Excitotoxic neuroprotection and vulnerability with CaMKII inhibition

Albers, 1999, Dose escalation study of the NMDA glycine-site antagonist licostinel in acute ischemic stroke, Stroke, 30, 508, 10.1161/01.STR.30.3.508 Aronowski, 1996, Ca2+/calmodulin-dependent protein kinase II in postsynaptic densities after reversible cerebral ischemia in rats, Brain Res., 709, 103, 10.1016/0006-8993(95)01311-3 Aronowski, 1992, Ischemia-induced translocation of Ca2+/calmodulin-dependent protein kinase II: potential role in neuronal damage, J. Neurochem., 58, 1743, 10.1111/j.1471-4159.1992.tb10049.x Bok, 2007, CaMKII and CaMKIV mediate distinct prosurvival signaling pathways in response to depolarization in neurons, Mol. Cell. Neurosci., 36, 13, 10.1016/j.mcn.2007.05.008 Bradshaw, 2002, Chemical quenched flow kinetic studies indicate an intraholoenzyme autophosphorylation mechanism for Ca2+/calmodulin-dependent protein kinase II, J. Biol. Chem., 277, 20991, 10.1074/jbc.M202154200 Bredesen, 2007, Key note lecture: toward a mechanistic taxonomy for cell death programs, Stroke, 38, 652, 10.1161/01.STR.0000257802.82826.a7 Burgin, 1990, In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain, J. Neurosci., 10, 1788, 10.1523/JNEUROSCI.10-06-01788.1990 Chang, 1998, Characterization of a calmodulin kinase II inhibitor protein in brain, Proc. Natl Acad. Sci. USA, 95, 10890, 10.1073/pnas.95.18.10890 Chao, 2010, Intersubunit capture of regulatory segments is a component of cooperative CaMKII activation, Nat. Struct. Mol. Biol., 17, 264, 10.1038/nsmb.1751 Chen, 2008, NS21: re-defined and modified supplement B27 for neuronal cultures, J. Neurosci. Methods, 171, 239, 10.1016/j.jneumeth.2008.03.013 Choi, 1985, Glutamate neurotoxicity in cortical cell culture is calcium dependent, Neurosci. Lett., 58, 293, 10.1016/0304-3940(85)90069-2 Churn, 1995, Excitotoxic activation of the NMDA receptor results in inhibition of calcium/calmodulin kinase II activity in cultured hippocampal neurons, J. Neurosci., 15, 3200, 10.1523/JNEUROSCI.15-04-03200.1995 Dash, 1991, cAMP response element-binding protein is activated by Ca2+/calmodulin- as well as cAMP-dependent protein kinase, Proc. Natl Acad. Sci. USA, 88, 5061, 10.1073/pnas.88.11.5061 Davis, 2000, Selfotel in acute ischemic stroke: possible neurotoxic effects of an NMDA antagonist, Stroke, 31, 347, 10.1161/01.STR.31.2.347 Deshpande, 1992, Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: evidence against programmed cell death, Exp. Brain Res., 88, 91, 10.1007/BF02259131 Dirnagl, 1999, Pathobiology of ischaemic stroke: an integrated view, Trends Neurosci., 22, 391, 10.1016/S0166-2236(99)01401-0 Dosemeci, 2000, A novel particulate form of Ca(2+)/calmodulin-dependent [correction of Ca(2+)/CaMKII-dependent] protein kinase II in neurons, J. Neurosci., 20, 3076, 10.1523/JNEUROSCI.20-09-03076.2000 Dosemeci, 2001, Glutamate-induced transient modification of the postsynaptic density, Proc. Natl Acad. Sci. USA, 98, 10428, 10.1073/pnas.181336998 Enslen, 1994, Characterization of Ca2+/calmodulin-dependent protein kinase IV. Role in transcriptional regulation, J. Biol. Chem., 269, 15520, 10.1016/S0021-9258(17)40710-1 Fan, 2006, The role of CaMKII in BDNF-mediated neuroprotection