Mutation in the Sip1 transcription factor leads to a disturbance of the preconditioning of AMPA receptors by episodes of hypoxia in neurons of the cerebral cortex due to changes in their activity and subunit composition. The protective effects of interleukin-10.
Turovskaya, Maria V; Zinchenko, Valery P; Babaev, Alexei Aet al.
2018 • In Archives of Biochemistry and Biophysics, 654, p. 126-135
[en] The Sip1 mutation plays the main role in pathogenesis of the Mowat-Wilson syndrome, which is characterized by the pronounced epileptic symptoms. Cortical neurons of homozygous mice with Sip1 mutation are resistant to AMPA receptor activators. Disturbances of the excitatory signaling components are also observed on such a phenomenon of neuroplasticity as hypoxic preconditioning. In this work, the mechanisms of loss of the AMPA receptor's ability to precondition by episodes of short-term hypoxia were investigated on cortical neurons derived from the Sip1 homozygous mice. The preconditioning effect was estimated by the level of suppression of the AMPA receptors activity with hypoxia episodes. Using fluorescence microscopy, we have shown that cortical neurons from the Sip1(fl/fl) mice are characterized by the absence of hypoxic preconditioning effect, whereas the amplitude of Ca(2+)-responses to the application of the AMPA receptor agonist, 5-Fluorowillardiine, in neurons from the Sip1 mice brainstem is suppressed by brief episodes of hypoxia. The mechanism responsible for this process is hypoxia-induced desensitization of the AMPA receptors, which is absent in the cortex neurons possessing the Sip1 mutation. However, the appearance of preconditioning in these neurons can be induced by phosphoinositide-3-kinase activation with a selective activator or an anti-inflammatory cytokine interleukin-10.
Turovskaya, Maria V; Institute of Cell Biophysics, Russian Academy of Sciences, Russia.
Zinchenko, Valery P; Institute of Cell Biophysics, Russian Academy of Sciences, Russia.
Babaev, Alexei A; Institute of Biology and Biomedicine, Lobachevsky State University of Nizhniy
Epifanova, Ekaterina ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques ; Institute of Biology and Biomedicine, Lobachevsky State University of Nizhniy
Tarabykin, Victor S; Institute of Biology and Biomedicine, Lobachevsky State University of Nizhniy
Turovsky, Egor A; Institute of Cell Biophysics, Russian Academy of Sciences, Russia. Electronic
Language :
English
Title :
Mutation in the Sip1 transcription factor leads to a disturbance of the preconditioning of AMPA receptors by episodes of hypoxia in neurons of the cerebral cortex due to changes in their activity and subunit composition. The protective effects of interleukin-10.
Adam, M.P., Schelley, S., Gallagher, R., Brady, A.N., Barr, K., Blumberg, B., Shieh, J.T., Graham, J., Slavotinek, A., Martin, M., Keppler-Noreuil, K., Storm, A.L., Hudgins, L., Clinical features and management issues in Mowat-Wilson syndrome. Am. J. Med. Genet. 140:24 (2006), 2730–2741.
Beal, M.F., Aging, energy, and oxidative stress in neurodegenerative diseases. Ann. Neurol. 38:3 (1991), 357–366.
Bhuiyan, M.I., Kim, Y.J., Mechanisms and prospects of ischemic tolerance indiced by cerebral preconditioning. Int. Neurourol. J. 14:4 (2010), 203–212.
Bok, J., Wang, Q., Huang, J., Green, S.H., CaMKII and CaMKIV mediate distinct prosurvival signaling pathways in response to depolarization in neurons. Mol. Cell. Neurosci. 36:1 (2007), 13–26.
Buchan, A., Li, H., Cho, S., Pulsinelli, W., Blockade of the AMPA receptor prevents CA1 hippocampal injury following severe but transient forebrain ischemia in adult rats. Neurosci. Lett. 132:2 (1991), 255–258.
