GluN2D subunit-containing NMDA receptors control tissue plasminogen activator-mediated spatial memory

Journal of Neuroscience

Volumn 32, Issue 37, 2012, Pages 12726-12734

  Obiang, Pauline ^a   Macrez, Richard ^a,b   Jullienne, Amandine ^a   Bertrand, Thomas ^a   Lesept, Flavie ^a   Ali, Carine ^a   Maubert, Eric ^a   Vivien, Denis ^a   Agin, Véronique ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b CAEN UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; TISSUE PLASMINOGEN ACTIVATOR;

ACTIVE IMMUNIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; COGNITION; CONTROLLED STUDY; EMBRYO; EMOTIONALITY; FEAR; IMMUNOBLOTTING; LOCOMOTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; RECOGNITION; SPATIAL MEMORY; TASK PERFORMANCE; TRAINING; VIDEO MICROSCOPY;

ANIMALS; GLUTAMIC ACID; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; SPACE PERCEPTION; TISSUE PLASMINOGEN ACTIVATOR;

EID: 84866236673     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6202-11.2012     Document Type: Article

References (48)

1. Bardgett ME, Boeckman R, Krochmal D, Fernando H, Ahrens R, Csernansky JG (2003) NMDA receptor blockade and hippocampal neuronal loss impair fear conditioning and position habit reversal in C57Bl/6 mice. Brain Res Bull 60:131-142.
2. Baron A, Montagne A, Cassé F, Launay S, Maubert E, Ali C, Vivien D (2010) NR2D-containing NMDA receptors mediate tissue plasminogen activatorpromoted neuronal excitotoxicity. Cell Death Differ 17:860-871.
3. Benchenane K, Castel H, Boulouard M, Bluthé R, Fernandez-Monreal M, Roussel BD, Lopez-Atalaya JP, Butt-Gueulle S, Agin V, Maubert E, Dantzer R, Touzani O, Dauphin F, Vivien D, Ali C (2007) Anti-NR1 N-terminal-domain vaccination unmasks the crucial action of t PA on NMDA-receptor-mediated toxicity and spatial memory. J Cell Sci 120:578-585.
4. Calabresi P, Napolitano M, Centonze D, Marfia GA, Gubellini P, Teule MA, Berretta N, Bernardi G, Frati L, Tolu M, Gulino A (2000) Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur J Neurosci 12:1002-1012.
5. Chen ZL, Strickland S (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91:917-925.
6. Collen D, Lijnen HR (1991) Basic and clinical aspects of fibrinolysis and thrombolysis. Blood 78:3114-3124.
7. Correa F, Gauberti M, Parcq J, Macrez R, Hommet Y, Obiang P, Hernangó-mez M, Montagne A, Liot G, Guaza C, Maubert E, Ali C, Vivien D, Docagne F (2011) Tissue plasminogen activator prevents white matter damage following stroke. J Exp Med 208:1229-1242.
8. Costa BM, Feng B, Tsintsadze TS, Morley RM, Irvine MW, Tsintsadze V, Lozovaya NA, Jane DE, Monaghan DT (2009) N-methyl-D-aspartate (NMDA) receptor NR2 subunit selectivity of a series of novel piperazine-2,3-dicarboxylate derivatives: preferential blockade of extrasynaptic NMDA receptors in the rat hippocampal CA3-CA1 synapse. J Pharmacol Exp Ther 331:618-626.
9. Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
10. Dellu F, Contarino A, Simon H, Koob GF, Gold LH (2000) Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiol Learn Mem 73:31-48.
11. Fernández-Monreal M, López-Atalaya JP, Benchenane K, Cacquevel M, Dulin F, Le Caer JP, Rossier J, Jarrige AC, Mackenzie ET, Colloc'h N, Ali C, Vivien D (2004) Arginine 260 of the amino-terminal domain of NR1 subunit is critical for tissue-type plasminogen activator-mediated enhancement of N-methyl-D-aspartate receptor signaling. J Biol Chem 279:50850-50856.
12. Gao C, Gill MB, Tronson NC, Guedea AL, Guzmán YF, Huh KH, Corcoran KA, Swanson GT, Radulovic J (2010) Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation. Hippocampus 20:1072-1082.
