Tissue plasminogen activator inhibits NMDA-receptor-mediated increases in calcium levels in cultured hippocampal neurons

Frontiers in Cellular Neuroscience

Volumn 9, Issue OCT, 2015, Pages

  Robinson, Samuel D ^a,c   Lee, Tet Woo ^a,d   Christie, David L ^a,b   Birch, Nigel P ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b Universities of Auckland and Otago   (New Zealand)

^c UNIVERSITY OF UTAH   (United States)

^d UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Calcium signaling; Hippocampal neurons; NMDA receptor; Synapse; Tissue plasminogen activator

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; ALPHA 2 ANTIPLASMIN; CALCIUM; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIMODIPINE; PLASMIN; POTASSIUM CHANNEL BLOCKING AGENT; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; NERVE CELL; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; RAT;

EID: 84944451091     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00404     Document Type: Article

References (64)

1. Bading, H., Ginty, D. D., and Greenberg, M. E. (1993). Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181-186. doi: 10.1126/science.8097060
2. Banker, G. A., and Cowan, W. M. (1977). Rat hippocampal neurons in dispersed cell culture. Brain Res. 126, 397-442. doi: 10.1016/0006-8993(77)90594-7
3. Baranes, D., Lederfein, D., Huang, Y. Y., Chen, M., Bailey, C. H., and Kandel, E. R. (1998). Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron. 21, 813-825. doi: 10.1016/s0896-6273(00)80597-8
4. Bard, L., and Groc, L. (2011). Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor. Mol. Cell. Neurosci. 48, 298-307. doi: 10.1016/j.mcn.2011.05.009
5. Barnes, P., and Thomas, K. L. (2008). Proteolysis of proBDNF is a key regulator in the formation of memory. PLoS One 3:e3248. doi: 10.1371/journal.pone.0003248
6. Baron, A., Montagne, A., Cassé, F., Launay, S., Maubert, E., Ali, C., et al. (2010). NR2D-containing NMDA receptors mediate tissue plasminogen activator-promoted neuronal excitotoxicity. Cell Death Differ. 17, 860-871. doi: 10.1038/cdd.2009.172
7. Bates, D. Maechler, M., and Bolker, B., and Walker, S. (2013). lme4: Linear mixed- effects models using Eigen and S4. R package version 1.1-7.
8. Benchenane, K., Castel, H., Boulouard, M., Bluthé, R., Fernandez-Monreal, M., Roussel, B. D., et al. (2007). Anti-NR1 N-terminal-domain vaccination unmasks the crucial action of tPA on NMDA-receptor-mediated toxicity and spatial memory. J. Cell Sci. 120, 578-585. doi: 10.1242/jcs.03354
9. Borges, V. M., Lee, T. W., Christie, D. L., and Birch, N. P. (2010). Neuroserpin regulates the density of dendritic protrusions and dendritic spine shape in cultured hippocampal neurons. J. Neurosci. Res. 88, 2610-2617. doi: 10.1002/jnr.22428
10. Bukhari, N., Torres, L., Robinson, J. K., and Tsirka, S. E. (2011). Axonal regrowth after spinal cord injury via chondroitinase and the tissue plasminogen activator (tPA)/plasmin system. J. Neurosci. 31, 14931-14943. doi: 10.1523/jneurosci.3339-11.2011
11. Calabresi, P., Napolitano, M., Centonze, D., Marfia, G. A., Gubellini, P., Teule, M. A., et al. (2000). Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur. J. Neurosci. 12, 1002-1012. doi: 10.1046/j.1460-9568.2000.00991.x
12. Cassé, F., Bardou, I., Danglot, L., Briens, A., Montagne, A., Parcq, J., et al. (2012). Glutamate controls tPA recycling by astrocytes, which in turn influences glutamatergic signals. J. Neurosci. 32, 5186-5199. doi: 10.1523/jneurosci.5296-11.2012
