Chronic blockade of extrasynaptic NMDA receptors ameliorates synaptic dysfunction and pro-death signaling in Huntington disease transgenic mice

Neurobiology of Disease

Volumn 62, Issue , 2014, Pages 533-542

  Dau, Alejandro ^a   Gladding, Clare M ^a   Sepers, Marja D ^a   Raymond, Lynn A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Calcium signaling; Calpain; Extrasynaptic; GluN2B; Huntington disease; Memantine; NMDA receptor; P38; PCREB; Striatum

Indexed keywords

CALPAIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EXTRASYNAPTIC NMDA RECEPTOR; MEMANTINE; MITOGEN ACTIVATED PROTEIN KINASE P38; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUNTINGTON CHOREA; MALE; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYNAPSE;

CALCIUM SIGNALING; CALPAIN; EXTRASYNAPTIC; GLUN2B; HUNTINGTON DISEASE; MEMANTINE; NMDA RECEPTOR; P38; PCREB; STRIATUM;

ANIMALS; CALCIUM SIGNALING; CALPAIN; CORPUS STRIATUM; CREB-BINDING PROTEIN; EXCITATORY AMINO ACID ANTAGONISTS; HUNTINGTON DISEASE; MEMANTINE; MICE; MICE, TRANSGENIC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 84890027845     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.11.013     Document Type: Article

References (61)

