Opposing action of conantokin-G on synaptically and extrasynaptically- activated NMDA receptors

Neuropharmacology

Volumn 62, Issue 7, 2012, Pages 2227-2238

  Balsara, Rashna ^a   Li, Neill ^a   Weber Adrian, Danielle ^a   Huang, Louxiu ^a   Castellino, Francis J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Actin organization; Conantokin inhibitors; Knockout mice; Neuron signaling; NMDA receptor subunits; NMDAR inhibition; Synaptic and extrasynaptic NMDA receptors

Indexed keywords

ACTIN; CALCIUM ION; CONANTOKIN G; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIZOCILPINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN MITOCHONDRION; CALCIUM TRANSPORT; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; DRUG TARGETING; EMBRYO; ENZYME ACTIVATION; MOUSE; NERVE CELL; NERVE POTENTIAL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; SYNAPSE; WILD TYPE;

EID: 84863420876     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.01.018     Document Type: Article

References (68)

1. K. Akashi, T. Kakizaki, H. Kamiya, M. Fukaya, M. Yamasaki, M. Abe, R. Natsume, M. Watanabe, and K. Sakimura NMDA receptor GluN2B (GluR epsilon 2/NR2B) subunit is crucial for channel function, postsynaptic macromolecular organization, and actin cytoskeleton at hippocampal CA3 synapses J. Neurosci. 29 2009 10869 10882
2. T. Arzberger, K. Krampfl, S. Leimgruber, and A. Weindl Changes of NMDA receptor subunit (NR1, NR2B) and glutamate transporter (GLT1) mRNA expression in Huntington's disease-an in situ hybridization study J. Neuropathol. Exp. Neurol. 56 1997 440 454 (Pubitemid 27465027)
3. Y.P. Auberson, H. Allgeier, S. Bischoff, K. Lingenhoehl, R. Moretti, and M. Schmutz 5-phosphonomethylquinoxalinediones as competitive NMDA receptor antagonists with a preference for the human 1A/2A, rather than 1A/2B receptor composition Bioorg. Med. Chem. Lett. 12 2002 1099 1102 (Pubitemid 34242811)
4. M.E. Barton, H.S. White, and K.S. Wilcox The effect of CGX-1007 and CI-1041, novel NMDA receptor antagonists, on NMDA receptor-mediated EPSCs Epilepsy Res. 59 2004 13 24 (Pubitemid 38595417)
5. C.J. Carter, K.G. Lloyd, B. Zivkovic, and B. Scatton Ifenprodil and SL 82.0715 as cerebral antiischemic agents. III. Evidence for antagonistic effects at the polyamine modulatory site within the N-methyl-D-aspartate receptor complex J. Pharmacol. Exp. Ther. 253 1990 475 482 (Pubitemid 20181685)
6. J.E. Chatterton, M. Awobuluyi, L.S. Premkumar, H. Takahashi, M. Talantova, Y. Shin, J.K. Cui, S.C. Tu, A.S.K. Kevin, N. Nakanishi, G. Tong, S.A. Lipton, and D.X. Zhang Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits Nature 415 2002 793 798 (Pubitemid 34150501)
7. B.A. Chizh, and P.M. Headley NMDA antagonists and neuropathic pain-multiple drug targets and multiple uses Curr. Pharm. Des. 11 2005 2977 2994 (Pubitemid 41158087)
8. A.M. Ciabarra, J.M. Sullivan, L.G. Gahn, G. Pecht, S. Heinemann, and K.A. Sevarino Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family J. Neurosci. 15 1995 6498 6508 (Pubitemid 3001297)
9. C.F. Claiborne, J.A. McCauley, B.E. Libby, N.R. Curtis, H.J. Diggle, J.J. Kulagowski, S.R. Michelson, K.D. Anderson, D.A. Claremon, R.M. Freidinger, R.A. Bednar, S.D. Mosser, S.L. Gaul, T.M. Connolly, C.L. Condra, B. Bednar, G.L. Stump, J.J. Lynch, A. Macaulay, K.A. Wafford, K.S. Koblan, and N.J. Liverton Orally efficacious NR2B-selective NMDA receptor antagonists Bioorg. Med. Chem. Lett. 13 2003 697 700 (Pubitemid 36298471)
10. S.G. Cull-Candy, and D.N. Leszkiewicz Role of distinct NMDA receptor subtypes at central synapses Sci. STKE. 2004 2004 re16
11. N.R. Curtis, H.J. Diggle, J.J. Kulagowski, C. London, S. Grimwood, P.H. Hutson, F. Murray, P. Richards, A. Macaulay, and K.A. Wafford Novel N1-(benzyl)cinnamamidine derived NR2B subtype-selective NMDA receptor antagonists Bioorg. Med. Chem. Lett. 13 2003 693 696 (Pubitemid 36298470)