13. Centonze, D., Napolitano, M., Saulle, E., Gubellini, P., Picconi, B., Martorana, A., et al. (2002). Tissue plasminogen activator is required for corticostriatal long-term potentiation. Eur. J. Neurosci. 16, 713-721. doi: 10.1046/j.1460-9568.2002.02106.x
14. Cesarman-Maus, G., and Hajjar, K. A. (2005). Molecular mechanisms of fibrinolysis. Br. J. Haematol. 129, 307-321. doi: 10.1111/j.1365-2141.2005.05444.x
15. Fernández-Monreal, M., López-Atalaya, J. P., Benchenane, K., Cacquevel, M., Dulin, F., Le Caer, J.-P., et al. (2004a). 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. doi: 10.1074/jbc.m407069200
16. Fernández-Monreal, M., López-Atalaya, J. P., Benchenane, K., Léveillé, F., Cacquevel, M., Plawinski, L., et al. (2004b). Is tissue-type plasminogen activator a neuromodulator? Mol. Cell. Neurosci. 25, 594-601. doi: 10.1016/j.mcn.2003.11.002
17. Frey, U., Müller, M., and Kuhl, D. (1996). A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J. Neurosci. 16, 2057-2063.
18. Friedman, G. C., and Seeds, N. W. (1994). Tissue plasminogen activator expression in the embryonic nervous system. Brain Res. Dev. Brain Res. 81, 41-49. doi: 10.1016/0165-3806(94)90066-3
19. Hardingham, G. E., Arnold, F. J., and Bading, H. (2001a). A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat. Neurosci. 4, 565-566. doi: 10.1038/88380
20. Hardingham, G. E., Arnold, F. J., and Bading, H. (2001b). Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4, 261-267. doi: 10.1038/85109
21. Hardingham, G. E., Fukunaga, Y., and Bading, H. (2002). Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405-414. doi: 10.1038/nn835
22. Højsgaard, U. (2014). pbkrtest: Parametric bootstrap and Kenward Roger based methods for mixed model comparison.
23. Huang, Y. Y., Bach, M. E., Lipp, H. P., Zhuo, M., Wolfer, D. P., Hawkins, R. D., et al. (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. doi: 10.1073/pnas.93.16.8699
24. Jensen, F. E., and Wang, C. (1996). Hypoxia-induced hyperexcitability in vivo and in vitro in the immature hippocampus. Epilepsy Res. 26, 131-140. doi: 10.1016/s0920-1211(96)00049-6
25. Jullienne, A., Montagne, A., Orset, C., Lesept, F., Jane, D. E., Monaghan, D. T., et al. (2011). Selective inhibition of GluN2D-containing N-methyl-D-aspartate receptors prevents tissue plasminogen activator-promoted neurotoxicity both in vitro and in vivo. Mol. Neurodegener. 6:68. doi: 10.1186/1750-1326-6-68
26. Kvajo, M., Albrecht, H., Meins, M., Hengst, U., Troncoso, E., Lefort, S., et al. (2004). Regulation of brain proteolytic activity is necessary for the in vivo function of NMDA receptors. J. Neurosci. 24, 9734-9743. doi: 10.1523/jneurosci.3306-04.2004
27. Lau, C. G., and Zukin, R. S. (2007). NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci. 8, 413-426.doi: 10.1038/nrn2153
28. Lazic, S. E. (2010). The problem of pseudoreplication in neuroscientific studies: is it affecting your analysis? BMC Neurosci. 11:5. doi: 10.1186/1471-2202-11-5
29. Lee, T. W., Tumanov, S., Villas-Bôas, S. G., Montgomery, J. M., and Birch, N. P. (2015). Chemicals eluting from disposable plastic syringes and syringe filters alter neurite growth, axogenesis and the microtubule cytoskeleton in cultured hippocampal neurons. J. Neurochem. 133, 53-65. doi: 10.1111/jnc.13009
30. Lenth, R. V. (2013). lsmeans: least-squares means. R package version 1.0605
31. th Edn. Cary, NC: SAS Institute.
32. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., et al. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024. doi: 10.1126/science.1096615
