Thrombin induces ischemic LTP (iLTP): Implications for synaptic plasticity in the acute phase of ischemic stroke

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Stein, Efrat Shavit ^a   Itsekson Hayosh, Zeev ^a   Aronovich, Anna ^b,c   Reisner, Yair ^c   Bushi, Doron ^a   Pick, Chaim G ^b   Tanne, David ^a,b   Chapman, Joab ^a,b   Vlachos, Andreas ^d   Maggio, Nicola ^a  

^a SHEBA MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN;

ANIMAL; BIOSYNTHESIS; BRAIN ISCHEMIA; GENETICS; HIPPOCAMPAL CA1 REGION; KNOCKOUT MOUSE; LONG TERM POTENTIATION; METABOLISM; MOUSE; PATHOLOGY;

ANIMALS; BRAIN ISCHEMIA; CA1 REGION, HIPPOCAMPAL; LONG-TERM POTENTIATION; MICE; MICE, KNOCKOUT; RECEPTOR, PAR-1; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; THROMBIN;

EID: 84923076510     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07912     Document Type: Article

References (48)

1. Yang, Y. & Rosenberg, G. A. Blood-brain barrier breakdown in acute and chronic cerebrovascular disease. Stroke 42, 3323-3328 (2011).
2. Baron, J. C., Yamauchi, H., Fujioka, M. & Endres, M. Selective neuronal loss in ischemic stroke and cerebrovascular disease. J Cereb Blood Flow Metab 34, 2-18 (2014).
3. Uchiyama, S. The concept of acute cerebrovascular syndrome. Front Neurol Neurosci 33, 11-18 (2014).
4. Calabresi, P., Centonze, D., Pisani,A., Cupini, L. & Bernardi, G. Synaptic plasticity in the ischaemic brain. Lancet Neurol 2, 622-629 (2003).
5. Di Filippo, M. et al. Plasticity and repair in the post-ischemic brain. Neuropharmacology 55, 353-362 (2008).
6. Crepel, V., Epsztein, J. & Ben-Ari, Y. Ischemia induces short-and long-term remodeling of synaptic activity in the hippocampus. J Cell Mol Med 7, 401-407 (2003).
7. Crepel, V., Hammond, C., Chinestra, P.,Diabira, D. & Ben-Ari, Y. A selective LTP of NMDA receptor-mediated currents induced by anoxia in CA1 hippocampal neurons. J Neurophysiol 70, 2045-2055 (1993).
8. Hsu, K. S. & Huang, C. C. Characterization of the anoxia-induced long-term synaptic potentiation in area CA1 of the rat hippocampus. Br J Pharmacol 122, 671-681 (1997).
9. Bushi, D. et al. Quantitative detection of thrombin activity in an ischemic stroke model. J Mol Neurosci 51, 844-850 (2013).
10. Chen, B. et al. Thrombin activity associated with neuronal damage during acute focal ischemia. J Neurosci 32, 7622-7631 (2012).
11. Maggio, N. et al. The anticoagulant activated protein C (aPC) promotes metaplasticity in the hippocampus through an EPCR-PAR1-S1P1 receptors dependent mechanism. Hippocampus 24, 1030-8 (2014).
12. Maggio, N. et al. Thrombin regulation of synaptic plasticity: implications for physiology and pathology. Exp Neurol 247, 595-604 (2013).
13. Festoff, B. W., Suo, Z. & Citron, B. A. Plasticity and stabilization of neuromuscular and CNS synapses: interactions between thrombin protease signaling pathways and tissue transglutaminase. International review of cytology 211, 153-177 (2001).
14. Davies, B. J., Pickard, B. S., Steel, M.,Morris, R. G. & Lathe, R. Serine proteases in rodent hippocampus. J Biol Chem 273, 23004-23011 (1998).
15. Almonte, A. G. et al. Learning and memory deficits in mice lacking protease activated receptor-1. Neurobiol Learn Mem 88, 295-304 (2007).
16. Gingrich, M. B., Junge, C. E., Lyuboslavsky, P. & Traynelis, S. F. Potentiation of NMDA receptor function by the serine protease thrombin. The Journal of neuroscience: the official journal of the Society for Neuroscience 20, 4582-4595 (2000).
17. Maggio, N., Shavit, E., Chapman, J. & Segal, M. Thrombin induces long-term potentiation of reactivity to afferent stimulation and facilitates epileptic seizures in rat hippocampal slices: toward understanding the functional consequences of cerebrovascular insults. The Journal of neuroscience: the official journal of the Society for Neuroscience 28, 732-736 (2008).
18. Chapman, J. Coagulation in inflammatory diseases of the central nervous system. Semin Thromb Hemost 39, 876-880 (2013).
19. Maggio, N. & Segal, M. Unique regulation of long term potentiation in the rat ventral hippocampus. Hippocampus 17, 10-25 (2007).
20. Maggio, N. & Segal, M. Cellular basis of a rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices. Hippocampus 22, 267-275 (2012).
