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Targeting calpain in synaptic plasticity

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Pages 579-592 | Published online: 04 Feb 2013

Bibliography

  • Lynch G, Baudry M. The biochemistry of memory: a new and specific hypothesis. Science 1984;224:1057-63
  • Liu J, Liu MC, Wang KK. Physiological and pathological actions of calpains in glutamatergic neurons. Sci Signal 2008;1:tr3
  • Wu HY, Lynch DR. Calpain and synaptic function. Mol Neurobiol 2006;33:215-36
  • Denny JB, Polan-Curtain J, Ghuman A, Calpain inhibitors block long-term potentiation. Brain Res 1990;534:317-20
  • del Cerro S, Larson J, Oliver MW, Development of hippocampal long-term potentiation is reduced by recently introduced calpain inhibitors. Brain Res 1990;530:91-5
  • Oliver MW, Baudry M, Lynch G. The protease inhibitor leupeptin interferes with the development of LTP in hippocampal slices. Brain Res 1989;505:233-8
  • Staubli U, Larson J, Thibault O, Chronic administration of a thiol-proteinase inhibitor blocks long-term potentiation of synaptic responses. Brain Res 1988;444:153-8
  • Muller D, Molinari I, Soldati L, A genetic deficiency in calpastatin and isovalerylcarnitine treatment is associated with enhanced hippocampal long-term potentiation. Synapse 1995;19:37-45
  • Grammer M, Kuchay S, Chishti A, Lack of phenotype for LTP and fear conditioning learning in calpain 1 knock-out mice. Neurobiol Learn Mem 2005;84:222-7
  • Zadran S, Akopian G, Zadran H, RVG-mediated Calpain2 gene silencing in the brain impairs learning and memory. Neuromolecular Med 2012; Epub ahead of print
  • Morris RG, Anderson E, Lynch GS, Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 1986;319:774-6
  • Cao G, Xing J, Xiao X, Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J Neurosci 2007;27:9278-93
  • Sorimachi H, Hata S, Ono Y. Impact of genetic insights into calpain biology. J Biochem 2011;150:23-37
  • Nakagawa K, Masumoto H, Sorimachi H, Dissociation of m-calpain subunits occurs after autolysis of the N-terminus of the catalytic subunit, and is not required for activation. J Biochem 2001;130:605-11
  • Moldoveanu T, Jia Z, Davies PL. Calpain activation by cooperative Ca2+ binding at two non-EF-hand sites. J Biol Chem 2004;279:6106-14
  • Tompa P, Emori Y, Sorimachi H, Domain III of calpain is a ca2+-regulated phospholipid-binding domain. Biochem Biophys Res Commun 2001;280:1333-9
  • Hosfield CM, Elce JS, Davies PL, Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. Embo J 1999;18:6880-9
  • Cong J, Goll DE, Peterson AM, The role of autolysis in activity of the Ca2+-dependent proteinases (mu-calpain and m-calpain). J Biol Chem 1989;264:10096-103
  • Kapprell HP, Goll DE. Effect of Ca2+ on binding of the calpains to calpastatin. J Biol Chem 1989;264:17888-96
  • Maravall M, Mainen ZF, Sabatini BL, Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 2000;78:2655-67
  • Schollmeyer JE. Calpain II involvement in mitosis. Science 1988;240:911-13
  • Sarin A, Adams DH, Henkart PA. Protease inhibitors selectively block T cell receptor-triggered programmed cell death in a murine T cell hybridoma and activated peripheral T cells. J Exp Med 1993;178:1693-700
  • Glading A, Bodnar RJ, Reynolds IJ, Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol Cell Biol 2004;24:2499-512
  • Shao H, Chou J, Baty CJ, Spatial localization of m-calpain to the plasma membrane by phosphoinositide biphosphate binding during epidermal growth factor receptor-mediated activation. Mol Cell Biol 2006;26:5481-96
  • Zadran S, Jourdi H, Rostamiani K, Brain-derived neurotrophic factor and epidermal growth factor activate neuronal m-calpain via mitogen-activated protein kinase-dependent phosphorylation. J Neurosci 2010;30:1086-95
  • Abe K, Takeichi M. NMDA-receptor activation induces calpain-mediated beta-catenin cleavages for triggering gene expression. Neuron 2007;53:387-97