12. S.D. Donevan, and R.T. McCabe Conantokin G is an NR2B-selective competitive antagonist of N-methyl-D-aspartate receptors Mol. Pharmacol. 58 2000 614 623
13. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo Neuron 38 2003 447 460 (Pubitemid 36579146)
14. K.R. Gogas Glutamate-based therapeutic approaches: NR2B receptor antagonists Curr. Opin. Pharmacol. 6 2006 68 74 (Pubitemid 43103821)
15. J.A. Haack, T.N. Parks, and B.M. Olivera Conantokin-G antagonism of the NMDA receptor subtype expressed in cultured cerebellar granule cells Neurosci. Lett. 163 1993 63 66 (Pubitemid 23349395)
16. L.G. Hammerland, B.M. Olivera, and D. Yoshikami Conantokin-G selectively inhibits N-methyl-D-aspartate-induced currents in Xenopus oocytes injected with mouse brain mRNA Eur. J. Pharmacol. 226 1992 239 244
17. G.E. Hardingham, and H. Bading Coupling of extrasynaptic NMDA receptors to a CREB shut-off pathway is developmentally regulated Biochim. Biophys. Acta. 1600 2002 148 153 (Pubitemid 38224409)
18. G.E. Hardingham, Y. Fukunaga, and H. Bading Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways Nat. Neurosci. 5 2002 405 414 (Pubitemid 34454245)
19. M. Hetman, and G. Kharebava Survival signaling pathways activated by NMDA receptors Curr. Top. Med. Chem. 6 2006 787 799
20. M. Hollmann, and S. Heinemann Cloned glutamate receptors Annu. Rev. Neurosci. 17 1994 31 108 (Pubitemid 24117025)
21. L. Huang, R.D. Balsara, Z. Sheng, and F.J. Castellino Conantokins inhibit NMDAR-dependent calcium influx in developing rat hippocampal neurons in primary culture with resulting effects on CREB phosphorylation Mol. Cell. Neurosci. 45 2010 163 172
22. A. Ivanov, C. Pellegrino, S. Rama, I. Dumalska, Y. Salyha, Y. Ben-Ari, and I. Medina Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons J. Physiol. 572 2006 789 798
23. J.D. Jentsch, and R.H. Roth The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia Neuropsychopharmacology 20 1999 201 225 (Pubitemid 29067401)
24. J.A. Kemp, and R.M. McKernan NMDA receptor pathways as drug targets Nat. Neurosci. 5 2002 1039 1042 (Pubitemid 35247194)
25. J.N. Kew, and J.A. Kemp Ionotropic and metabotropic glutamate receptor structure and pharmacology Psychopharmacology 179 2005 4 29 (Pubitemid 40576690)
26. R.C. Klein, Z. Galdzicki, and F.J. Castellino Inhibition of NMDA-induced currents by conantokin-G and conantokin-T in cultured embryonic murine hippocampal neurons Neuropharmacology 38 1999 1819 1829 (Pubitemid 29509720)
27. H.C. Kornau, L.T. Schenker, M. Kennedy, and P.H. Seeburg Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95 Science 269 1995 1737 1740
28. G. Krapivinsky, L. Krapivinsky, Y. Manasian, A. Ivanov, R. Tyzio, C. Pellegrino, Y. Ben-Ari, D.E. Clapham, and I. Medina The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1 Neuron 40 2003 775 784 (Pubitemid 37431037)
29. K.D. Kuppenbender, D.G. Standaert, T. Feuerstein, J.B. Penney, A.B. Young, and G.B. Landwehrmeyer Expression of NMDA receptor subunit mRNAs in neurochemically identified projection and interneurons in the human striatum J. Comp. Neurol. 419 2000 407 421 (Pubitemid 30185983)
30. T. Kutsuwada, K. Sakimura, T. Manabe, C. Takayama, N. Katakura, E. Kushiya, R. Natsume, M. Watanabe, Y. Inoue, T. Yagi, S. Aizawa, M. Arakawa, T. Takahashi, Y. Nakamura, H. Mori, and M. Mishina Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor epsilon 2 subunit mutant mice Neuron 16 1996 333 344
31. P. Legendre, and G.L. Westbrook Ifenprodil blocks N-methyl-D-aspartate receptors by a two-component mechanism Mol. Pharmacol. 40 1991 289 298
32. Y. Liu, T.P. Wong, M. Aarts, A. Rooyakkers, L. Liu, T.W. Lai, D.C. Wu, J. Lu, M. Tymianski, A.M. Craig, and Y.T. Wang NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo J. Neurosci. 27 2007 2846 2857 (Pubitemid 46438991)