1. Aarts M., Liu Y., Liu L., Besshoh S., Arundine M., Gurd J.W., Wang Y.-T., Salter M.W., Tymianski M. Treatment of ischemic brain damage by perturbing NMDA receptor- PSD-95 protein interactions. Science 2002, 298:846-850.
2. Aracava Y., Pereira E.F.R., Maelicke A., Albuquerque E.X. Memantine blocks α7* nicotinic acetylcholine receptors more potently than N-methyl-d-aspartate receptors in rat hippocampal neurons. J. Pharmacol. Exp. Ther. 2005, 312:1195-1205.
3. Cao J., Viholainen J.I., Dart C., Warwick H.K., Leyland M.L., Courtney M.J. The PSD95-nNOS interface: a target for inhibition of excitotoxic p38 stress-activated protein kinase activation and cell death. J. Cell Biol. 2005, 168:117-126.
4. Cepeda C., Ariano M.A., Calvert C.R., Flores-Hernández J., Chandler S.H., Leavitt B.R., Hayden M.R., Levine M.S. NMDA receptor function in mouse models of Huntington disease. J. Neurosci. Res. 2001, 66:525-539.
5. Chen N., Luo T., Wellington C., Metzler M., McCutcheon K., Hayden M.R., Raymond L.A. Subtype-specific enhancement of NMDA receptor currents by mutant huntingtin. J. Neurochem. 1999, 72:1890-1898.
6. Cowan C.M., Fan M.M.Y., Fan J., Shehadeh J., Zhang L.Y.J., Graham R.K., Hayden M.R., Raymond L.A. Polyglutamine-modulated striatal calpain activity in YAC transgenic Huntington disease mouse model: impact on NMDA receptor function and toxicity. J. Neurosci. 2008, 28:12725-12735.
7. Cui L., Jeong H., Borovecki F., Parkhurst C.N., Tanese N., Krainc D. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 2006, 127:59-69.
8. Dravid S.M., Erreger K., Yuan H., Nicholson K., Le P., Lyuboslavsky P., Almonte A., Murray E., Mosely C., Barber J., et al. Subunit-specific mechanisms and proton sensitivity of NMDA receptor channel block. J. Physiol. 2007, 581:107-128.
9. Fan M.M.Y., Fernandes H.B., Zhang L.Y.J., Hayden M.R., Raymond L.A. Altered NMDA receptor trafficking in a yeast artificial chromosome transgenic mouse model of Huntington's disease. J. Neurosci. Off. J. Soc. Neurosci. 2007, 27:3768-3779.
10. Fan J., Cowan C.M., Zhang L.Y.J., Hayden M.R., Raymond L.A. Interaction of postsynaptic density protein-95 with NMDA receptors influences excitotoxicity in the yeast artificial chromosome mouse model of Huntington's disease. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:10928-10938.
11. Fan J., Gladding C.M., Wang L., Zhang L.Y.J., Kaufman A.M., Milnerwood A.J., Raymond L.A. P38 MAPK is involved in enhanced NMDA receptor-dependent excitotoxicity in YAC transgenic mouse model of Huntington disease. Neurobiol. Dis. 2012, 45:999-1009.
12. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 2006, 116:615-622.
13. Gafni J., Ellerby L.M. Calpain activation in Huntington's disease. J. Neurosci. Off. J. Soc. Neurosci. 2002, 22:4842-4849.
14. Gafni J., Hermel E., Young J.E., Wellington C.L., Hayden M.R., Ellerby L.M. Inhibition of calpain cleavage of huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J. Biol. Chem. 2004, 279:20211-20220.
15. Gerfen C.R., Surmeier D.J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 2011, 34:441-466.
16. Ghatan S., Larner S., Kinoshita Y., Hetman M., Patel L., Xia Z., Youle R.J., Morrison R.S. p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J. Cell Biol. 2000, 150:335-347.
17. Gladding C.M., Raymond L.A. Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol. Cell. Neurosci. 2011, 48:308-320.
18. Gladding C.M., Sepers M.D., Xu J., Zhang L.Y.J., Milnerwood A.J., Lombroso P.J., Raymond L.A. Calpain and STriatal-Enriched protein tyrosine phosphatase (STEP) activation contribute to extrasynaptic NMDA receptor localization in a Huntington's disease mouse model. Hum. Mol. Genet. 2012, 21:3739-3752.
19. Goebel-Goody S.M., Davies K.D., Alvestad Linger R.M., Freund R.K., Browning M.D. Phospho-regulation of synaptic and extrasynaptic N-methyl-d-aspartate receptors in adult hippocampal slices. Neuroscience 2009, 158:1446-1459.
20. Gomez-Lazaro M., Galindo M.F., Melero-Fernandez de Mera R.M., Fernandez-Gómez F.J., Concannon C.G., Segura M.F., Comella J.X., Prehn J.H.M., Jordan J. Reactive oxygen species and p38 mitogen-activated protein kinase activate Bax to induce mitochondrial cytochrome c release and apoptosis in response to malonate. Mol. Pharmacol. 2007, 71:736-743.
