apoptosis signaling kinase 1 (ASK1)/p38 signaling pathway, in which oxidation of ASK1 is required for phosphorylation of p38. In response to peroxide, Prdx1 catalyzed oxidation of ASK1 to a disulfide-linked multimer, and this occurred via transient formation of a Prdx1-ASK1 mixed disulfide intermediate. Oxidation of ASK1 and phosphorylation of p38 were inhibited by knockdown of Prdx1, but also by overexpression of Prdx2. This suggests that these two cytosolic Prdxs have distinct roles in the cellular peroxide response and compete for available peroxide substrate. These data imply that Prdx1 can function as a peroxide receptor in response to extracellular H(2)O(2), receiving the peroxide signal and transducing it into a disulfide bond that is subsequently transmitted to the substrate, ASK1, resulting in p38 phosphorylation. Interestingly, in response to peroxide, Prdx1 and Prdx3 transiently formed reducible higher molecular weight complexes, suggesting that multiple proteins are targets for Prdx-mediated oxidation via a disulfide-exchange mechanism. This model of active peroxide signal distribution via disulfide exchange is consistent with Prdx function in yeast and explains how peroxides may trigger specific disulfide bond formation in mammalian cells. Copyright © 2012 Elsevier Inc. All rights reserved.
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              Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer.

              An abundant cDNA enriched in Spemann's organizer, cerberus, was isolated by differential screening. It encodes a secreted protein that is expressed in the anterior endomesoderm. Microinjection of cerberus mRNA into Xenopus embryos induces ectopic heads, and duplicated hearts and livers. The results suggest a role for a molecule expressed in the anterior endoderm in the induction of head structures in the vertebrate embryo.
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                Author and article information

                Contributors
                parktj@unist.ac.kr
                leeh@knu.ac.kr
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                21 August 2017
                21 August 2017
                2017
                : 7
                Affiliations
                [1 ]ISNI 0000 0001 0661 1556, GRID grid.258803.4, KNU-Center for Nonlinear Dynamics, , School of Life Sciences, BK21 Plus KNU Creative BioResearch Group, College of Natural Sciences, Kyungpook National University, ; Daegu, 41566 South Korea
                [2 ]ISNI 0000 0004 0381 814X, GRID grid.42687.3f, School of Life Sciences, , Ulsan National Institute of Science and Technology (UNIST), ; Ulsan, 44919 South Korea
                [3 ]ISNI 0000 0001 0661 1556, GRID grid.258803.4, College of Pharmacy, , Research Institute of Pharmaceutical Sciences, Kyungpook National University, ; Daegu, 41566 South Korea
                [4 ]ISNI 0000 0001 0661 1556, GRID grid.258803.4, Department of Pharmacology, , College of Medicine, Kyungpook National University, ; Daegu, 41944 South Korea
                [5 ]ISNI 0000 0001 0669 3109, GRID grid.412091.f, Department of Immunology, , School of Medicine, Keimyung University, ; Daegu, 42601 South Korea
                [6 ]ISNI 0000 0001 0661 1556, GRID grid.258803.4, Department of Anatomy, , College of Medicine, Kyungpook National University, ; Daegu, 41944 South Korea
                [7 ]ISNI 0000 0001 0742 4007, GRID grid.49100.3c, Department of Life Sciences, , Pohang University of Science and Technology, ; Pohang, Kyungbuk 37673 South Korea
                Article
                9262
                10.1038/s41598-017-09262-6
                5567039
                28827763
                8bbc108b-c377-4e8b-9e0e-aa967797f95e
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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