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Hydrogen Peroxide Regulates Metaplasticity in the Hippocampus

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Synaptic Plasticity and Transsynaptic Signaling

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References

  • Avshalumov MV, Chen BT, Rice ME. (2000) Mechanisms underlying H(2)O(2)-mediated inhibition of synaptic transmission in rat hippocampal slices. Brain Res. 882:86–94.

    Article  PubMed  CAS  Google Scholar 

  • Avshalumov MV, Rice ME. (2002) NMDA receptor activation mediates hydrogen peroxide induced pathophysiology in rat hippocampal slices. J Neurophysiol. 87:2896–903.

    PubMed  CAS  Google Scholar 

  • Auerbach JM, Segal M. (1997) Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci. 17:8695–701.

    PubMed  CAS  Google Scholar 

  • Beckman KB, Ames BN. (1998) The free radical theory of aging matures. Physiol Rev. 78:547–81.

    PubMed  CAS  Google Scholar 

  • Beckman JS, Estevez AG, Grow JP, Barbeito L. (2001) Superoxide dismutase and the death of motoneurons in ALS. Trends Neursci. 24:S15–20.

    Article  CAS  Google Scholar 

  • Benzi G, Moretti A. (1995) Are reactive oxygen species involved in Alzheimer’s disease? Neurobiol Aging. 16:661–74.

    Article  PubMed  CAS  Google Scholar 

  • Bliss TV, Collingridge GL. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:31–9.

    Article  PubMed  CAS  Google Scholar 

  • Bhat NR, Zhang P. (1999) Hydrogen peroxide activation of multiple mitogen-activated protein kinases in an oligodendrocyte cell line: role of extracellular signal-regulated kinase in hydrogen peroxide-induced cell death. J Neurochem. 72:112–9.

    Article  PubMed  CAS  Google Scholar 

  • Bito H, Deisseroth K, Tsien RW. (1996) CREB phosphorylation and dephosphorylation: a Ca2+-and stimulus duration-dependent switch for hippocampal gene expression. Cell. 87:1203–14.

    Article  PubMed  CAS  Google Scholar 

  • Bogumil R, Namgaladze D, Schaarschmidt D, Schmachtel T, Hellstern S, Mutzel R, Ullrich V. (2000) Inactivation of calcineurin by hydrogen peroxide and phenylarsine oxide. Evidence for a dithiol-disulfide equilibrium and implications for redox regulation. Eur J Biochem. 267:1407–15.

    Article  PubMed  CAS  Google Scholar 

  • Borroni AM, Fichtenholtz H, Woodside BL, Teyler TJ. (2000) Role of voltage-dependent calcium channel long-term potentiation (LTP) and NMDA LTP in spatial memory. J Neurosci. 20:9272–6.

    PubMed  CAS  Google Scholar 

  • Burlacu A, Jinga V, Gafencu AV, Simionescu M. (2001) Severity of oxidative stress generates different mechanisms of endothelial cell death. Cell Tissue Res. 306:409–16.

    Article  PubMed  CAS  Google Scholar 

  • Campbell LW, Hao SY, Thibault O, Blalock EM, Landfield PW. (1996) Aging changes in voltage-gated calcium currents in hippocampal CAI neurons. J Neurosci. 16:6286–95.

    PubMed  CAS  Google Scholar 

  • Crossthwaite AJ, Hasan S, Williams RJ. (2002) Hydrogen peroxide-mediated phosphorylation of ERK 1/2, Akt/PKB and JNK in cortical neurones: dependence on Ca(2+) and P13-kinase. J Neurochem. 80:24–35.

    Article  PubMed  CAS  Google Scholar 

  • Datta K, Babbar P, Srivastava T, Sinha S, Chattopadhyay P. (2002) p53 dependent apoptosis in glioma cell lines in response to hydrogen peroxide induced oxidative stress. Int J Biochem Cell Biol. 34:148–57.

    Article  PubMed  CAS  Google Scholar 

  • Davare MA, Dong F, Rubin CS, Hell JW. (1999) The A-kinase anchor protein MAP2B and cAMP-dependent protein kinase are associated with class C L-type calcium channels in neurons. J Biol Chem. 274:30280–7.

    Article  PubMed  CAS  Google Scholar 

  • Dudek SM, Bear MF. (1992) Homosynaptic long-term depression in area CAI of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A. 89:4363–7.

    Article  PubMed  CAS  Google Scholar 

  • Epstein CJ, Avraham KB, Lovett M, Smith S, Elroy-Stein O, Rotman G, Bry C, Groner Y. (1987) Transgenic mice with increased Cu/Zn-superoxide dismutase activity: animal model of dosage effects in Down syndrome. Proc Natl Acad Sci U S A. 84:8044–8.