21. Hansson O., Guatteo E., Mercuri N.B., Bernardi G., Li X.J., Castilho R.F., Brundin P. Resistance to NMDA toxicity correlates with appearance of nuclear inclusions, behavioural deficits and changes in calcium homeostasis in mice transgenic for exon 1 of the huntington gene. Eur. J. Neurosci. 2001, 14:1492-1504.
22. Hardingham G.E., Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 2010, 11:682-696.
23. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 2002, 5:405-414.
24. Huntington's Disease Collaborative Research Group A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993, 72:971-983.
25. Impey S., Fong A.L., Wang Y., Cardinaux J.R., Fass D.M., Obrietan K., Wayman G.A., Storm D.R., Soderling T.R., Goodman R.H. Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 2002, 34:235-244.
26. Johnson J.W., Kotermanski S.E. Mechanism of action of memantine. Curr. Opin. Pharmacol. 2006, 6:61-67.
27. Kaufman A.M., Milnerwood A.J., Sepers M.D., Coquinco A., She K., Wang L., Lee H., Craig A.M., Cynader M., Raymond L.A. Opposing roles of synaptic and extrasynaptic NMDA receptor signaling in cocultured striatal and cortical neurons. J. Neurosci. 2012, 32:3992-4003.
28. Kim Y.J., Yi Y., Sapp E., Wang Y., Cuiffo B., Kegel K.B., Qin Z.-H., Aronin N., DiFiglia M. Caspase 3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl. Acad. Sci. 2001, 98:12784-12789.
29. Kotermanski S.E., Johnson J.W. Mg2+ imparts NMDA receptor subtype selectivity to the Alzheimer's drug memantine. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:2774-2779.
30. Li L., Fan M., Icton C.D., Chen N., Leavitt B.R., Hayden M.R., Murphy T.H., Raymond L.A. Role of NR2B-type NMDA receptors in selective neurodegeneration in Huntington disease. Neurobiol. Aging 2003, 24:1113-1121.
31. Milnerwood A.J., Raymond L.A. Corticostriatal synaptic function in mouse models of Huntington's disease: early effects of huntingtin repeat length and protein load. J. Physiol. 2007, 585:817-831.
32. Milnerwood A.J., Gladding C.M., Pouladi M.A., Kaufman A.M., Hines R.M., Boyd J.D., Ko R.W.Y., Vasuta O.C., Graham R.K., Hayden M.R., et al. Early increase in extrasynaptic NMDA receptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
33. Milnerwood A.J., Kaufman A.M., Sepers M.D., Gladding C.M., Zhang L., Wang L., Fan J., Coquinco A., Qiao J.Y., Lee H., et al. Mitigation of augmented extrasynaptic NMDAR signaling and apoptosis in cortico-striatal co-cultures from Huntington's disease mice. Neurobiol. Dis. 2012, 48:40-51.
34. Okamoto S., Pouladi M.A., Talantova M., Yao D., Xia P., Ehrnhoefer D.E., Zaidi R., Clemente A., Kaul M., Graham R.K., et al. Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat. Med. 2009, 15:1407-1413.
35. Otton H.J., Lawson McLean A., Pannozzo M.A., Davies C.H., Wyllie D.J.A. Quantification of the Mg2+-induced potency shift of amantadine and memantine voltage-dependent block in human recombinant GluN1/GluN2A NMDARs. Neuropharmacology 2011, 60:388-396.
36. Pacchioni A.M., Vallone J., Worley P.F., Kalivas P.W. Neuronal pentraxins modulate cocaine-induced neuroadaptations. J. Pharmacol. Exp. Ther. 2009, 328:183-192.
37. Papadia S., Hardingham G.E. The dichotomy of NMDA receptor signaling. Neuroscientist 2007, 13:572-579.
38. Puddifoot C., Martel M.-A., Soriano F.X., Camacho A., Vidal-Puig A., Wyllie D.J.A., Hardingham G.E. PGC-1a negatively regulates extrasynaptic NMDAR activity and excitotoxicity. J. Neurosci. Off. J. Soc. Neurosci. 2012, 32:6995-7000.
39. Raina P., Santaguida P., Ismaila A., Patterson C., Cowan D., Levine M., Booker L., Oremus M. Effectiveness of cholinesterase inhibitors and memantine for treating dementia: evidence review for a clinical practice guideline. Ann. Intern. Med. 2008, 148:379-397.
40. Rammes G., Rupprecht R., Ferrari U., Zieglgänsberger W., Parsons C. The N-methyl-d-aspartate receptor channel blockers memantine, MRZ 2/579 and other amino-alkyl-cyclohexanes antagonise 5-HT3 receptor currents in cultured HEK-293 and N1E-115 cell systems in a non-competitive manner. Neurosci. Lett. 2001, 306:81-84.