Gereau, R.W. 4th, Heinemann, S.F., Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5. Neuron 20:1 (1998), 143–151.
Gorski, J.A., Talley, T., Qiu, M., Puelles, L., Rubenstein, J.L.R., Jones, K.R., Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci. 22 (2002), 6309–6314.
Hanada, T., The AMPA receptor as a therapeutic target in epilepsy: preclinical and clinical evidence. J. Recept. Ligand Channel Res. 7 (2014), 39–50.
Henley, J.M., Wilkinson, K.A., AMPA receptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging. Dialogues Clin. Neuroscience 15:1 (2013), 11–27.
Higashi, Y., Maruhashi, M., Nelles, L., Van de Putte, T., Verschueren, K., Miyoshi, T., Yoshimoto, A., Kondoh, H., Huylebroeck, D., Generation of the floxed allele of the SIP1 (Smad-interacting protein 1) gene for Cre-mediated conditional knockout in the mouse. Genesis 32:2 (2002), 82–84.
Hollmann, M., Hartley, M., Heinemann, S., Ca2+-permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science (Wash. DC) 252:5007 (1991), 851–853.
Johnson, F.O., Yuan, Y., Hajela, R.K., Chitrakar, A., Parsell, D.M., Atchison, W.D., Exposure to an environmental neurotoxicant hastens the onset of amyotrophic lateral sclerosis-like phenotype in human Cu2+/Zn2+ superoxide dismutase 1 G93A mice: glutamate-mediated excitotoxicity. J. Pharmacol. Exp. Therapeut. 338:2 (2011), 518–527.
Jonas, P., AMPA-type glutamate receptors-nonselective cation channels mediating fast excitatory transmission in the CNS. EXS 66 (1993), 61–76.
Kjøller, C., Diemer, N.H., GluR2 protein synthesis and metabolism in rat hippocampus following transient ischemia and ischemic tolerance induction. Neurochem. Int. 37:1 (2000), 7–15.
Kumar, J., Mayer, M.L., Functional insights from glutamate receptor ion channel structures. Annu. Rev. Physiol. 75 (2013), 313–337.
Li, H., Buchan, A., Treatment with an AMPA antagonist 12 hours following severe normothermic forebrain ischemia prevents CA1 neuronal injury. J. Cerebr. Blood Flow Metabol. 13:6 (1993), 933–939.
Li, D.P., Byan, H.S., Pan, H.L., Switch to glutamate receptor 2-lacking AMPA receptors increases neuronal excitability in hypothalamus and sympathetic drive in hypertension. J. Neurosci. 32:1 (2012), 372–380.
McCarran, W.J., Goldberg, M.P., White matter axon vulnerability to AMPA/kainite receptor-mediated ischemic injury is developmentakky regulated. J. Neurosci. 27:15 (2007), 4220–4229.
Miquelajauregui, A., Van de Putte, T., Polyakov, A., Nityanandam, A., Boppana, S., Seuntjens, E., Karabinos, A., Higashi, Y., Huylebroeck, D., Tarabykin, V., Smad-interacting protein-1 (Zfhx1b) acts upstream of Wnt signaling in the mouse hippocampus and controls its formation. Proc. Natl. Acad. Sci. U.S.A. 104:31 (2007), 12919–12924.
Noh, K.M., Yokota, H., Mashiko, T., Castillo, P.E., Zukin, R.S., Bennett, M.V., Blockade of calcium-permeable AMPA receptors protects hippocampal neurons against global ischemia-induced death. Proc. Natl. Acad. Sci. U.S.A. 102:34 (2005), 12230–12235.
Oh, M.C., Kim, J.M., Safaee, M., Kaur, G., Sun, M.Z., Kaur, R., Celli, A., Mauro, T.M., Parsa, A.T., Overexpression of calcium-permeable glutamate receptors in glioblastoma derived brain tumor initiating cells. PLoS One, 7(10), 2012, 47846.