of retinal ganglion cells (RGC-5), Brain Res., 1067, 48, 10.1016/j.brainres.2005.10.030 Fink, 2003, Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII, Neuron, 39, 283, 10.1016/S0896-6273(03)00428-8 Foster, 1987, Systemic administration of MK-801 prevents N-methyl-D-aspartate-induced neuronal degeneration in rat brain, Neurosci. Lett., 76, 307, 10.1016/0304-3940(87)90420-4 Frank, 2002, The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports—principles and applications, J. Immunol. Methods, 267, 13, 10.1016/S0022-1759(02)00137-0 Frank, 1996, SPOT synthesis. Epitope analysis with arrays of synthetic peptides prepared on cellulose membranes, Methods Mol. Biol., 66, 149 Fu, 2004, NMDA receptor-mediated immediate Ser831 phosphorylation of GluR1 through CaMKIIalpha in rat hippocampus during early global ischemia, Neurosci. Res., 48, 85, 10.1016/j.neures.2003.09.009 Gao, 2006, CaMKII-independent effects of KN93 and its inactive analog KN92: reversible inhibition of L-type calcium channels, Biochem. Biophys. Res. Commun., 345, 1606, 10.1016/j.bbrc.2006.05.066 Goebel, 2009, Selective blockade of CaMKII-alpha inhibits NMDA-induced caspase-3-dependent cell death but does not arrest PARP-1 activation or loss of plasma membrane selectivity in rat retinal neurons, Brain Res., 1256, 190, 10.1016/j.brainres.2008.12.051 Hajimohammadreza, 1995, A specific inhibitor of calcium/calmodulin-dependent protein kinase-II provides neuroprotection against NMDA- and hypoxia/hypoglycemia-induced cell death, J. Neurosci., 15, 4093, 10.1523/JNEUROSCI.15-05-04093.1995 Hanson, 1994, Calcium/calmodulin-dependent protein kinase II activity in focal ischemia with reperfusion in rats, Stroke, 25, 466, 10.1161/01.STR.25.2.466 Hao, 2005, Calcium/calmodulin-dependent protein kinase II (CaMKII), through NMDA receptors and L-voltage-gated channels, modulates the serine phosphorylation of GluR6 during cerebral ischemia and early reperfusion period in rat hippocampus, Brain Res. Mol. Brain Res., 140, 55, 10.1016/j.molbrainres.2005.07.005 Houston, 2006, CaMK-II modulation of GABA(A) receptors expressed in HEK293, NG108-15 and rat cerebellar granule neurons, Eur. J. Neurosci., 24, 2504, 10.1111/j.1460-9568.2006.05145.x Hoyte, 2004, The rise and fall of NMDA antagonists for ischemic stroke, Curr. Mol. Med., 4, 131, 10.2174/1566524043479248 Hu, 1998, Assembly of proteins to postsynaptic densities after transient cerebral ischemia, J. Neurosci., 18, 625, 10.1523/JNEUROSCI.18-02-00625.1998 Hudmon, 2002, Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function, Annu. Rev. Biochem., 71, 473, 10.1146/annurev.biochem.71.110601.135410 Hudmon, 1996, Inactivation and self-association of Ca2+/calmodulin-dependent protein kinase II during autophosphorylation, J. Biol. Chem., 271, 8800, 10.1074/jbc.271.15.8800 Hudmon, 2005, A mechanism for Ca2+/calmodulin-dependent protein kinase II clustering at synaptic and nonsynaptic sites based on self-association, J. Neurosci., 25, 6971, 10.1523/JNEUROSCI.4698-04.2005 Ishida, 1995, A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II, Biochem. Biophys. Res. Commun., 212, 806, 10.1006/bbrc.1995.2040 Kolb, 1995, Ca2+/calmodulin kinase II translocates in a hippocampal slice model of