41. Rammes G., Danysz W., Parsons C.G. Pharmacodynamics of memantine: an update. Curr. Neuropharmacol. 2008, 6:55-78.
42. Rosi S., Vazdarjanova A., Ramirez-Amaya V., Worley P.F., Barnes C.A., Wenk G.L. Memantine protects against LPS-induced neuroinflammation, restores behaviorally-induced gene expression and spatial learning in the rat. Neuroscience 2006, 142:1303-1315.
43. Rumbaugh G., Adams J.P., Kim J.H., Huganir R.L. SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:4344-4351.
44. Saavedra A., Giralt A., Rue L., Xifro X., Xu J., Ortega Z., Lucas J.J., Lombroso P.J., Alberch J., Perez-Navarro E. STriatal-Enriched protein tyrosine Phosphatase expression and activity in Huntington's disease - a STEP in the resistance to excitotoxicity. J. Neurosci. Off. J. Soc. Neurosci. 2011, 31:8150-8162.
45. Seeman P., Caruso C., Lasaga M. Memantine agonist action at dopamine D2High receptors. Synapse 2008, 62:149-153.
46. Slow E.J., van Raamsdonk J., Rogers D., Coleman S.H., Graham R.K., Deng Y., Oh R., Bissada N., Hossain S.M., Yang Y.-Z., et al. Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum. Mol. Genet. 2003, 12:1555-1567.
47. Sobolevsky A.I., Koshelev S.G., Khodorov B.I. Interaction of memantine and amantadine with agonist-unbound NMDA-receptor channels in acutely isolated rat hippocampal neurons. J. Physiol. 1998, 512(Pt 1):47-60.
48. Soriano F.X., Martel M.-A., Papadia S., Vaslin A., Baxter P., Rickman C., Forder J., Tymianski M., Duncan R., Aarts M., et al. Specific targeting of pro-death NMDA receptor signals with differing reliance on the NR2B PDZ ligand. J. Neurosci. Off. J. Soc. Neurosci. 2008, 28:10696-10710.
49. Starling A.J., André V.M., Cepeda C., de Lima M., Chandler S.H., Levine M.S. Alterations in N-methyl-d-aspartate receptor sensitivity and magnesium blockade occur early in development in the R6/2 mouse model of Huntington's disease. J. Neurosci. Res. 2005, 82:377-386.
50. Tovar K.R., Westbrook G.L. Mobile NMDA receptors at hippocampal synapses. Neuron 2002, 34:255-264.
51. Tzingounis A.V., Wadiche J.I. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 2007, 8:935-947.
52. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., Richardson E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 1985, 44:559-577.
53. Wu G.-Y., Deisseroth K., Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2808-2813.
54. Wu J., Shih H.-P., Vigont V., Hrdlicka L., Diggins L., Singh C., Mahoney M., Chesworth R., Shapiro G., Zimina O., et al. Neuronal store-operated calcium entry pathway as a novel therapeutic target for Huntington's disease treatment. Chem. Biol. 2011, 18:777-793.
55. Xia P., Chen H.V., Zhang D., Lipton S.A. Memantine preferentially blocks extrasynaptic over synaptic NMDA receptor currents in hippocampal autapses. J. Neurosci. Off. J. Soc. Neurosci. 2010, 30:11246-11250.
56. Xu J., Kurup P., Zhang Y., Goebel-Goody S.M., Wu P.H., Hawasli A.H., Baum M.L., Bibb J.A., Lombroso P.J. Extrasynaptic NMDA receptors couple preferentially to excitotoxicity via calpain-mediated cleavage of STEP. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:9330-9343.
57. Zeron M.M., Chen N., Moshaver A., Lee A.T., Wellington C.L., Hayden M.R., Raymond L.A. Mutant huntingtin enhances excitotoxic cell death. Mol. Cell. Neurosci. 2001, 17:41-53.
58. Zeron M.M., Hansson O., Chen N., Wellington C.L., Leavitt B.R., Brundin P., Hayden M.R., Raymond L.A. Increased sensitivity to N-methyl-d-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 2002, 33:849-860.
59. Zeron M.M., Fernandes H.B., Krebs C., Shehadeh J., Wellington C.L., Leavitt B.R., Baimbridge K.G., Hayden M.R., Raymond L.A. Potentiation of NMDA receptor-mediated excitotoxicity linked with intrinsic apoptotic pathway in YAC transgenic mouse model of Huntington's disease. Mol. Cell. Neurosci. 2004, 25:469-479.
60. Zhang H., Li Q., Graham R.K., Slow E., Hayden M.R., Bezprozvanny I. Full length mutant huntingtin is required for altered Ca2+ signaling and apoptosis of striatal neurons in the YAC mouse model of Huntington's disease. Neurobiol. Dis. 2008, 31:80-88.
61. Zuccato C., Valenza M., Cattaneo E. Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 2010, 90:905-981.