  • Franco SJ, Huttenlocher A. Regulating cell migration: calpains make the cut. J Cell Sci 2005;118:3829-38
  • Glading A, Lauffenburger DA, Wells A. Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol 2002;12:46-54
  • Tomimatsu Y, Idemoto S, Moriguchi S, Proteases involved in long-term potentiation. Life Sci 2002;72:355-61
  • Wang KK. Calpain and caspase: can you tell the difference? Trends Neurosci 2000;23:20-6
  • Crocker SJ, Smith PD, Jackson-Lewis V, Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J Neurosci 2003;23:4081-91
  • Gafni J, Ellerby LM. Calpain activation in Huntington's disease. J Neurosci 2002;22:4842-9
  • Saito K, Elce JS, Hamos JE, Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc Natl Acad Sci USA 1993;90:2628-32
  • Xu W, Wong TP, Chery N, Calpain-mediated mGluR1alpha truncation: a key step in excitotoxicity. Neuron 2007;53:399-412
  • Donkor IO. Calpain inhibitors: a survey of compounds reported in the patent and scientific literature. Expert Opin Ther Patents 2011;21:601-36
  • Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 2008;456:409-12
  • Carlin RK, Bartelt DC, Siekevitz P. Identification of fodrin as a major calmodulin-binding protein in postsynaptic density preparations. J Cell Biol 1983;96:443-8
  • Bennett V. Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm. Physiol Rev 1990;70:1029-65
  • Banik NL, Matzelle DC, Gantt-Wilford G, Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res 1997;752:301-6
  • Fischer I, Romano-Clarke G, Grynspan F. Calpain-mediated proteolysis of microtubule associated proteins MAP1B and MAP2 in developing brain. Neurochem Res 1991;16:891-8
  • Johnson GV, Litersky JM, Jope RS. Degradation of microtubule-associated protein 2 and brain spectrin by calpain: a comparative study. J Neurochem 1991;56:1630-8
  • Potter DA, Tirnauer JS, Janssen R, Calpain regulates actin remodeling during cell spreading. J Cell Biol 1998;141:647-62
  • Perrin BJ, Amann KJ, Huttenlocher A. Proteolysis of cortactin by calpain regulates membrane protrusion during cell migration. Mol Biol Cell 2006;17:239-50
  • Dulong S, Goudenege S, Vuillier-Devillers K, Myristoylated alanine-rich C kinase substrate (MARCKS) is involved in myoblast fusion through its regulation by protein kinase Calpha and calpain proteolytic cleavage. Biochem J 2004;382:1015-23
  • Carroll RC, Zukin RS. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 2002;25:571-7
  • Lynch DR, Guttmann RP. Excitotoxicity: perspectives based on N-methyl-D-aspartate receptor subtypes. J Pharmacol Exp Ther 2002;300:717-23
  • Wu HY, Yuen EY, Lu YF, Regulation of N-methyl-D-aspartate receptors by calpain in cortical neurons. J Biol Chem 2005;280:21588-93
  • Bi X, Chen J, Dang S, Characterization of calpain-mediated proteolysis of GluR1 subunits of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors in rat brain. J Neurochem 1997;68:1484-94
  • Lu X, Rong Y, Bi R, Calpain-mediated truncation of rat brain AMPA receptors increases their Triton X-100 solubility. Brain Res 2000;863:143-50
  • Bano D, Young KW, Guerin CJ, Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity. Cell 2005;120:275-85
  • Hell JW, Westenbroek RE, Breeze LJ, N-methyl-D-aspartate receptor-induced proteolytic conversion of postsynaptic class C L-type calcium channels in hippocampal neurons. Proc Natl Acad Sci USA 1996;93:3362-7
  • Magnusson A, Haug LS, Walaas SI, Calcium-induced degradation of the inositol (1,4,5)-trisphosphate receptor/Ca(2+)-channel. FEBS Lett 1993;323:229-32
  • Dong YN, Waxman EA, Lynch DR. Interactions of postsynaptic density-95 and the NMDA receptor 2 subunit control calpain-mediated cleavage of the NMDA receptor. J Neurosci 2004;24:11035-45
  • Jourdi H, Lu X, Yanagihara T, Prolonged positive modulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors induces calpain-mediated PSD-95/Dlg/ZO-1 protein degradation and AMPA receptor down-regulation in cultured hippocampal slices. J Pharmacol Exp Ther 2005;314:16-26