13. Gveric D, Hanemaaijer R, Newcombe J, van Lent NA, Sier CF, Cuzner ML (2001) Plasminogen activators in multiple sclerosis lesions: implications for the inflammatory response and axonal damage. Brain 124:1978-1988.
14. Hagino Y, Kasai S, Han W, Yamamoto H, Nabeshima T, Mishina M, Ikeda K (2010) Essential role of NMDA receptor channel ε4 subunit (Glu N2D) in the effects of phencyclidine, but not methamphetamine. PLo S One 5:e13722.
15. Hu K, Yang J, Tanaka S, Gonias SL, Mars WM, Liu Y (2006) Tissue-type plasminogen activator acts as a cytokine that triggers intracellular signal transduction and induces matrix metalloproteinase-9 gene expression. J Biol Chem 281:2120-2127.
16. Huang YY, Bach ME, Lipp HP, Zhuo M, Wolfer DP, Hawkins RD, Schoonjans L, Kandel ER, Godfraind JM, Mulligan R, Collen D, Carmeliet P (1996) Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc Natl Acad Sci U S A 93:8699-8704.
17. Ikeda K, Araki K, Takayama C, Inoue Y, Yagi T, Aizawa S, Mishina M (1995) Reduced spontaneous activity of mice defective in the epsilon 4 subunit of the NMDA. Brain Res Mol Brain Res 33:61-71.
18. Jullienne A, Montagne A, Orset C, Lesept F, Jane DE, Monaghan DT, Maubert E, Vivien D, Ali C (2011) Selective inhibition of Glu N2D-containing N-methyl-D-aspartate receptors prevents tissue plasminogen activatorpromoted neurotoxicity both in vitro and in vivo. Mol Neurodegener 6:68.
19. Kew JN, Kemp JA (2005) Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl) 179:4-29. [Erratum (2005) 182:320]
20. Kvajo M, Albrecht H, Meins M, Hengst U, Troncoso E, Lefort S, Kiss JZ, Petersen CC, Monard D (2004) Regulation of brain proteolytic activity is necessary for the in vivo function of NMDA receptors. J Neurosci 24:9734-9743.
21. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, Eskin A (2002) Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5:155-161.
22. Liot G, Roussel BD, Lebeurrier N, Benchenane K, López-Atalaya JP, Vivien D, Ali C (2006) Tissue-type plasminogen activator rescues neurones from serum deprivation-induced apoptosis through a mechanism independent of its proteolytic activity. J Neurochem 98:1458-1464.
23. Liu D, Cheng T, Guo H, Fernández JA, Griffin JH, Song X, Zlokovic BV (2004a) Tissue plasminogen activator neurovascular toxicity is controlled by activated protein C. Nat Med 10:1379-1383.
24. Liu IY, Lyons WE, Mamounas LA, Thompson RF (2004b) Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning. J Neurosci 24:7958-7963.
25. Lu W, Bhasin M, Tsirka SE (2002) Involvement of tissue plasminogen activator in onset and effector phases of experimental allergic encephalomyelitis. J Neurosci 22:10781-10789.
26. Macrez R, Bezin L, Le Mauff B, Ali C, Vivien D (2010) Functional occurrence of the interaction of tissue plasminogen activator with the NR1 Subunit of N-methyl-D-aspartate receptors during stroke. Stroke 41:2950-2955.
27. Macrez R, Obiang P, Gauberti M, Roussel B, Baron A, Parcq J, Cassé F, Hommet Y, Orset C, Agin V, Bezin L, Berrocoso TG, Petersen KU, Montaner J, Maubert E, Vivien D, Ali C (2011) Antibodies preventing the interaction of tissue-type plasminogen activator with N-methyl-Daspartate receptors reduce stroke damages and extend the therapeutic window of thrombolysis. Stroke 42:2315-2322.
28. Madani R, Hulo S, Toni N, Madani H, Steimer T, Muller D, Vassalli JD (1999) Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J 18:3007-3012.
29. Mataga N, Nagai N, Hensch TK (2002) Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci U S A 99:7717-7721.