    Article  PubMed  CAS  Google Scholar 

  • Ermak G, Morgan TE, Davies KJ. (2001) Chronic overexpression of the calcineurin inhibitory gene DSCR1 (Adapt78) is associated with Alzheimer’s disease. J Biol Chem. 276:38787–94.

    Article  PubMed  CAS  Google Scholar 

  • Foster TC, Sharrow KM, Masse JR, Norris CM, Kumar A. (2001) Calcineurin links Ca2+ dysregulation with brain aging. J Neurosci. 21:4066–73.

    PubMed  CAS  Google Scholar 

  • Gahtan E, Auerbach JM, Groner Y, Segal M. (1998) Reversible impairment of long-term potentiation in transgenic Cu/Zn-SOD mice. Eur J Neurosci. 10:538–44.

    Article  PubMed  CAS  Google Scholar 

  • Gen W, Tani M, Takeshita J, Ebihara Y, Tamaki K. (2001) Mechanisms of Ca2+ overload induced by extracellular H2O2 in quiescent isolated rat cardiomyocytes. Basic Res Cardiol. 96:623–9.

    Article  PubMed  CAS  Google Scholar 

  • Halliwell B. (1992) Reactive oxygen species and the central nervous system. J Neurochem. 59,1609–23.

    PubMed  CAS  Google Scholar 

  • Hell JW, Yokoyama CT, Breeze LJ, Chavkin C, Catterall WA. (1995) Phosphorylation of presynaptic and postsynaptic calcium channels by cAMP-dependent protein kinase in hippocampal neurons. EMBO J. 14:3036–44.

    PubMed  CAS  Google Scholar 

  • Herson PS, Lee K, Pinnock RD, Hughes J, Ashford ML. (1999) Hydrogen peroxide induces intracellular calcium overload by activation of a non-selective cation channel in an insulin-secreting cell line. J Biol Chem. 274:833–41.

    Article  PubMed  CAS  Google Scholar 

  • Huang C, Ding M, Li J, Leonard SS, Rojanasakul Y, Castranova V, Vallyathan V, Ju G, Shi X. (2001) Vanadium-induced nuclear factor of activated T cells activation through hydrogen peroxide. J Biol Chem. 276:22397–403.

    Article  PubMed  CAS  Google Scholar 

  • Hyslop PA, Zhang Z, Pearson DV, Phebus LA. (1995) Measurement of striatal H2O2 by microdialysis following global forebrain ischemia and reperfusion in the rat: correlation with the cytotoxic potential of H2O2 in vitro. Brain Res. 671:181–6.

    Article  PubMed  CAS  Google Scholar 

  • Jang JH, Surh YJ. (2001) Protective effects of resveratrol on hydrogen peroxide-induced apoptosis in rat pheochromocytoma (PC12) cells. Mutat Res. 496:181–90.

    PubMed  CAS  Google Scholar 

  • Kamsler A, Segal M. (2003a) Hydrogen peroxide modulation of synaptic plasticity. J Neurosci. 23:269–76.

    PubMed  CAS  Google Scholar 

  • Kamsler A, Segal M. (2003b) Paradoxical actions of hydrogen peroxide on LTP in transgenic SOD-1 mice. J. Neurosci. 23:10359–10367.

    PubMed  CAS  Google Scholar 

  • Kamsler A., Segal, M. (2004) Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol Neurobiol 29:167–78.

    Article  PubMed  CAS  Google Scholar 

  • Kanno S, Ishikawa M, Takayanagi M, Takayanagi Y, Sasaki K. (1999) Exposure to hydrogen peroxide induces cell death via apoptosis in primary cultured mouse hepatocytes. Biol Pharm Bull. 22:1296–300.

    PubMed  CAS  Google Scholar 

  • Kinouchi H, Epstein CJ, Mizui T, Carlson E, Chen SF, Chan PH. (1991) Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc Natl Acad Sci U S A. 88:11158–62.

    Article  PubMed  CAS  Google Scholar 

  • Klann E. (1998) Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CAI. J Neurophysiol. 80:452–7.

    PubMed  CAS  Google Scholar 

  • Klann E, Roberson ED, Knapp LT, Sweatt JD. (1998) A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem. 273:4516–22.

    Article  PubMed  CAS  Google Scholar 

  • Klann E, Thiels E (1999) Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocampal synaptic plasticity. Prog Neuropsychopharmacol Biol Psychiat. 23:359–76.

    Article  CAS  Google Scholar 

  • Knapp LT, Klann E. (2002) Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. J Neurosci. 22:674–83.

    PubMed  CAS  Google Scholar 

  • Lafon-Cazal M, Pietri S, Culcasi M, Bockaert J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature. 364:535–7.

    Article  PubMed  CAS  Google Scholar 

  • Lee ZW, Kweon SM, Kim BC, Leem SH, Shin I, Kim JH, Ha KS. (1998) Phosphatidic acid-induced elevation of intracellular Ca2+ is mediated by RhoA and H2O2 in Rat-2 fibroblasts. J Biol Chem. 273:12710–5.