21. Picconi, B. et al. NR2B subunit exerts a critical role in postischemic synaptic plasticity. Stroke 37, 1895-1901 (2006).
22. Beilin, O., Gurwitz, D., Korczyn, A. D. & Chapman, J. Quantitative measurements of mouse brain thrombin-like and thrombin inhibition activities. Neuroreport 12, 2347-2351 (2001).
23. Itzekson, Z. et al. Reversal of trauma-induced amnesia in mice by a thrombin receptor antagonist. J Mol Neurosci 53, 87-95 (2014).
24. Arcangeli, S. et al. Ischemic-LTP in striatal spiny neurons of both direct and indirect pathway requires the activation of D1-like receptors and NO/soluble guanylate cyclase/cGMP transmission. J Cereb Blood Flow Metab 33, 278-286 (2013).
25. Hauel, N. H. et al. Structure-based design of novel potent nonpeptide thrombin inhibitors. J Med Chem 45, 1757-1766 (2002).
26. Lee, C. J. et al. Astrocytic control of synaptic NMDA receptors. J Physiol 581, 1057-1081 (2007).
27. Strande, J. L. et al. SCH 79797, a selective PAR1 antagonist, limits myocardial ischemia/reperfusion injury in rat hearts. Basic Res Cardiol 102, 350-358 (2007).
28. Maggio, N. & Segal, M. Striking variations in corticosteroid modulation of longterm potentiation along the septotemporal axis of the hippocampus. JNeurosci 27, 5757-5765 (2007).
29. Chen, B., Cheng, Q., Yang, K. & Lyden, P. D. Thrombin mediates severe neurovascular injury during ischemia. Stroke 41, 2348-2352 (2010).
30. Centonze, D. et al. Tissue plasminogen activator is required for striatal postischemic synaptic potentiation. Neuroreport 13, 115-118 (2002).
31. Junge, C. E. et al. Protease-activated receptor-1 in human brain: localization and functional expression in astrocytes. Exp Neurol 188, 94-103 (2004).
32. Mandl-Weber, S., Haslinger, B. & Sitter, T. Thrombin upregulates production of plasminogen activator inhibitor type 1 in human peritoneal mesothelial cells. Perit Dial Int 19, 319-324 (1999).
33. Centonze, D. et al. Tissue plasminogen activator is required for corticostriatal long-term potentiation. Eur J Neurosci 16, 713-721 (2002).
34. Tomimatsu, Y., Idemoto, S., Moriguchi, S., Watanabe, S. & Nakanishi, H. Proteases involved in long-term potentiation. Life Sci 72, 355-361 (2002).
35. Zhuo,M. et al. Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J Neurosci 20, 542-549 (2000).
36. Baranes, D. et al. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21, 813-825 (1998).
37. Maggio, N. et al. Thrombin regulation of synaptic transmission: implications for seizure onset. Neurobiol Dis 50, 171-178 (2013).
38. Maggio, N. et al. Treating seizures and epilepsy with anticoagulants? Front Cell Neurosci 7, 19 (2013).
39. Cheng, Y. et al. Thrombin-induced cerebral hemorrhage: role of proteaseactivated receptor-1. Transl Stroke Res 5, 472-475 (2014).
40. Keep, R. F. et al. Blood-brain barrier function in intracerebral hemorrhage. Acta Neurochir Suppl 105, 73-77 (2008).
41. Gong, Y. et al. Increase in brain thrombin activity after experimental intracerebral hemorrhage. Acta Neurochir Suppl 105, 47-50 (2008).
42. Siller-Matula, J. M., Schwameis, M., Blann, A., Mannhalter, C. & Jilma, B. Thrombin as a multi-functional enzyme. Focus on in vitro and in vivo effects. Thromb Haemost 106, 1020-1033 (2011).
43. Shikamoto, Y. & Morita, T. Expression of factor X in both the rat brain and cells of the central nervous system. FEBS Lett 463, 387-389 (1999).
44. Dihanich, M., Kaser, M., Reinhard, E., Cunningham, D. & Monard, D. Prothrombin mRNA is expressed by cells of the nervous system. Neuron 6, 575-581 (1991).
45. Sokolova, E. & Reiser, G. Prothrombin/thrombin and the thrombin receptors PAR-1 and PAR-4 in the brain: localization, expression and participation in neurodegenerative diseases. Thrombosis and haemostasis 100, 576-581 (2008).
46. Almonte, A. G. et al. Protease-activated receptor-1 modulates hippocampal memory formation and synaptic plasticity. J Neurochem 124, 109-122 (2013).
47. Striggow, F. et al. The protease thrombin is an endogenous mediator of hippocampal neuroprotection against ischemia at low concentrations but causes degeneration at high concentrations. Proc Natl Acad Sci U S A 97, 2264-2269 (2000).
48. Guo, H. et al. Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3. Neuron 41, 563-572 (2004).