  • Lu X, Rong Y, Baudry M. Calpain-mediated degradation of PSD-95 in developing and adult rat brain. Neurosci Lett 2000;286:149-53
  • Sans N, Petralia RS, Wang YX, A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 2000;20:1260-71
  • Jourdi H, Iwakura Y, Narisawa-Saito M, Brain-derived neurotrophic factor signal enhances and maintains the expression of AMPA receptor-associated PDZ proteins in developing cortical neurons. Dev Biol 2003;263:216-30
  • Yu L, Rostamiani K, Hsu YT, Calpain-mediated regulation of stargazin in adult rat brain. Neuroscience 2011;178:13-20
  • Fukunaga K, Soderling TR, Miyamoto E. Activation of Ca2+/calmodulin-dependent protein kinase II and protein kinase C by glutamate in cultured rat hippocampal neurons. J Biol Chem 1992;267:22527-33
  • Tan SE, Wenthold RJ, Soderling TR. Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulin-dependent protein kinase II and protein kinase C in cultured hippocampal neurons. J Neurosci 1994;14:1123-9
  • Hajimohammadreza I, Raser KJ, Nath R, Neuronal nitric oxide synthase and calmodulin-dependent protein kinase IIalpha undergo neurotoxin-induced proteolysis. J Neurochem 1997;69:1006-13
  • Hrabetova S, Sacktor TC. Bidirectional regulation of protein kinase M zeta in the maintenance of long-term potentiation and long-term depression. J Neurosci 1996;16:5324-33
  • Wu HY, Tomizawa K, Oda Y, Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J Biol Chem 2004;279:4929-40
  • Denny JB, Polan-Curtain J, Rodriguez S, Evidence that protein kinase M does not maintain long-term potentiation. Brain Res 1990;534:201-8
  • Malinow R, Schulman H, Tsien RW. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 1989;245:862-6
  • Otmakhov N, Griffith LC, Lisman JE. Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 1997;17:5357-65
  • Hu GY, Hvalby O, Walaas SI, Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation. Nature 1987;328:426-9
  • Lledo PM, Hjelmstad GO, Mukherji S, Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci USA 1995;92:11175-9
  • Xu L, Deng X. Suppression of cancer cell migration and invasion by protein phosphatase 2A through dephosphorylation of mu- and m-calpains. J Biol Chem 2006;281:35567-75
  • Tallant EA, Brumley LM, Wallace RW. Activation of a calmodulin-dependent phosphatase by a Ca2+-dependent protease. Biochemistry 1988;27:2205-11
  • Baumgartel K, Mansuy IM. Neural functions of calcineurin in synaptic plasticity and memory. Learn Mem 2012;19:375-84
  • Evergren E, Marcucci M, Tomilin N, Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 2004;5:514-28
  • Wigge P, McMahon HT. The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci 1998;21:339-44
  • Zhang B, Zelhof AC. Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin-Rvsp. Traffic 2002;3:452-60
  • Wu Y, Liang S, Oda Y, Truncations of amphiphysin I by calpain inhibit vesicle endocytosis during neural hyperexcitation. Embo J 2007;26:2981-90
  • Di Rosa G, Odrijin T, Nixon RA, Calpain inhibitors: a treatment for Alzheimer's disease. J Mol Neurosci 2002;19:135-41
  • Ando K, Kudo Y, Takahashi M. Negative regulation of neurotransmitter release by calpain: a possible involvement of specific SNAP-25 cleavage. J Neurochem 2005;94:651-8
  • Grumelli C, Berghuis P, Pozzi D, Calpain activity contributes to the control of SNAP-25 levels in neurons. Mol Cell Neurosci 2008;39:314-23
  • Bi X, Chen J, Baudry M. Developmental changes in calpain activity, GluR1 receptors and in the effect of kainic acid treatment in rat brain. Neuroscience 1997;81:1123-35
  • Carragher NO, Frame MC. Calpain: a role in cell transformation and migration. Int J Biochem Cell Biol 2002;34:1539-43
  • Lebart MC, Benyamin Y. Calpain involvement in the remodeling of cytoskeletal anchorage complexes. FEBS J 2006;273:3415-26