ischemia, J. Neurochem., 64, 2147, 10.1046/j.1471-4159.1995.64052147.x Laabich, 2000, Neuroprotective effect of AIP on N-methyl-D-aspartate-induced cell death in retinal neurons, Brain Res. Mol. Brain Res., 85, 32, 10.1016/S0169-328X(00)00226-6 Ledoux, 1999, Inhibitors of calmodulin-dependent protein kinase are nonspecific blockers of voltage-dependent K+ channels in vascular myocytes, J. Pharmacol. Exp. Ther., 290, 1165 Lipton, 1999, Ischemic cell death in brain neurons, Physiol. Rev., 79, 1431, 10.1152/physrev.1999.79.4.1431 Lisman, 2002, The molecular basis of CaMKII function in synaptic and behavioural memory, Nat. Rev. Neurosci., 3, 175, 10.1038/nrn753 Meng, 2002, Autophosphorylated calcium/calmodulin-dependent protein kinase II alpha induced by cerebral ischemia immediately targets and phosphorylates N-methyl-D-aspartate receptor subunit 2B (NR2B) in hippocampus of rats, Neurosci. Lett., 333, 59, 10.1016/S0304-3940(02)00961-8 Miller, 1986, Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch, Cell, 44, 861, 10.1016/0092-8674(86)90008-5 Morioka, 1995, Glutamate-induced loss of Ca2+/calmodulin-dependent protein kinase II activity in cultured rat hippocampal neurons, J. Neurochem., 64, 2132, 10.1046/j.1471-4159.1995.64052132.x Morris, 1999, Failure of the competitive N-methyl-D-aspartate antagonist Selfotel (CGS 19755) in the treatment of severe head injury: results of two phase III clinical trials. The Selfotel Investigators, J. Neurosurg., 91, 737, 10.3171/jns.1999.91.5.0737 Olney, 1969, Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate, Science, 164, 719, 10.1126/science.164.3880.719 Olney, 1971, Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study, J. Neuropathol. Exp. Neurol., 30, 75, 10.1097/00005072-197101000-00008 Olney, 1969, Brain lesions in an infant rhesus monkey treated with monosodium glutamate, Science, 166, 386, 10.1126/science.166.3903.386 Omae, 1996, The competitive NMDA antagonist, CGS-19755, improves postischemic hypoperfusion in selectively vulnerable regions in gerbils, J. Neurol. Sci., 138, 105, 10.1016/0022-510X(96)00004-4 Onodera, 1995, Calcium/calmodulin-dependent protein kinase II and protein phosphatase 2B (calcineurin) immunoreactivity in the rat hippocampus long after ischemia, Brain Res., 684, 95, 10.1016/0006-8993(95)00382-Z Perlin, 1992, Loss of type II calcium/calmodulin-dependent kinase activity correlates with stages of development of electrographic seizures in status epilepticus in rat, Epilepsy Res., 11, 111, 10.1016/0920-1211(92)90045-U Pohorecki, 1990, Ischemic brain injury in vitro: protective effects of NMDA receptor antagonists and calmidazolium, Brain Res., 528, 133, 10.1016/0006-8993(90)90205-P Portera-Cailliau, 1997, Excitotoxic neuronal death in the immature brain is an apoptosis–necrosis morphological continuum, J. Comp. Neurol., 378, 70, 10.1002/(SICI)1096-9861(19970203)378:1<10::AID-CNE4>3.0.CO;2-N Rose, 2003, Exercise increases Ca2+-calmodulin-dependent protein kinase II activity in human skeletal muscle, J. Physiol., 553, 303, 10.1113/jphysiol.2003.054171 Saitoh, 1985, Phosphorylation-dependent subcellular translocation of a Ca2+/calmodulin-dependent protein kinase produces an autonomous enzyme in Aplysia neurons, J. Cell Biol., 