    Article  PubMed  CAS  Google Scholar 

  • Lei B, Adachi N, Arai T. (1998) Measurement of the extracellular H2O2 in the brain by microdialysis. Brain Res Brain Res Protoc. 3:33–6.

    Article  PubMed  CAS  Google Scholar 

  • Levkovitz Y, Avignone E, Groner Y, Segal M. (1999) Upregulation of GABA neurotransmission suppresses hippocampal excitability and prevents long-term potentiation in transgenic superoxide dismutase-overexpressing mice. Neurosci. 19:10977–84.

    CAS  Google Scholar 

  • Li J, Huang B, Shi X, Castranova V, Vallyathan V, Huang C. (2002) Involvement of hydrogen peroxide in asbestos-induced NFAT activation. Mol Cell Biochem. 234–235:161–8.

    Article  PubMed  Google Scholar 

  • Liu J, Head E, Gharib AM, Yuan W, Ingersoll RT, Hagen TM, Cotman CW, Ames BN. (2002) Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-L carnitine and/or R-alpha-lipoic acid. Proc Natl Acad Sci U S A. 99:2356–61.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Torres M, Gredilla R, Sanz A, Barja G. (2002) Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med. 32:882–9.

    Article  PubMed  CAS  Google Scholar 

  • Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM. (2001) Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell. 104:675–86.

    PubMed  CAS  Google Scholar 

  • Manns JR, Hopkins RO, Squire LR. (2003) Semantic memory and the human hippocampus. Neuron. 38:127–33.

    Article  PubMed  CAS  Google Scholar 

  • McGahon BM, Martin DS, Horrobin DF, Lynch MA. (1999) Age-related changes in synaptic function: analysis of the effect of dietary supplementation with omega-3 fatty acids. Neuroscience. 94:305–14.

    Article  PubMed  CAS  Google Scholar 

  • Mermelstein PG, Bito H, Deisseroth K, Tsien RW. (2000) Critical dependence of cAMP response elementbinding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials. J Neurosci. 20:266–73.

    PubMed  CAS  Google Scholar 

  • Morgan SL, Teyler TJ. (1999) VDCCs and NMDARs underlie two forms of LTP in CAI hippocampus in vivo. J Neurophysiol. 82:736–40.

    PubMed  CAS  Google Scholar 

  • Nakazaki M, Kakei M, Yaekura K, Koriyama N, Morimitsu S, Ichinari K, Yada T, Tei C. (2000) Diverse effects of hydrogen peroxide on cytosolic Ca2+ homeostasis in rat pancreatic beta-cells. Cell Struct Funct. 25:187–93.

    Article  PubMed  CAS  Google Scholar 

  • Nam SH, Jung SY, Yoo CM, Ahn EH, Suh CK. (2002) H2O2 enhances Ca2+ release from osteoblast internal stores. Yonsei Med J. 43:229–35.

    PubMed  CAS  Google Scholar 

  • Norris CM, Halpain S, Foster TC. (1998a) Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol. 80:1567–70.

    PubMed  CAS  Google Scholar 

  • Norris CM, Halpain S, Foster TC. (1998b) Reversal of age-related alterations in synaptic plasticity by blockade of L-type Ca2+ channels. J Neurosci. 18:3171–9.

    PubMed  CAS  Google Scholar 

  • Norris CM, Blalock EM, Chen KC, Porter NM, Landfield PW. (2002) Calcineurin enhances L-type Ca2+ channel activity in hippocampal neurons: increased effect with age in culture. Neuroscience. 110:213–25.

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell E, Vereker E, Lynch MA. (2000) Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. Eur J Neurosci. 12:345–52.

    Article  PubMed  CAS  Google Scholar 

  • Onuma H, Lu YF, Tomizawa K, Moriwaki A, Tokuda M, Hatase O, Matsui H. (1998) A calcineurin inhibitor, FK506 blocks voltage-gated calcium channel-dependent LTP in the hippocampus. Neurosci Res 30:313–9.

    Article  PubMed  CAS  Google Scholar 

  • Peled-Kamar M, Lotem J, Okon E, Sachs L, Groner Y. (1995) Thymic abnormalities and enhanced apoptosis of thymocytes and bone marrow cells in transgenic mice overexpressing Cu/Zn-superoxide dismutase: implications for Down syndrome. EMBO J. 14:4985–93.

    PubMed  CAS  Google Scholar 

  • Pellmar TC, Hollinden GE, Sarvey JM. (1991) Free radicals accelerate the decay of long-term potentiation in field CAI of guinea-pig hippocampus. Neuroscience. 44:353–9.