33. Lochner, J. E., Honigman, L. S., Grant, W. F., Gessford, S. K., Hansen, A. B., Silverman, M. A., et al. (2006). Activity-dependent release of tissue plasminogen activator from the dendritic spines of hippocampal neurons revealed by live-cell imaging. J. Neurobiol. 66, 564-577. doi: 10.1002/neu.20250
34. Macrez, R., Bezin, L., Le Mauff, B., Ali, C., and 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. doi: 10.1161/strokeaha.110.592360
35. Madani, R., Hulo, S., Toni, N., Madani, H., Steimer, T., Muller, D., et al. (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. doi: 10.1093/emboj/18.11.3007
36. Mannaioni, G., Orr, A. G., Hamill, C. E., Yuan, H., Pedone, K. H., McCoy, K. L., et al. (2008). Plasmin potentiates synaptic N-methyl-D-aspartate receptor function in hippocampal neurons through activation of protease- activated receptor-1. J. Biol. Chem. 283, 20600-20611. doi: 10.1074/jbc.m803015200
37. Martin, A. M., Kuhlmann, C., Trossbach, S., Jaeger, S., Waldron, E., Roebroek, A., et al. (2008). The functional role of the second NPXY motif of the LRP1 beta-chain in tissue-type plasminogen activator-mediated activation of N-methyl-D-aspartate receptors. J. Biol. Chem. 283, 12004-12013. doi: 10.1074/jbc.m707607200
38. Mataga, N., Mizuguchi, Y., and Hensch, T. (2004). Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron. 44, 1031-1041. doi: 10.1016/j.neuron.2004.11.028
39. Matys, T., and Strickland, S. (2003). Tissue plasminogen activator and NMDA receptor cleavage. Nat. Med. 9, 371-373. doi: 10.1038/nm0403-371
40. Neuhoff, H., Roeper, J., and Schweizer, M. (1999). Activity-dependent formation of perforated synapses in cultured hippocampal neurons. Eur. J. Neurosci. 11, 4241-4250. doi: 10.1046/j.1460-9568.1999.00856.x
41. Ng, K.-S., Leung, H.-W., Wong, P. T.-H., and Low, C.-M. (2012). Cleavage of NR2B N-terminus of N-methyl-D-aspartate (NMDA) receptor by tissue plasminogen activator: identification of the cleavage site and characterization of ifenprodil and glycine affinities on truncated NMDA receptor. J. Biol. Chem. 287, 25520-25529. doi: 10.1074/jbc.m112.374397
42. Nicole, O., Docagne, F., Ali, C., Margaill, I., Carmeliet, P., MacKenzie, E. T., et al. (2001). The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med. 7, 59-64. doi: 10.1038/83358
43. Oh, H.-S., Kwon, O. W., Chung, I., Lee, S. C., Koh, H. J., Lee, S.-H., et al. (2005). Retinal toxicity of commercial tissue plasminogen activator is mediated by the induction of nitric oxide in the mouse retinal primary cells. Curr. Eye Res. 30, 291-297. doi: 10.1080/02713680590923267
44. Pang, P. T., Teng, H. K., Zaitsev, E., Woo, N. T., Sakata, K., Zhen, S., et al. (2004). Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487-491. doi: 10.1126/science.1100135
45. Paoletti, P. (2011). Molecular basis of NMDA receptor functional diversity. Eur. J. Neurosci. 33, 1351-1365. doi: 10.1111/j.1460-9568.2011.07628.x
46. Parcq, J., Bertrand, T., Montagne, A., Baron, A. F., Macrez, R., Billard, J. M., et al. (2012). Unveiling an exceptional zymogen: the single-chain form of tPA is a selective activator of NMDA receptor-dependent signaling and neurotoxicity. Cell Death Differ. 19, 1983-1991. doi: 10.1038/cdd.2012.86
47. Pawlak, R., Rao, B. S. S., Melchor, J. P., Chattarji, S., McEwen, B., and Strickland, S. (2005). Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc. Natl. Acad. Sci. U S A 102, 18201-18206. doi: 10.1073/pnas.0509232102
