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Article

Calpain 2 Activated through N-Methyl-d-Aspartic Acid Receptor Signaling Cleaves CPEB3 and Abrogates CPEB3-Repressed Translation in Neurons

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Pages 3321-3332 | Received 04 Mar 2012, Accepted 08 Jun 2012, Published online: 20 Mar 2023

REFERENCES

  • Abe K, Takeichi M. 2007. NMDA-receptor activation induces calpain-mediated beta-catenin cleavages for triggering gene expression. Neuron 53:387–397.
  • Adamec E, Beermann ML, Nixon RA. 1998. Calpain I activation in rat hippocampal neurons in culture is NMDA receptor selective and not essential for excitotoxic cell death. Brain Res. Mol. Brain Res. 54:35–48.
  • Arthur JS, Elce JS, Hegadorn C, Williams K, Greer PA. 2000. Disruption of the murine calpain small subunit gene, Capn4: calpain is essential for embryonic development but not for cell growth and division. Mol. Cell. Biol. 20:4474–4481.
  • Ashby MC, et al. 2004. Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J. Neurosci. 24:5172–5176.
  • Banker G, Goslin K. 1988. Developments in neuronal cell culture. Nature 336:185–186.
  • Beattie EC, et al. 2000. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3:1291–1300.
  • Bevers MB, et al. 2010. RNAi targeting micro-calpain increases neuron survival and preserves hippocampal function after global brain ischemia. Exp. Neurol. 224:170–177.
  • Bevers MB, et al. 2009. Knockdown of m-calpain increases survival of primary hippocampal neurons following NMDA excitotoxicity. J. Neurochem. 108:1237–1250.
  • Bi X, et al. 1997. Characterization of calpain-mediated proteolysis of GluR1 subunits of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors in rat brain. J. Neurochem. 68:1484–1494.
  • Bramham CR, Wells DG. 2007. Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8:776–789.
  • Carillo S, et al. 1994. Differential sensitivity of FOS and JUN family members to calpains. Oncogene 9:1679–1689.
  • Chen PJ, Huang YS. 2011. CPEB2-eEF2 interaction impedes HIF-1alpha RNA translation. EMBO J. 31:959–971.
  • Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N. 2009. Translational control of long-lasting synaptic plasticity and memory. Neuron 61:10–26.
  • Croall DE, Ersfeld K. 2007. The calpains: modular designs and functional diversity. Genome Biol. 8:218. https://doi.org/10.1186/gb-2007-8-6-218.
  • Crocker SJ, et al. 2003. Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J. Neurosci. 23:4081–4091.
  • del Cerro S, et al. 1994. Stimulation of NMDA receptors activates calpain in cultured hippocampal slices. Neurosci. Lett. 167:149–152.
  • Denny JB, Polan-Curtain J, Ghuman A, Wayner MJ, Armstrong DL. 1990. Calpain inhibitors block long-term potentiation. Brain Res. 534:317–320.
  • Dutt P, et al. 2006. m-Calpain is required for preimplantation embryonic development in mice. BMC Dev. Biol. 6:3. https://doi.org/10.1186/1471-213X-6-3.
  • Faddis BT, Hasbani MJ, Goldberg MP. 1997. Calpain activation contributes to dendritic remodeling after brief excitotoxic injury in vitro. J. Neurosci. 17:951–959.
  • Frey U, Morris RG. 1997. Synaptic tagging and long-term potentiation. Nature 385:533–536.
  • Gellerman DM, Bi X, Baudry M. 1997. NMDA receptor-mediated regulation of AMPA receptor properties in organotypic hippocampal slice cultures. J. Neurochem. 69:131–136.
  • Giorgi C, et al. 2007. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179–191.
  • Goll DE, Thompson VF, Li H, Wei W, Cong J. 2003. The calpain system. Physiol. Rev. 83:731–801.
  • Grammer M, Kuchay S, Chishti A, Baudry M. 2005. Lack of phenotype for LTP and fear conditioning learning in calpain 1 knock-out mice. Neurobiol. Learn. Mem. 84:222–227.
  • Granic I, et al. 2010. Calpain inhibition prevents amyloid-beta-induced neurodegeneration and associated behavioral dysfunction in rats. Neuropharmacology 59:334–342.
  • Hegde AN. 2010. The ubiquitin-proteasome pathway and synaptic plasticity. Learn. Mem. 17:314–327.
  • Hosfield CM, Elce JS, Davies PL, Jia Z. 1999. Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18:6880–6889.
  • Hrabetova S, Sacktor TC. 1996. Bidirectional regulation of protein kinase M zeta in the maintenance of long-term potentiation and long-term depression. J. Neurosci. 16:5324–5333.
  • Huang YS, Kan MC, Lin CL, Richter JD. 2006. CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 25:4865–4876.
  • Huang YS, Richter JD. 2007. Analysis of mRNA translation in cultured hippocampal neurons. Methods Enzymol. 431:143–162.