  • Perrin BJ, Huttenlocher A. Calpain. Int J Biochem Cell Biol 2002;34:722-5
  • Vanderklish P, Saido TC, Gall C, Proteolysis of spectrin by calpain accompanies theta-burst stimulation in cultured hippocampal slices. Mol Brain Res 1995;32:25-35
  • Flevaris P, Stojanovic A, Gong H, A molecular switch that controls cell spreading and retraction. J Cell Biol 2007;179:553-65
  • Szczepanowska J. Involvement of Rac/Cdc42/PAK pathway in cytoskeletal rearrangements. Acta Biochim Pol 2009;56:225-34
  • Kulkarni S, Goll DE, Fox JE. Calpain cleaves RhoA generating a dominant-negative form that inhibits integrin-induced actin filament assembly and cell spreading. J Biol Chem 2002;277:24435-41
  • Du X, Saido TC, Tsubuki S, Calpain cleavage of the cytoplasmic domain of the integrin beta 3 subunit. J Biol Chem 1995;270:26146-51
  • Sawhney RS, Cookson MM, Omar Y, Integrin alpha2-mediated ERK and calpain activation play a critical role in cell adhesion and motility via focal adhesion kinase signaling: identification of a novel signaling pathway. J Biol Chem 2006;281:8497-510
  • Chan KT, Bennin DA, Huttenlocher A. Regulation of adhesion dynamics by calpain-mediated proteolysis of focal adhesion kinase (FAK). J Biol Chem 2010;285:11418-26
  • Shi Y, Pontrello CG, DeFea KA, Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J Neurosci 2009;29:8129-42
  • Faivre-Sarrailh C, Lena JY, Had L, Location of profilin at presynaptic sites in the cerebellar cortex; implication for the regulation of the actin-polymerization state during axonal elongation and synaptogenesis. J Neurocytol 1993;22:1060-72
  • Gungabissoon RA, Bamburg JR. Regulation of growth cone actin dynamics by ADF/cofilin. J Histochem Cytochem 2003;51:411-20
  • Hatada Y, Wu F, Sun ZY, Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at preexisting varicositis. J Neurosci 2000;20:RC82
  • Kuhn TB, Meberg PJ, Brown MD, Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. J Neurobiol 2000;44:126-44
  • Pham H, Yu H, Laski FA. Cofilin/ADF is required for retinal elongation and morphogenesis of the Drosophila rhabdomere. Dev Biol 2008;318:82-91
  • Rosenmund C, Westbrook GL. Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 1993;10:805-14
  • Meng Y, Zhang Y, Tregoubov V, Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 2002;35:121-33
  • Nishita M, Tomizawa C, Yamamoto M, Spatial and temporal regulation of cofilin activity by LIM kinase and Slingshot is critical for directional cell migration. J Cell Biol 2005;171:349-59
  • Ammer AG, Weed SA. Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 2008;65:687-707
  • Hering H, Sheng M. Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J Neurosci 2003;23:11759-69
  • Huang C, Tandon NN, Greco NJ, Proteolysis of platelet cortactin by calpain. J Biol Chem 1997;272:19248-52
  • Mingorance-Le Meur A, O'Connor TP. Neurite consolidation is an active process requiring constant repression of protrusive activity. EMBO J 2009;28:248-60
  • Routtenberg A, Rekart JL. Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci 2005;28:12-19
  • Kelleher RJ III, Govindarajan A, Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 2004;44:59-73
  • Frey U, Morris RG. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 1998;21:181-8
  • Bailey CH, Bartsch D, Kandel ER. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 1996;93:13445-52
  • Schuman EM, Dynes JL, Steward O. Synaptic regulation of translation of dendritic mRNAs. J Neurosci 2006;26:7143-6
  • Steward O, Schuman EM. Compartmentalized synthesis and degradation of proteins in neurons. Neuron 2003;40:347-59
  • Pfeiffer BE, Huber KM. Current advances in local protein synthesis and synaptic plasticity. J Neurosci 2006;26:7147-50
  • Tang SJ, Reis G, Kang H, A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci USA 2002;99:467-72
  • Nguyen PV. Protein synthesis during LTP: linking synaptic activity to translation. Trends Neurosci 2002;25:180
