1,375
Views
15
CrossRef citations to date
0
Altmetric
Research Paper

Chronic glutamate treatment selectively modulates AMPA RNA editing and ADAR expression and activity in primary cortical neurons

, , , , , & show all
Pages 43-53 | Received 23 Jun 2014, Accepted 01 Dec 2014, Published online: 31 Mar 2015

References

  • Bass BL. RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 2002; 71:817-46; PMID:12045112; http://dx.doi.org/10.1146/annurev.biochem.71.110601.135501
  • Orlandi C, Barbon A, Barlati S. Activity regulation of adenosine deaminases acting on RNA (ADARs). Mol Neurobiol 2012; 45:61-75; PMID:22113393; http://dx.doi.org/10.1007/s12035-011-8220-2
  • Nishikura K. Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 2010; 79:321-49; PMID:20192758; http://dx.doi.org/10.1146/annurev-biochem-060208-105251
  • Tariq A, Jantsch MF. Transcript diversification in the nervous system: a to I RNA editing in CNS function and disease development. Front Neurosci 2012; 6:99; PMID:22787438; http://dx.doi.org/10.3389/fnins.2012.00099
  • Paul MS, Bass BL. Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA. EMBO J 1998; 17:1120-7; PMID:9463389; http://dx.doi.org/10.1093/emboj/17.4.1120
  • Chen CX, Cho DS, Wang Q, Lai F, Carter KC, Nishikura K. A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains. RNA 2000; 6:755-67; PMID:10836796; http://dx.doi.org/10.1017/S1355838200000170
  • Kawahara Y, Ito K, Sun H, Kanazawa I, Kwak S. Low editing efficiency of GluR2 mRNA is associated with a low relative abundance of ADAR2 mRNA in white matter of normal human brain. Eur J Neurosci 2003; 18:23-33; PMID:12859334; http://dx.doi.org/10.1046/j.1460-9568.2003.02718.x
  • Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, Shemesh R, Fligelman ZY, Shoshan A, Pollock SR, Sztybel D, et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 2004; 22:1001-5; PMID:15258596; http://dx.doi.org/10.1038/nbt996
  • Li JB, Levanon EY, Yoon JK, Aach J, Xie B, Leproust E, Zhang K, Gao Y, Church GM. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 2009; 324:1210-3; PMID:19478186; http://dx.doi.org/10.1126/science.1170995
  • Sansam CL, Wells KS, Emeson RB. Modulation of RNA editing by functional nucleolar sequestration of ADAR2. Proc Natl Acad Sci U S A 2003; 100:14018-23; PMID:14612560; http://dx.doi.org/10.1073/pnas.2336131100
  • Tariq A, Garncarz W, Handl C, Balik A, Pusch O, Jantsch MF. RNA-interacting proteins act as site-specific repressors of ADAR2-mediated RNA editing and fluctuate upon neuronal stimulation. Nucleic Acids Res 2013; 41:2581-93; PMID:23275536; http://dx.doi.org/10.1093/nar/gks1353
  • Garncarz W, Tariq A, Handl C, Pusch O, Jantsch MF. A high-throughput screen to identify enhancers of ADAR-mediated RNA-editing. RNA Biol 2013; 10:192-204; PMID:23353575; http://dx.doi.org/10.4161/rna.23208
  • Marcucci R, Brindle J, Paro S, Casadio A, Hempel S, Morrice N, Bisso A, Keegan LP, Del Sal G, O'Connell MA. Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J 2011; 30:4211-22; PMID:21847096; http://dx.doi.org/10.1038/emboj.2011.303
  • Hartner JC, Schmittwolf C, Kispert A, Muller AM, Higuchi M, Seeburg PH. Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. J Biol Chem 2004; 279:4894-902; PMID:14615479; http://dx.doi.org/10.1074/jbc.M311347200
  • Higuchi M, Maas S, Single FN, Hartner J, Rozov A, Burnashev N, Feldmeyer D, Sprengel R, Seeburg PH. Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 2000; 406:78-81; PMID:10894545; http://dx.doi.org/10.1038/35017558