30. Matys T, Pawlak R, Matys E, Pavlides C, McEwen BS, Strickland S (2004) Tissue plasminogen activator promotes the effects of corticotropinreleasing factor on the amygdala and anxiety-like behavior. Proc Natl Acad Sci U S A 101:16345-16350.
31. Miyamoto Y, Yamada K, Noda Y, Mori H, Mishina M, Nabeshima T (2002) Lower sensitivity to stress and altered monoaminergic neuronal function in mice lacking the NMDA receptor epsilon 4 subunit. J Neurosci 22:2335-2342.
32. Nassar T, Yarovoi S, Fanne RA, Akkawi S, Jammal M, Allen TC, Idell S, Cines DB, Higazi AA (2010) Regulation of airway contractility by plasminogen activators through N-methyl-D-aspartate receptor-1. Am J Respir Cell Mol Biol 43:703-711.
33. Nicole O, Docagne F, Ali C, Margaill I, Carmeliet P, Mac Kenzie ET, Vivien D, Buisson A (2001) The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med 7:59-64.
34. Obiang P, Maubert E, Bardou I, Nicole O, Launay S, Bezin L, Vivien D, Agin V (2011) Enriched housing reverses age-associated impairment of cognitive functions and t PA-dependent maturation of BDNF. Neurobiol Learn Mem 96:121-129.
35. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of pro BDNF by t PA/plasmin is essential for long-term hippocampal plasticity. Science 306:487-491.
36. Pawlak R, Nagai N, Urano T, Napiorkowska-Pawlak D, Ihara H, Takada Y, Collen D, Takada A (2002) Rapid, specific and active site-catalyzed effect of tissue-plasminogen activator on hippocampus-dependent learning in mice. Neuroscience 113:995-1001.
37. Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S (2003) Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6:168-174.
38. Pawlak R, Melchor JP, Matys T, Skrzypiec AE, Strickland S (2005) Ethanolwithdrawal seizures are controlled by tissue plasminogen activator via modulation of NR2B-containing NMDA receptors. Proc Natl Acad Sci U S A 102:443-448.
39. Plow EF, Herren T, Redlitz A, Miles LA, Hoover-Plow JL (1995) The cell biology of the plasminogen system. FASEB J 9:939-945.
40. Samson AL, Nevin ST, Croucher D, Niego B, Daniel PB, Weiss TW, Moreno E, Monard D, Lawrence DA, Medcalf RL (2008) Tissue-type plasminogen activator requires a co-receptor to enhance NMDAreceptor function. J Neurochem 107:1091-1101.
41. Seeds NW, Williams BL, Bickford PC (1995) Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270:1992-1994.
42. Seeds NW, Basham ME, Ferguson JE (2003) Absence of tissue plasminogen activator gene or activity impairs mouse cerebellar motor learning. J Neurosci 23:7368-7375.
43. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill.
44. Tsirka SE, Gualandris A, Amaral DG, Strickland S (1995) Excitotoxininduced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377:340-344.
45. Wang YF, Tsirka SE, Strickland S, Stieg PE, Soriano SG, Lipton SA (1998) Tissue plasminogen activator (t PA) increases neuronal damage after focal cerebral ischemia in wild-type and t PA-deficient mice. Nat Med 4:228-231.
46. Wu YP, Siao CJ, Lu W, Sung TC, Frohman MA, Milev P, Bugge TH, Degen JL, Levine JM, Margolis RU, Tsirka SE (2000) The tissue plasminogen activator (t PA)/plasmin extracellular proteolytic system regulates seizureinduced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J Cell Biol 148:1295-1304.
47. Yamada K, Nagai T, Nabeshima T (2005) Drug dependence, synaptic plasticity, and tissue plasminogen activator. J Pharmacol Sci 97:157-161.
48. Zhuo M, Holtzman DM, Li Y, Osaka H, De Maro J, Jacquin M, Bu G (2000) Role of tissue plasminogen activator receptor LRP in hippocampal longterm potentiation. J Neurosci 20:542-549.