  • Bradshaw KD, Emptage NJ, Bliss TV. A role for dendritic protein synthesis in hippocampal late LTP. Eur J Neurosci 2003;18:3150-2
  • Gold PE. Protein synthesis inhibition and memory: formation vs amnesia. Neurobiol Learn Mem 2008;89:201-11
  • Kramar EA, Lin B, Lin CY, A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J Neurosci 2004;24:5151-61
  • Lynch G, Rex CS, Gall CM. LTP consolidation: substrates, explanatory power, and functional significance. Neuropharmacology 2007;52:12-23
  • Kang H, Schuman EM. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995;267:1658-62
  • Schuman EM. Neurotrophin regulation of synaptic transmission. Curr Opin Neurobiol 1999;9:105-9
  • Kanhema T, Dagestad G, Panja D, Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: evidence for compartment-specific translation control. J Neurochem 2006;99:1328-37
  • Soule J, Messaoudi E, Bramham CR. Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain. Biochem Soc Trans 2006;34:600-4
  • Rao VR, Pintchovski SA, Chin J, AMPA receptors regulate transcription of the plasticity-related immediate-early gene Arc. Nat Neurosci 2006;9:887-95
  • Bramham CR, Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 2005;76:99-125
  • Sutton MA, Schuman EM. Local translational control in dendrites and its role in long-term synaptic plasticity. J Neurobiol 2005;64:116-31
  • Giovannini MG. The role of the extracellular signal-regulated kinase pathway in memory encoding. Rev Neurosci 2006;17:619-34
  • Sweatt JD. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 2004;14:311-17
  • Shimizu K, Phan T, Mansuy IM, Proteolytic degradation of SCOP in the hippocampus contributes to activation of MAP kinase and memory. Cell 2007;128:1219-29
  • Oliver MW, Baudry M, Lynch G. The protease inhibitor leupeptin interferes with the development of LTP in hippocampal slices. Brain Res 1989;505:233-8
  • Vanderklish P, Bednarski E, Lynch G. Translational suppression of calpain blocks long-term potentiation. Learn Mem 1996;3:209-17
  • Murachi T. Calcium-dependent proteinases and specific inhibitors: calpain and calpastatin. Biochem Soc Symp 1984;49:149-67
  • Gartner A, Staiger V. Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns. Proc Natl Acad Sci USA 2002;99:6386-91
  • Aicardi G, Argilli E, Cappello S, Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. Proc Natl Acad Sci USA 2004;101:15788-92
  • Emes RD, Grant SG. The human postsynaptic density shares conserved elements with proteomes of unicellular eukaryotes and prokaryotes. Front Neurosci 2011;5:44
  • Zhao S, Liang Z, Demko V, Massive expansion of the calpain gene family in unicellular eukaryotes. BMC Evol Biol 2012;12:193
  • Leloup L, Wells A. Calpains as potential anti-cancer targets. Expert Opin Ther Targets 2011;15:309-23
  • Yamada M, Hirotsune S, Wynshaw-Boris A. A novel strategy for therapeutic intervention for the genetic disease: preventing proteolytic cleavage using small chemical compound. Int J Biochem Cell Biol 2010;42:1401-7
  • Simoes AT, Goncalves N, Koeppen A, Calpastatin-mediated inhibition of calpains in the mouse brain prevents mutant ataxin 3 proteolysis, nuclear localization and aggregation, relieving Machado-Joseph disease. Brain 2012;135:2428-39
  • Higuchi M, Tomioka M, Takano J, Distinct mechanistic roles of calpain and caspase activation in neurodegeneration as revealed in mice overexpressing their specific inhibitors. J Biol Chem 2005;280:15229-37
  • Vosler PS, Brennan CS, Chen J. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol Neurobiol 2008;38:78-100
  • Zatz M, Starling A. Calpains and disease. N Engl J Med 2005;352:2413-23
  • Wei X, Miou Z, Baudry M. Neuroprotection by cell permeable TAT-mGluR1 peptide in ischemia: synergy between carrier and cargo sequences. Neuroscientist 2008;14:409-14

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