  • Wang Q, Khillan J, Gadue P, Nishikura K. Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis. Science 2000; 290:1765-8; PMID:11099415; http://dx.doi.org/10.1126/science.290.5497.1765
  • Hoopengardner B, Bhalla T, Staber C, Reenan R. Nervous system targets of RNA editing identified by comparative genomics. Science 2003; 301:832-6; PMID:12907802; http://dx.doi.org/10.1126/science.1086763
  • Rosenthal JJ, Seeburg PH. A-to-I RNA editing: effects on proteins key to neural excitability. Neuron 2012; 74:432-9; PMID:22578495; http://dx.doi.org/10.1016/j.neuron.2012.04.010
  • Maas S, Kawahara Y, Tamburro KM, Nishikura K. A-to-I RNA editing and human disease. RNA Biol 2006; 3:1-9; PMID:17114938; http://dx.doi.org/10.4161/rna.3.1.2495
  • Akbarian S, Smith MA, Jones EG. Editing for an AMPA receptor subunit RNA in prefrontal cortex and striatum in Alzheimer's disease, Huntington's disease and schizophrenia. Brain Res 1995; 699:297-304; PMID:8616634; http://dx.doi.org/10.1016/0006-8993(95)00922-D
  • Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I, Kwak S. Glutamate receptors: RNA editing and death of motor neurons. Nature 2004; 427:801; PMID:14985749; http://dx.doi.org/10.1038/427801a
  • Silberberg G, Lundin D, Navon R, Ohman M. Deregulation of the A-to-I RNA editing mechanism in psychiatric disorders. Hum Mol Genet 2012; 21:311-21; PMID:21984433; http://dx.doi.org/10.1093/hmg/ddr461
  • Singh M. Dysregulated A to I RNA editing and non-coding RNAs in neurodegeneration. Front Genet 2012; 3:326; PMID:23346095; http://dx.doi.org/10.3389/fgene.2012.00214
  • Seeburg PH. A-to-I editing: new and old sites, functions and speculations. Neuron 2002; 35:17-20; PMID:12123604; http://dx.doi.org/10.1016/S0896-6273(02)00760-2
  • Barbon A, Barlati S. Glutamate receptor RNA editing in health and disease. Biochemistry (Mosc) 2011; 76:882-9; PMID:22022961; http://dx.doi.org/10.1134/S0006297911080037
  • Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 2010; 62:405-96; PMID:20716669; http://dx.doi.org/10.1124/pr.109.002451
  • Lomeli H, Mosbacher J, Melcher T, Hoger T, Geiger JR, Kuner T, Monyer H, Higuchi M, Bach A, Seeburg PH. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 1994; 266:1709-13; PMID:7992055; http://dx.doi.org/10.1126/science.7992055
  • Kamboj SK, Swanson GT, Cull-Candy SG. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 1995; 486 (Pt 2):297-303; PMID:7473197; http://dx.doi.org/10.1113/jphysiol.1995.sp020812
  • Hollmann M, Hartley M, Heinemann S. Ca2+ permeability of KA-AMPA–gated glutamate receptor channels depends on subunit composition. Science 1991; 252:851-3; PMID:1709304; http://dx.doi.org/10.1126/science.1709304
  • Burnashev N, Monyer H, Seeburg PH, Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 1992; 8:189-98; PMID:1370372; http://dx.doi.org/10.1016/0896-6273(92)90120-3
  • Greger IH, Khatri L, Kong X, Ziff EB. AMPA receptor tetramerization is mediated by Q/R editing. Neuron 2003; 40:763-74; PMID:14622580; http://dx.doi.org/10.1016/S0896-6273(03)00668-8
  • Greger IH, Khatri L, Ziff EB. RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 2002; 34:759-72; PMID:12062022; http://dx.doi.org/10.1016/S0896-6273(02)00693-1
  • Isaac JT, Ashby MC, McBain CJ. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007; 54:859-71; PMID:17582328; http://dx.doi.org/10.1016/j.neuron.2007.06.001