  • Jang YN, et al. 2009. Calpain-mediated N-cadherin proteolytic processing in brain injury. J. Neurosci. 29:5974–5984.
  • Keleman K, Kruttner S, Alenius M, Dickson BJ. 2007. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci. 10:1587–1593.
  • Lee DH, Goldberg AL. 1998. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8:397–403.
  • Lee HK, Kameyama K, Huganir RL, Bear MF. 1998. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21:1151–1162.
  • Lei Z, Deng P, Li Y, Xu ZC. 2010. Downregulation of Kv4.2 channels mediated by NR2B-containing NMDA receptors in cultured hippocampal neurons. Neuroscience 165:350–362.
  • Lu X, Rong Y, Baudry M. 2000. Calpain-mediated degradation of PSD-95 in developing and adult rat brain. Neurosci. Lett. 286:149–153.
  • Lu X, Rong Y, Bi R, Baudry M. 2000. Calpain-mediated truncation of rat brain AMPA receptors increases their Triton X-100 solubility. Brain Res. 863:143–150.
  • Lugli G, Larson J, Martone ME, Jones Y, Smalheiser NR. 2005. Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner. J. Neurochem. 94:896–905.
  • Nimmrich V, et al. 2008. Inhibition of calpain prevents N-methyl-d-aspartate-induced degeneration of the nucleus basalis and associated behavioral dysfunction. J. Pharmacol. Exp. Ther. 327:343–352.
  • Pariat M, et al. 1997. Proteolysis by calpains: a possible contribution to degradation of p53. Mol. Cell. Biol. 17:2806–2815.
  • Pavlopoulos E, et al. 2011. Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 147:1369–1383.
  • Peng SC, Lai YT, Huang HY, Huang HD, Huang YS. 2010. A novel role of CPEB3 in regulating EGFR gene transcription via association with Stat5b in neurons. Nucleic Acids Res. 38:7446–7457.
  • Pike BR, et al. 2004. Accumulation of calpain and caspase-3 proteolytic fragments of brain-derived alphaII-spectrin in cerebral spinal fluid after middle cerebral artery occlusion in rats. J. Cereb. Blood Flow Metab. 24:98–106.
  • Richter JD. 2007. CPEB: a life in translation. Trends Biochem. Sci. 32:279–285.
  • Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 23:1–11.
  • Ruiz-Vela A, Gonzalez de Buitrago G, Martinez AC. 1999. Implication of calpain in caspase activation during B cell clonal deletion. EMBO J. 18:4988–4998.
  • Salehi-Ashtiani K, Luptak A, Litovchick A, Szostak JW. 2006. A genomewide search for ribozymes reveals an HDV-like sequence in the human CPEB3 gene. Science 313:1788–1792.
  • Sha D, et al. 2008. Role of mu-calpain in proteolytic cleavage of brain L-glutamic acid decarboxylase. Brain Res. 1207:9–18.
  • Siman R, Baudry M, Lynch G. 1985. Regulation of glutamate receptor binding by the cytoskeletal protein fodrin. Nature 313:225–228.
  • Staubli U, Larson J, Thibault O, Baudry M, Lynch G. 1988. Chronic administration of a thiol-proteinase inhibitor blocks long-term potentiation of synaptic responses. Brain Res. 444:153–158.
  • Steward O, Wallace CS, Lyford GL, Worley PF. 1998. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741–751.
  • Suzuki K, Hata S, Kawabata Y, Sorimachi H. 2004. Structure, activation, and biology of calpain. Diabetes 53(Suppl 1):S12–S18.
  • Takano J, et al. 2011. Vital role of the calpain-calpastatin system for placental-integrity-dependent embryonic survival. Mol. Cell. Biol. 31:4097–4106.
  • Tan Y, et al. 2006. Conditional disruption of ubiquitous calpains in the mouse. Genesis 44:297–303.
  • Tomimatsu Y, Idemoto S, Moriguchi S, Watanabe S, Nakanishi H. 2002. Proteases involved in long-term potentiation. Life Sci. 72:355–361.
  • Vogler C, et al. 2009. CPEB3 is associated with human episodic memory. Front. Behav. Neurosci. 3:4. https://doi.org/10.3389/neuro.08.004.2009.
  • Vosler PS, et al. 2011. Ischemia-induced calpain activation causes eukaryotic (translation) initiation factor 4G1 (eIF4GI) degradation, protein synthesis inhibition, and neuronal death. Proc. Natl. Acad. Sci. U. S. A. 108:18102–18107.
  • Wright JW, Harding JW. 2009. Contributions of matrix metalloproteinases to neural plasticity, habituation, associative learning and drug addiction. Neural Plast. 2009:579382. https://doi.org/10.1155/2009/579382.
  • Wu HY, et al. 2005. Regulation of N-methyl-d-aspartate receptors by calpain in cortical neurons. J. Biol. Chem. 280:21588–21593.
  • Yuen EY, Gu Z, Yan Z. 2007. Calpain regulation of AMPA receptor channels in cortical pyramidal neurons. J. Physiol. 580:241–254.

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