100, 835, 10.1083/jcb.100.3.835 Sessoms-Sikes, 2005, CaMKIIalpha enhances the desensitization of NR2B-containing NMDA receptors by an autophosphorylation-dependent mechanism, Mol. Cell. Neurosci., 29, 139, 10.1016/j.mcn.2005.01.006 Sinor, 2000, NMDA and glutamate evoke excitotoxicity at distinct cellular locations in rat cortical neurons in vitro, J. Neurosci., 20, 8831, 10.1523/JNEUROSCI.20-23-08831.2000 Smith, 1990, Specificities of autoinhibitory domain peptides for four protein kinases. Implications for intact cell studies of protein kinase function, J. Biol. Chem., 265, 1837, 10.1016/S0021-9258(19)39904-1 Snider, 1999, Apoptosis and necrosis in cerebrovascular disease, Ann. NY Acad. Sci., 893, 243, 10.1111/j.1749-6632.1999.tb07829.x Sumi, 1991, The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells, Biochem. Biophys. Res. Commun., 181, 968, 10.1016/0006-291X(91)92031-E Suzuki, 1994, Rapid translocation of cytosolic Ca2+/calmodulin-dependent protein kinase II into postsynaptic density after decapitation, J. Neurochem., 63, 1529, 10.1046/j.1471-4159.1994.63041529.x Suzuki, 2003, Ability of NMDA and non-NMDA receptor antagonists to inhibit cerebral ischemic damage in aged rats, Brain Res., 964, 116, 10.1016/S0006-8993(02)04088-X Szydlowska, 2010, Calcium, ischemia and excitotoxicity, Cell Calcium, 47, 122, 10.1016/j.ceca.2010.01.003 Takagi, 2003, Transient global ischemia enhances phosphorylation of the GluR1 subunit of the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate receptor in the hippocampal CA1 region in rats, Neurosci. Lett., 341, 33, 10.1016/S0304-3940(03)00153-8 Takano, 2003, Calmodulin and calmodulin-dependent kinase II mediate neuronal cell death induced by depolarization, Brain Res., 962, 41, 10.1016/S0006-8993(02)03932-X Tao-Cheng, 2002, Calcium/calmodulin-dependent protein kinase II clusters in adult rat hippocampal slices, Neuroscience, 115, 435, 10.1016/S0306-4522(02)00451-7 Vaslin, 2009, Unconjugated TAT carrier peptide protects against excitotoxicity, Neurotox. Res., 15, 123, 10.1007/s12640-009-9012-6 Vest, 2007, Dual mechanism of a natural CaMKII inhibitor, Mol. Biol. Cell, 18, 5024, 10.1091/mbc.E07-02-0185 Vest, 2010, Effective post-insult neuroprotection by a novel Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) inhibitor, J. Biol. Chem., 285, 20675, 10.1074/jbc.M109.088617 Waxham, 1996, Ischemia-induced neuronal damage: a role for calcium/calmodulin-dependent protein kinase II, J. Cereb. Blood Flow Metab., 16, 1, 10.1097/00004647-199601000-00001 Westgate, 1994, Activity of Ca2+/calmodulin-dependent protein kinase II following ischemia: a comparison between CA1 and dentate gyrus in a hippocampal slice model, J. Neurochem., 63, 2217, 10.1046/j.1471-4159.1994.63062217.x Wheeler, 2008, CaMKII locally encodes L-type channel activity to signal to nuclear CREB in excitation–transcription coupling, J. Cell Biol., 183, 849, 10.1083/jcb.200805048 Zalewska, 1996, Brain ischaemia transiently activates Ca2+/calmodulin-independent protein kinase II, NeuroReport, 7, 637, 10.1097/00001756-199601310-00062 Zalewska, 1996, Changes of Ca2+/calmodulin-dependent protein kinase-II after transient ischemia in gerbil hippocampus, Acta Neurobiol Exp (Wars), 56, 41