48. Pawlak, R., and Strickland, S. (2002). Tissue plasminogen activator and seizures: a clot-buster’s secret life. J. Clin. Invest. 109, 1529-1531. doi: 10.1172/jci200215961
49. Rajapakse, S., Ogiwara, K., Takano, N., Moriyama, A., and Takahashi, T. (2005). Biochemical characterization of human kallikrein 8 and its possible involvement in the degradation of extracellular matrix proteins. FEBS Lett. 579, 6879-6884. doi: 10.1016/j.febslet.2005.11.039
50. Rao, V. R., and Finkbeiner, S. (2007). NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci. 30, 284-291. doi: 10.1016/j.tins.2007.03.012
51. R Development Core Team. (2013). R: a language and environment for statistical computing. R. Foundation. for Statistical Computing, Vienna, Austria. Retrieved 4 January, 2014.
52. Reddrop, C., Moldrich, R. X., Beart, P. M., Farso, M., Liberatore, G. T., Howells, D. W., et al. (2005). Vampire bat salivary plasminogen activator (desmoteplase) inhibits tissue-type plasminogen activator-induced potentiation of excitotoxic injury. Stroke 36, 1241-1246. doi: 10.1161/01.str.0000166050.84056.48
53. Rijken, D. C., Hoylaerts, M., and Collen, D. (1982). Fibrinolytic properties of one-chain and two-chain human extrinsic (tissue-type) plasminogen activator. J. Biol. Chem. 257, 2920-2925.
54. Ruxton, G. D., and Beauchamp, G. (2008). Time for some a priori thinking about post hoc testing. Behav. Ecol. 19, 690-693. doi: 10.1093/beheco/arn020
55. Samson, A. L., Nevin, S. T., Croucher, D., Niego, B., Daniel, P. B., Weiss, T. W., et al. (2008a). Tissue-type plasminogen activator requires a co-receptor to enhance NMDA receptor function. J. Neurochem. 107, 1091-1101. doi: 10.1111/j.1471-4159.2008.05687.x
56. Samson, A. L., Nevin, S. T., and Medcalf, R. L. (2008b). Low molecular weight contaminants in commercial preparations of plasmin and t-PA activate neurons. J. Thromb. Haemost. 6, 2218-2220. doi: 10.1111/j.1538-7836.2008.03174.x
57. Sappino, A. P., Madani, R., Huarte, J., Belin, D., Kiss, J. Z., Wohlwend, A., et al. (1993). Extracellular proteolysis in the adult murine brain. J. Clin. Invest. 92, 679-685. doi: 10.1172/jci116637
58. Soriano, F. X., Papadia, S., Hofmann, F., Hardingham, N. R., Bading, H., and Hardingham, G. E. (2006). Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J. Neurosci. 26, 4509-4518. doi: 10.1523/jneurosci.0455-06.2006
59. Teesalu, T., Kulla, A., Simisker, A., Sirén, V., Lawrence, D. A., Asser, T., et al. (2004). Tissue plasminogen activator and neuroserpin are widely expressed in the human central nervous system. Thromb. Haemost. 92, 358-368. doi: 10.1160/th02-12-0310
60. Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., et al. (2010). Glutamate receptor ion channels: structure, regulation and function. Pharmacol. Rev. 62, 405-496. doi: 10.1124/pr.109.002451
61. Wang, X., and Gruenstein, E. I. (1997). Mechanism of synchronized Ca2+ oscillations in cortical neurons. Brain Res. 767, 239-249. doi: 10.1016/s0006-8993(97)00585-4
62. Ware, J. H., Dibenedetto, A. J., and Pittman, R. N. (1995). Localization of tissue plasminogen activator mRNA in adult rat brain. Brain Res. Bull. 37, 275-281. doi: 10.1016/0361-9230(95)00008-3
63. Wu, Y. P., Siao, C. J., Lu, W., Sung, T. C., Frohman, M. A., Milev, P., et al. (2000). The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J. Cell Biol. 148, 1295-1304. doi: 10.1083/jcb.148.6.1295
64. Zhuo, M., Holtzman, D. M., Li, Y., Osaka, H., DeMaro, J., Jacquin, M., et al. (2000). Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J. Neurosci. 20, 542-549