Opitz, T., Grooms, S.Y., Bennett, M.V., Zukin, R.S., Remodeling of α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit composition in hippocampal neurons after global ischemia. Proc. Natl. Acad. Sci. U.S.A. 97:24 (2000), 13360–13365.
Page, K.J., Everitt, B.J., Robbins, T.W., Marston, H.M., Wilkinson, L.S., Dissociable effects on spatial maze and passive avoidance acquisition and retention following AMPA- and ibotenic acid-induced excitotoxic lesions of the basal forebrain in rats: differential dependence on cholinergic neuronal loss. Neuroscience 43:2–3 (1991), 457–472.
Park, Y.H., Mueller, B.H. 2nd2, McGrady, N.R., Ma, H.Y., Yorio, T., AMPA receptor desensitization is the determinant of AMPA receptor mediated excitotoxicity in purified retinal ganglion cells. Exp. Eye Res. 132 (2015), 136–150.
Pellegrini-Giampietro, D.E., Zukin, R.S., Bennett, M.V., Cho, S., Pulsinelli, W.A., Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc. Natl. Acad. Sci. U.S.A. 89:21 (1992), 10499–10503.
Poddar, R., Chen, A., Winter, L., Rajagopal, S., Paul, S., Role of AMPA receptors in homocysteine-NMDA receptor-induced crosstalk between ERK and p38 MAPK. J. Neurochem. 142:4 (2017), 560–573.
Porter, B.E., Cui, X.N., Brooks–Kayal, A.R., Status epilepticus differentially alters AMPA and kainate receptor subunit expression in mature and immature dentate granule neurons. Eur. J. Neurosci. 23:11 (2006), 2857–2863.
Powell, E.M., Interneuron development and epilepsy: early genetic defects cause long-term consequences in seizuresand susceptibility. Epilepsy Current 13:4 (2013), 172–176.
Sattler, R., Tymianski, M., Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol. Neurobiol. 24:1–3 (2001), 107–129.
Savina, T.A., Shchipakina, T.G., Levin, S.G., Godukhin, O.V., Interleukin-10 prevents the hypoxia-induced decreases in expressions of AMPA receptor subunit GluA1 and alpha subunit of Ca(2+)/calmodulin-dependent protein kinase II in hippocampal neurons. Neurosci. Lett. 534 (2013), 279–284.
See, V., Boutillier, A.L., Bito, H., Loeffler, J.P., Calcium/calmodulin-dependent protein kinase type IV (CaMKIV) inhibits apoptosis induced by potassium deprivation in cerebellar granule neurons. Faseb. J. 15:1 (2001), 134–144.
Semenov, D.G., Samoilov, M.O., Lazarewicz, J.W., Preconditioning reduces hypoxia-evoked alterations in glutamatergic Ca2+ signaling in rat cortex. Acta Neurobiol. Exp. 68:2 (2008), 169–179.
Slevin, M., Krupinski, J., Kumar, P., Gaffney, J., Kumar, S.J., Gene activation and protein expression following ischaemic stroke: strategies towards neuroprotection. Cell Mol. Med. 9:1 (2005), 85–102.
Sommer, B., Keinanen, K., Verdoorn, T.A., Wisden, W., Burnashev, N., Herb, A., Kohler, M., Takagi, T., Sakmann, B., Seeburg, P.H., Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science (Wash. DC) 249:4976 (1990), 1580–1585.
Sun, Y., Olson, R., Horning, M., Armstrong, N., Mayer, M., Gouaux, E., Mechanism of glutamate receptor desensitization. Nature 417:6886 (2002), 245–253.
Talos, D.M., Fishman, R.E., Park, H., Folkerth, R.D., Follett, P.L., Volpe, J.J., Jensen, F.E., Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J. Comp. Neurol. 497:1 (2006), 42–60.
Tanaka, H., Calderone, A., Jover, T., Grooms, S., Yokota, H., Zukin, R., Benett, M., Ischemic preconditioning acts upstream of GluR2 down-regulation to afford neuroprotection in the hippocampal CA1. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 2362–2367.