  • Liu SJ, Zukin RS. Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 2007; 30:126-34; PMID:17275103; http://dx.doi.org/10.1016/j.tins.2007.01.006
  • Brusa R, Zimmermann F, Koh DS, Feldmeyer D, Gass P, Seeburg PH, Sprengel R. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 1995; 270:1677-80; PMID:7502080; http://dx.doi.org/10.1126/science.270.5242.1677
  • Peng PL, Zhong X, Tu W, Soundarapandian MM, Molner P, Zhu D, Lau L, Liu S, Liu F, Lu Y. ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 2006; 49:719-33; PMID:16504947; http://dx.doi.org/10.1016/j.neuron.2006.01.025
  • Aizawa H, Sawada J, Hideyama T, Yamashita T, Katayama T, Hasebe N, Kimura T, Yahara O, Kwak S. TDP-43 pathology in sporadic ALS occurs in motor neurons lacking the RNA editing enzyme ADAR2. Acta Neuropathol 2010; 120:75-84; PMID:20372915; http://dx.doi.org/10.1007/s00401-010-0678-x
  • Hideyama T, Yamashita T, Aizawa H, Tsuji S, Kakita A, Takahashi H, Kwak S. Profound downregulation of the RNA editing enzyme ADAR2 in ALS spinal motor neurons. Neurobiol Dis 2012; 45:1121-8; PMID:22226999; http://dx.doi.org/10.1016/j.nbd.2011.12.033
  • Hideyama T, Yamashita T, Suzuki T, Tsuji S, Higuchi M, Seeburg PH, Takahashi R, Misawa H, Kwak S. Induced loss of ADAR2 engenders slow death of motor neurons from Q/R site-unedited GluR2. J Neurosci 2010; 30:11917-25; PMID:20826656; http://dx.doi.org/10.1523/JNEUROSCI.2021-10.2010
  • Mahajan SS, Thai KH, Chen K, Ziff E. Exposure of neurons to excitotoxic levels of glutamate induces cleavage of the RNA editing enzyme, adenosine deaminase acting on RNA 2, and loss of GLUR2 editing. Neuroscience 2011; 189:305-15; PMID:21620933; http://dx.doi.org/10.1016/j.neuroscience.2011.05.027
  • Krampfl K, Schlesinger F, Zorner A, Kappler M, Dengler R, Bufler J. Control of kinetic properties of GluR2 flop AMPA-type channels: impact of R/G nuclear editing. Eur J Neurosci 2002; 15:51-62; PMID:11860506; http://dx.doi.org/10.1046/j.0953-816x.2001.01841.x
  • Barbon A, Fumagalli F, Caracciolo L, Madaschi L, Lesma E, Mora C, Carelli S, Slotkin TA, Racagni G, Di Giulio AM, et al. Acute spinal cord injury persistently reduces R/G RNA editing of AMPA receptors. J Neurochem 2010; 114:397-407; PMID:20456005; http://dx.doi.org/10.1111/j.1471-4159.2010.06767.x
  • Lau A, Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch 2010; 460:525-42; PMID:20229265; http://dx.doi.org/10.1007/s00424-010-0809-1
  • Choi DW. Glutamate receptors and the induction of excitotoxic neuronal death. Prog Brain Res 1994; 100:47-51; PMID:7938533; http://dx.doi.org/10.1016/S0079-6123(08)60767-0
  • Michaelis EK. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog Neurobiol 1998; 54:369-415; PMID:9522394; http://dx.doi.org/10.1016/S0301-0082(97)00055-5
  • Levanon EY, Hallegger M, Kinar Y, Shemesh R, Djinovic-Carugo K, Rechavi G, Jantsch MF, Eisenberg E. Evolutionarily conserved human targets of adenosine to inosine RNA editing. Nucleic Acids Res 2005; 33:1162-8; PMID:15731336; http://dx.doi.org/10.1093/nar/gki239
  • Nishimoto Y, Yamashita T, Hideyama T, Tsuji S, Suzuki N, Kwak S. Determination of editors at the novel A-to-I editing positions. Neurosci Res 2008; 61:201-6; PMID:18407364; http://dx.doi.org/10.1016/j.neures.2008.02.009
  • Abekhoukh S, Bardoni B. CYFIP family proteins between autism and intellectual disability: links with Fragile X syndrome. Front Cell Neurosci 2014; 8:81; PMID:24733999; http://dx.doi.org/10.3389/fncel.2014.00081