33. R.C. Malenka, and M.F. Bear LTP and LTD: an embarrassment of riches Neuron 44 2004 5 21 (Pubitemid 39348827)
34. A.B. Malmberg, H. Gilbert, R.T. McCabe, and A.I. Basbaum Powerful antinociceptive effects of the cone snail venom-derived subtype-selective NMDA receptor antagonists conantokins G and T Pain 101 2003 109 116 (Pubitemid 36044658)
35. M.A. Martel, D.J. Wyllie, and G.E. Hardingham In developing hippocampal neurons, NR2B-containing N-methyl-D-aspartate receptors (NMDARs) can mediate signaling to neuronal survival and synaptic potentiation, as well as neuronal death Neuroscience 158 2009 334 343
36. G. Moddel, B. Jacobson, Z. Ying, D. Janigro, W. Bingaman, J. Gonzalez-Martinez, C. Kellinghaus, R.A. Prayson, and I.M. Najm The NMDA receptor NR2B subunit contributes to epileptogenesis in human cortical dysplasia Brain Res. 1046 2005 10 23 (Pubitemid 40775869)
37. K. Moriyoshi, M. Masu, T. Ishii, R. Shigemoto, N. Mizuno, and S. Nakanishi Molecular cloning and characterization of the rat NMDA receptor Nature 354 1991 31 37 (Pubitemid 21896774)
38. J. Nagy, and L. Laszlo Increased sensitivity to NMDA is involved in alcohol-withdrawal induced cytotoxicity observed in primary cultures of cortical neurones chronically pre-treated with ethanol Neurochem. Int. 40 2002 585 591 (Pubitemid 34246237)
39. M. Narita, M. Soma, H. Mizoguchi, L.F. Tseng, and T. Suzuki Implications of the NR2B subunit-containing NMDA receptor localized in mouse limbic forebrain in ethanol dependence Eur. J. Pharmacol. 401 2000 191 195 (Pubitemid 30488196)
40. J.E. Nash, M.P. Hill, and J.M. Brotchie Anti-Parkinsonian actions of blockade of NR2B-containing NMDA receptors in the reserpine-treated rat Exp. Neurol. 155 1999 42 48 (Pubitemid 29072603)
41. N. Offenhauser, D. Castelletti, L. Mapelli, B.E. Soppo, M.C. Regondi, P. Rossi, E. D'Angelo, C. Frassoni, A. Amadeo, A. Tocchetti, B. Pozzi, A. Disanza, D. Guarnieri, C. Betsholtz, G. Scita, U. Heberlein, and P.P. Di Fiore Increased ethanol resistance and consumption in Eps8 knockout mice correlates with altered actin dynamics Cell 127 2006 213 226 (Pubitemid 44466639)
42. J.W. Olney, J.W. Newcomer, and N.B. Farber NMDA receptor hypofunction model of schizophrenia J. Psychiatr. Res. 33 1999 523 533
43. G.C. Palmer Neuroprotection by NMDA receptor antagonists in a variety of neuropathologies Curr. Drug. Targets. 2 2001 241 271 (Pubitemid 32821469)
44. P. Paoletti, and J. Neyton NMDA receptor subunits: function and pharmacology Curr. Opin. Pharmacol. 7 2007 39 47 (Pubitemid 46238036)
45. R. Pawlak, J.P. Melchor, T. Matys, A.E. Skrzypiec, and S. Strickland Ethanol-withdrawal seizures are controlled by tissue plasminogen activator via modulation of NR2B-containing NMDA receptors Proc. Natl. Acad. Sci. U S A 102 2005 443 448 (Pubitemid 40116786)
46. M. Prorok, and F.J. Castellino The molecular basis of conantokin antagonism of NMDA receptor function Curr. Drug. Targets. 8 2007 633 642 (Pubitemid 46785061)
47. M. Prorok, S.E. Warder, T. Blandl, and F.J. Castellino Calcium binding properties of synthetic γ-carboxyglutamic acid containing marine cone snail "sleeper" peptides, conantokin-G and conantokin-T Biochemistry 35 1996 16528 16534
48. K. Prybylowski, K. Chang, N. Sans, L. Kan, S. Vicini, and R.J. Wenthold The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2 Neuron 47 2005 845 857 (Pubitemid 41266951)
49. N. Rebola, B.N. Srikumar, and C. Mulle Activity-dependent synaptic plasticity of NMDA receptors J. Physiol. 588 2010 93 99
50. K. Sakimura, T. Kutsuwada, I. Ito, T. Manabe, C. Takayama, E. Kushiya, T. Yagi, S. Aizawa, Y. Inoue, H. Sugiyama, and M. Mishina Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit Nature 373 1995 151 155