Tsubokawa, H., Oguro, K., Robinson, H., Single glutamate channels in CA1 pyramidal neurons after transient ischemia. Neuroreport 6 (1995), 527–531.
Tukhovskaya, E.A., Turovsky, E.A., Turovskaya, M.V., Levin, S.G., Murashev, A.N., Zinchenko, V.P., Godukhin, O.V., Anti-inflammatory cytokine interleukin-10 increases resistance to brain ischemia through modulation of ischemia-induced intracellular Ca2+ response. Neurosci. Lett. 571 (2014), 55–60.
Turovsky, E.A., Turovskaya, M.V., Gaidin, S.G., Zinchenko, V.P., Cytokine IL-10, activators of PI3-kinase, agonists of α-2 adrenoreceptor and antioxidants prevent ischemia-induced cell death in rat hippocampal cultures. Arch. Biochem. Biophys. 615 (2017), 35–43.
Turovskaya, M.V., Babaev, A.A., Zinchenko, V.P., Epifanova, E.A., Borisova, E.V., Tarabykin, V.S., Turovsky, E.A., Sip-1 mutation causes a disturbance in activity of NMDA- and AMPA-, but not kainate receptors of neurons in cerebral cortex. Neurosci. Lett. 650 (2017), 180–186.
Turovsky, E.A., Babaev, A.A., Tarabykin, V.S., Turovskaya, M.V., Sip1 mutation suppresses the resistance of cerebral cortex neurons to hypoxia through the disturbance of mechanisms of hypoxic preconditioning. Biochemistry (Mosc.), Suppl.: Membr. Cell Biol. 11:4 (2017), 330–337.
Turovskaya, M.V., Turovsky, E.A., Kononov, A.V., Zinchenko, V.P., Short-term hypoxia induces a selective death of GABAergic neurons. Biochemistry (Mosc.), Suppl.: Membrane and Cell Biology 8:1 (2014), 125–135.
Turovsky, E.A., Turovskaya, M.V., Kononov, A.V., Zinchenko, V.P., Short-term episodes of hypoxia induce posthypoxic hyperexcitability and selective death of GABAergic hippocampal neurons. Exp. Neurol. 250 (2013), 1–7.
Turovskaya, M.V., Turovsky, E.A., Zinchenko, V.P., Levin, S.G., Shamsutdinova, A.A., Godukhin, O.V., Repeated brief episodes of hypoxia modulate the calcium responses of ionotropic glutamate receptors in hippocampal neurons. Neurosci. Lett. 496:1 (2011), 11–14.
Underhill, S.M., Goldberg, M.P., Hypoxic injury of isolated axons is independent of ionotropic glutamate receptors. Neurobiol. Dis. 25:2 (2007), 284–290.
Vieira, M., Fernandes, J., Burgeiro, A., Thomas, G.M., Huganir, R.L., Duarte, C.B., Carvalho, A.L., Santos, A.E., Excitotoxicity through Ca2+-permeable AMPA receptors requires Ca2+-dependent JNK activation. Neurobiol. Dis. 40:3 (2010), 645–655.
Winklbauer, R., Medina, A., Swain, R.K., Steinbeisser, H., Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413:6858 (2001), 856–860.
Xu, T.L., Li, J.S., Jin, Y.H., Akaike, N., Modulation of the glycine response by Ca2+-permeable AMPA receptors in rat spinal neurones. J. Physiol. 514:Pt.3 (1999), 701–711.
Levin, S.G., Sirota, N.P., Nenov, M.N., Savina, T.A., Godukhin, O.V., Interleukin-10 and PD150606 modulate expression of AMPA receptor GluA1 and GluA2 subunits under hypoxic conditions. Neuroreport 29:2 (2018 Jan 17), 84–91, 10.1097/WNR.0000000000000928.