    Article  PubMed  CAS  Google Scholar 

  • Roveri A, Coassin M, Maiorino M, Zamburlini A, van Amsterdam FT, Ratti E, Ursini F. (1992) Effect of hydrogen peroxide on calcium homeostasis in smooth muscle cells. Arch Biochem Biophys. 297:265–70.

    Article  PubMed  CAS  Google Scholar 

  • Saito A, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH. (2003) Overexpression of copper/zinc superoxide dismutase in transgenic mice protects against neuronal cell death after transient focal ischemia by blocking activation of the Bad cell death signaling pathway. J Neurosci. 23:1710–8.

    PubMed  CAS  Google Scholar 

  • Soderling TR, Derkach VA. (2000) Postsynaptic protein phosphorylation and LTP. Trends Neurosci. 23:75–80.

    Article  PubMed  CAS  Google Scholar 

  • Stanton PK, Sarvey JM. (1984) Blockade of long-term potentiation in rat hippocampal CAI region by inhibitors of protein synthesis. J Neurosci. 4:3080–8.

    PubMed  CAS  Google Scholar 

  • Sugawara T, Noshita N, Lewen A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, Chan PH. (2002) Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci. 22:209–17

    PubMed  CAS  Google Scholar 

  • Thibault O, Hadley R, Landfield PW. (2001) Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J Neurosci. 21:9744–56.

    PubMed  CAS  Google Scholar 

  • Thiels E, Urban NN, Gonzalez-Burgos GR, Kanterewicz BI, Barrionuevo G, Chu CT, Oury TD, Klann E. (2000) Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J Neurosci. 20:7631–9.

    PubMed  CAS  Google Scholar 

  • Vereker E, O’Donnell E, Lynch A, Kelly A, Nolan Y, Lynch MA. (2001) Evidence that interleukin-lbeta and reactive oxygen species production play a pivotal role in stress-induced impairment of LTP in the rat dentate gyrus. Eur J Neurosci. 14:1809–19.

    Article  PubMed  CAS  Google Scholar 

  • Volk T, Hensel M, Kox WJ. (1997) Transient Ca2+ changes in endothelial cells induced by low doses of reactive oxygen species: role of hydrogen peroxide. Mol Cell Biochem. 171:11–21.

    Article  PubMed  CAS  Google Scholar 

  • Wang JH: Kelly PT. (1997) Postsynaptic calcineurin activity downregulates synaptic transmission by weakening intracellular Ca2+ signaling mechanisms in hippocampal CAI neurons. J Neurosci. 17:4600–11

    PubMed  CAS  Google Scholar 

  • Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER. (1998) Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell. 92:25–37.

    Article  PubMed  CAS  Google Scholar 

  • Yang ZW, Zheng T, Wang J, Zhang A, Altura BT, Altura BM. (1999) Hydrogen peroxide induces contraction and raises [Ca2+]i in canine cerebral arterial smooth muscle: participation of cellular signaling pathways. Naunyn Schmiedebergs Arch Pharmacol. 360:646–53.

    Article  PubMed  CAS  Google Scholar 

  • Yarom R, Sapoznikov D, Havivi Y, Avraham KB, Schickler M, Groner Y. (1988) Premature aging changes in neuromuscular junctions of transgenic mice with an extra human CuZnSOD gene: a model for tongue pathology in Down’s syndrome. J Neurol Sci. 88:41–53.

    Article  PubMed  CAS  Google Scholar 

  • Yermolaieva O, Brot N, Weissbach H, Heinemann SH, Hoshi T. (2000) Reactive oxygen species and nitric oxide mediate plasticity of neuronal calcium signaling. Proc Natl Acad Sci U S A. 97:448–53.

    Article  PubMed  CAS  Google Scholar 

  • Zeng H, Chattarji S, Barbarosie M, Rondi-Reig L, Philpot BD, Miyakawa T, Bear MF, Tonegawa S. (2001) Forebrain-specific calcineurin knockout selectively impairs bi-directional synaptic plasticity and working/episodic-like memory. Cell. 107:617–29.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel, 76100

    A. Kamsler & M. Segal

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  1. A. Kamsler
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  2. M. Segal
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Editors and Affiliations

  1. Department of Neurology, New York Medical College, Valhalla, NY, 10595, USA

    Patrick K. Stanton

  2. Department of Physiology, University of Bergen, Bergen, 5009, Norway

    Clive Bramham

  3. CNRRR Department, Helen Hayes Hospital, West Haverstraw, NY, 10993, USA

    Helen E. Scharfman

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Kamsler, A., Segal, M. (2005). Hydrogen Peroxide Regulates Metaplasticity in the Hippocampus. In: Stanton, P.K., Bramham, C., Scharfman, H.E. (eds) Synaptic Plasticity and Transsynaptic Signaling. Springer, Boston, MA. https://doi.org/10.1007/0-387-25443-9_4

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