51. N. Sans, R.S. Petralia, Y.X. Wang, J. Blahos, J.W. Hell, and R.J. Wenthold A developmental change in NMDA receptor-associated proteins at hippocampal synapses J. Neurosci. 20 2000 1260 1271 (Pubitemid 30220482)
52. P. Skolnick, K. Boje, R. Miller, M. Pennington, and M.-L. Maccecchini Noncompetitive inhibition of N-methyl-D-aspartate by conantokin-G: evidence for an allosteric interaction at polyamine sites J. Neurochem. 59 1992 1516 1521
53. R.I. Stanika, N.B. Pivovarova, C.A. Brantner, C.A. Watts, C. Winters, and S.B. Andrews Coupling diverse routes of calcium entry to mitochondrial dysfunction and glutamate excitotoxicity Proc. Natl. Acad. Sci. U S A 106 2009 9854 9859
54. G. Stocca, and S. Vicini Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons J. Physiol. 507 1998 13 24 (Pubitemid 28102672)
55. A.K. Stout, H.M. Raphael, B.I. Kanterewicz, E. Klann, and I.J. Reynolds Glutamate-induced neuron death requires mitochondrial calcium uptake Nat. vNeurosci. 1 1998 366 373
56. P.H. Tan, L.C. Yang, H.C. Shih, K.C. Lan, and J.T. Cheng Gene knockdown with intrathecal siRNA of NMDA receptor NR2B subunit reduces formalin-induced nociception in the rat Gene. Ther. 12 2005 59 66
57. C.G. Thomas, A.J. Miller, and G.L. Westbrook Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons J. Neurophysiol. 95 2006 1727 1734
58. K.R. Tovar, and G.L. Westbrook The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro J. Neurosci. 19 1999 4180 4188 (Pubitemid 29222289)
59. M.H. Ulbrich, and E.Y. Isacoff Rules of engagement for NMDA receptor subunits Proc. Natl. Acad. Sci. U S A 105 2008 14163 14168
60. M. Verhage, A.S. Maia, J.J. Plomp, A.B. Brussaard, J.H. Heeroma, H. Vermeer, R.F. Toonen, R.E. Hammer, T.K. van den Berg, M. Missler, H.J. Geuze, and T.C. Sudhof Synaptic assembly of the brain in the absence of neurotransmitter secretion Science 287 2000 864 869 (Pubitemid 30084331)
61. F. Wei, G.D. Wang, G.A. Kerchner, S.J. Kim, H.M. Xu, Z.F. Chen, and M. Zhuo Genetic enhancement of inflammatory pain by forebrain NR2B overexpression Nat. Neurosci. 4 2001 164 169 (Pubitemid 32125261)
62. J. Wei, M. Dong, C. Xiao, F. Jiang, F.J. Castellino, M. Prorok, and Q. Dai Conantokins and variants derived from cone snail venom inhibit naloxone-induced withdrawal jumping in morphine-dependent mice Neurosci. Lett. 405 2006 137 141 (Pubitemid 44142830)
63. R.J. White, and I.J. Reynolds Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure J. Neurosci. 16 1996 5688 5697 (Pubitemid 26293392)
64. A.J. Williams, J.R. Dave, J.B. Phillips, Y. Lin, R.T. McCabe, and F.C. Tortella Neuroprotective efficacy and therapeutic window of the high-affinity N-methyl-D-aspartate antagonist conantokin-G: in vitro (primary cerebellar neurons) and in vivo (rat model of transient focal brain ischemia) studies J. Pharmacol. Exp. Ther. 294 2000 378 386 (Pubitemid 30434711)
65. A.J. Williams, G. Ling, R. Berti, J.R. Moffett, C. Yao, X.M. Lu, J.R. Dave, and F.C. Tortella Treatment with the snail peptide CGX-1007 reduces DNA damage and alters gene expression of c-fos and bcl-2 following focal ischemic brain injury in rats Exp. Brain Res. 153 2003 16 26 (Pubitemid 37363645)
66. B. Wittekindt, S. Malany, R. Schemm, L. Otvos, M.L. Maccecchini, B. Laube, and H. Betz Point mutations identify the glutamate binding pocket of the N-methyl-D-aspartate receptor as major site of Conantokin-G inhibition Neuropharmacology 41 2001 753 761 (Pubitemid 32972193)
67. M. Wyszynski, J. Lin, A. Rao, E. Nigh, A.H. Beggs, A.M. Craig, and M. Sheng Competitive binding of alpha-actinin and calmodulin to the NMDA receptor Nature 385 1997 439 442 (Pubitemid 27065929)
68. S.J. Zhang, M.N. Steijaert, D. Lau, G. Schutz, C. Delucinge-Vivier, P. Descombes, and H. Bading Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death Neuron 53 2007 549 562 (Pubitemid 46216756)