  • Riedmann EM, Schopoff S, Hartner JC, Jantsch MF. Specificity of ADAR-mediated RNA editing in newly identified targets. RNA 2008; 14:1110-8; PMID:18430892; http://dx.doi.org/10.1261/rna.923308
  • Wahlstedt H, Daniel C, Enstero M, Ohman M. Large-scale mRNA sequencing determines global regulation of RNA editing during brain development. Genome Res 2009; 19:978-86; PMID:19420382; http://dx.doi.org/10.1101/gr.089409.108
  • Balik A, Penn AC, Nemoda Z, Greger IH. Activity-regulated RNA editing in select neuronal subfields in hippocampus. Nucleic Acids Res 2013; 41:1124-34; PMID:23172290; http://dx.doi.org/10.1093/nar/gks1045
  • Rueter SM, Dawson TR, Emeson RB. Regulation of alternative splicing by RNA editing. Nature 1999; 399:75-80; PMID:10331393; http://dx.doi.org/10.1038/19992
  • Feng Y, Sansam CL, Singh M, Emeson RB. Altered RNA editing in mice lacking ADAR2 autoregulation. Mol Cell Biol 2006; 26:480-8; http://dx.doi.org/10.1128/MCB.26.2.480-488.2006
  • Orlandi C, La Via L, Bonini D, Mora C, Russo I, Barbon A, Barlati S. AMPA receptor regulation at the mRNA and protein level in rat primary cortical cultures. PLoS One 2011; 6:e25350; PMID:21966506; http://dx.doi.org/10.1371/journal.pone.0025350
  • Lesuisse C, Martin LJ. Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death. J Neurobiol 2002; 51:9-23; PMID:11920724; http://dx.doi.org/10.1002/neu.10037
  • de Lima AD, Merten MD, Voigt T. Neuritic differentiation and synaptogenesis in serum-free neuronal cultures of the rat cerebral cortex. J Comp Neurol 1997; 382:230-46; PMID:9183691; http://dx.doi.org/10.1002/(SICI)1096-9861(19970602)382:2%3c230::AID-CNE7%3e3.0.CO;2-4
  • Rao A, Kim E, Sheng M, Craig AM. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci 1998; 18:1217-29; PMID:9454832
  • Qian Y, Guan T, Tang X, Huang L, Huang M, Li Y, Sun H, Yu R, Zhang F. Astrocytic glutamate transporter-dependent neuroprotection against glutamate toxicity: an in vitro study of maslinic acid. Eur J Pharmacol 2011; 651:59-65; PMID:21118675; http://dx.doi.org/10.1016/j.ejphar.2010.10.095
  • Ha JS, Lee CS, Maeng JS, Kwon KS, Park SS. Chronic glutamate toxicity in mouse cortical neuron culture. Brain Res 2009; 1273:138-43; PMID:19344697; http://dx.doi.org/10.1016/j.brainres.2009.03.050
  • Bordji K, Becerril-Ortega J, Nicole O, Buisson A. Activation of extrasynaptic, but not synaptic, NMDA receptors modifies amyloid precursor protein expression pattern and increases amyloid-ss production. J Neurosci 2010; 30:15927-42; PMID:21106831; http://dx.doi.org/10.1523/JNEUROSCI.3021-10.2010
  • Barbon A, Vallini I, La Via L, Marchina E, Barlati S. Glutamate receptor RNA editing: a molecular analysis of GluR2, GluR5 and GluR6 in human brain tissues and in NT2 cells following in vitro neural differentiation. Brain Res Mol Brain Res 2003; 117:168-78; PMID:14559151; http://dx.doi.org/10.1016/S0169-328X(03)00317-6
  • Barbon A, Orlandi C, La Via L, Caracciolo L, Tardito D, Musazzi L, Mallei A, Gennarelli M, Racagni G, Popoli M, et al. Antidepressant treatments change 5-HT2C receptor mRNA expression in rat prefrontal/frontal cortex and hippocampus. Neuropsychobiology 2011; 63:160-8; PMID:21228608; http://dx.doi.org/10.1159/000321593
  • Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002; 30:e36; PMID:11972351; http://dx.doi.org/10.1093/nar/30.9.e36

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.