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      Regulation of neuronal development and function by ROS

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          Abstract

          Reactive oxygen species ( ROS) have long been studied as destructive agents in the context of nervous system ageing, disease and degeneration. Their roles as signalling molecules under normal physiological conditions is less well understood. Recent studies have provided ample evidence of ROS‐regulating neuronal development and function, from the establishment of neuronal polarity to growth cone pathfinding; from the regulation of connectivity and synaptic transmission to the tuning of neuronal networks. Appreciation of the varied processes that are subject to regulation by ROS might help us understand how changes in ROS metabolism and buffering could progressively impact on neuronal networks with age and disease.

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          Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path.

          T Bliss, T. Lomo (1973)
          1. The after-effects of repetitive stimulation of the perforant path fibres to the dentate area of the hippocampal formation have been examined with extracellular micro-electrodes in rabbits anaesthetized with urethane.2. In fifteen out of eighteen rabbits the population response recorded from granule cells in the dentate area to single perforant path volleys was potentiated for periods ranging from 30 min to 10 hr after one or more conditioning trains at 10-20/sec for 10-15 sec, or 100/sec for 3-4 sec.3. The population response was analysed in terms of three parameters: the amplitude of the population excitatory post-synaptic potential (e.p.s.p.), signalling the depolarization of the granule cells, and the amplitude and latency of the population spike, signalling the discharge of the granule cells.4. All three parameters were potentiated in 29% of the experiments; in other experiments in which long term changes occurred, potentiation was confined to one or two of the three parameters. A reduction in the latency of the population spike was the commonest sign of potentiation, occurring in 57% of all experiments. The amplitude of the population e.p.s.p. was increased in 43%, and of the population spike in 40%, of all experiments.5. During conditioning at 10-20/sec there was massive potentiation of the population spike (;frequency potentiation'). The spike was suppressed during stimulation at 100/sec. Both frequencies produced long-term potentiation.6. The results suggest that two independent mechanisms are responsible for long-lasting potentiation: (a) an increase in the efficiency of synaptic transmission at the perforant path synapses; (b) an increase in the excitability of the granule cell population.
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            Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.

            Julia Foreman, Vadim Demidchik, John H F Bothwell … (2003)
            Cell expansion is a central process in plant morphogenesis, and the elongation of roots and root hairs is essential for uptake of minerals and water from the soil. Ca2+ influx from the extracellular store is required for (and sets the rates of) cell elongation in roots. Arabidopsis thaliana rhd2 mutants are defective in Ca2+ uptake and consequently cell expansion is compromised--rhd2 mutants have short root hairs and stunted roots. To determine the regulation of Ca2+ acquisition in growing root cells we show here that RHD2 is an NADPH oxidase, a protein that transfers electrons from NADPH to an electron acceptor leading to the formation of reactive oxygen species (ROS). We show that ROS accumulate in growing wild-type (WT) root hairs but their levels are markedly decreased in rhd2 mutants. Blocking the activity of the NADPH oxidase with diphenylene iodonium (DPI) inhibits ROS formation and phenocopies Rhd2-. Treatment of rhd2 roots with ROS partly suppresses the mutant phenotype and stimulates the activity of plasma membrane hyperpolarization-activated Ca2+ channels, the predominant root Ca2+ acquisition system. This indicates that NADPH oxidases control development by making ROS that regulate plant cell expansion through the activation of Ca2+ channels.
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              Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes.

              Gerd Bienert, Anders L B Møller, Kim A Kristiansen … (2007)
              The metabolism of aerobic organisms continuously produces reactive oxygen species. Although potentially toxic, these compounds also function in signaling. One important feature of signaling compounds is their ability to move between different compartments, e.g. to cross membranes. Here we present evidence that aquaporins can channel hydrogen peroxide (H2O2). Twenty-four aquaporins from plants and mammals were screened in five yeast strains differing in sensitivity toward oxidative stress. Expression of human AQP8 and plant Arabidopsis TIP1;1 and TIP1;2 in yeast decreased growth and survival in the presence of H2O2. Further evidence for aquaporin-mediated H2O2 diffusion was obtained by a fluorescence assay with intact yeast cells using an intracellular reactive oxygen species-sensitive fluorescent dye. Application of silver ions (Ag+), which block aquaporin-mediated water diffusion in a fast kinetics swelling assay, also reversed both the aquaporin-dependent growth repression and the H2O2-induced fluorescence. Our results present the first molecular genetic evidence for the diffusion of H2O2 through specific members of the aquaporin family.
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                Author and article information

                Contributors
                Matthew C. W. Oswald: mo364@cam.ac.uk
                Sean T. Sweeney: sean.sweeney@york.ac.uk
                Matthias Landgraf: ml10006@cam.ac.uk
                Journal
                Journal ID (nlm-ta): FEBS Lett
                Journal ID (iso-abbrev): FEBS Lett
                Journal ID (doi): 10.1002/(ISSN)1873-3468
                Journal ID (publisher-id): FEB2
                Title: Febs Letters
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Print): 0014-5793
                ISSN (Electronic): 1873-3468
                Publication date (Electronic): 26 January 2018
                Publication date (Print): March 2018
                Volume: 592
                Issue: 5 , Unlocking Nervous System Function through ROS and Mitochondrial Signaling ( doiID: 10.1002/feb2.2018.592.issue-5 )
                Pages: 679-691
                Affiliations
                [ 1 ] Department of Zoology University of Cambridge UK
                [ 2 ] Department of Biology University of York Heslington York UK
                Author notes
                [*] [* ] Correspondence

                M. C. W. Oswald, M. Landgraf, Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

                Fax: +44 1223 336 676

                Tel: +44 1223 769 348

                E‐mails: mo364@ 123456cam.ac.uk (MCWO); ml10006@ 123456cam.ac.uk (ML)

                and

                S. T. Sweeney, Department of Biology, University of York, Heslington York YO10 5DD, UK

                Fax: +44 1904 328505

                Tel: +44 1904 328537

                E‐mail: sean.sweeney@ 123456york.ac.uk

                Article
                Publisher ID: FEB212972
                DOI: 10.1002/1873-3468.12972
                PMC ID: 5888200
                PubMed ID: 29323696
                SO-VID: 4d798098-28ac-4500-b543-b3c867b93323
                Copyright © © 2018 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 12 December 2017
                Date accepted : 02 January 2018
                Page count
                Figures: 2, Tables: 0, Pages: 13, Words: 9518
                Funding
                Funded by: BBSRC
                Award ID: BB/I012273/1
                Award ID: BB/IO1179X/1
                Award ID: BB/M002322/1
                Award ID: BB/M002934/1
                Categories
                Subject: Review Article
                Subject: Review Articles
                Subject: Neuroscience
                Custom metadata
                source-schema-version-number 2.0
                component-id feb212972
                cover-date March 2018
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.3.4 mode:remove_FC converted:06.04.2018

                ScienceOpen disciplines: Molecular biology
                Keywords: axon,cytoskeleton,dendrite,nadph oxidase,nervous system,neuronal polarity,pathfinding,plasticity,reactive oxygen species,synapse
                Data availability:
                ScienceOpen disciplines: Molecular biology
                Keywords: axon, cytoskeleton, dendrite, nadph oxidase, nervous system, neuronal polarity, pathfinding, plasticity, reactive oxygen species, synapse

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