Reversal of trauma-induced amnesia in mice by a thrombin receptor antagonist

Journal of Molecular Neuroscience

Volumn 53, Issue 1, 2014, Pages 87-95

  Itzekson, Zeev ^a,b   Maggio, Nicola ^b   Milman, Anat ^a,c   Shavit, Efrat ^a,b   Pick, Chaim G ^a   Chapman, Joab ^a,b  

^a TEL AVIV UNIVERSITY   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

^c TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

Author keywords

Amnesia; Hippocampus; Long term potentiation; mTBI; PAR1; Thrombin

Indexed keywords

1 AMINO 3 CYCLOPROPYLAMINO 7 (4 ISOPROPYLBENZYL) 7H PYRROLO[3,2 F]QUINAZOLINE; THROMBIN; N3-CYCLOPROPYL-7-((4-(1-METHYLETHYL)PHENYL)METHYL)-7H-PYRROLO(3, 2-F)QUINAZOLINE-1,3-DIAMINE; PROTEINASE ACTIVATED RECEPTOR 1; PYRROLE DERIVATIVE; QUINAZOLINE DERIVATIVE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN HOMOGENATE; BRAIN SLICE; CONTROLLED STUDY; COORDINATION; HIPPOCAMPUS; LOCOMOTION; LONG TERM POTENTIATION; MALE; MINIMAL TRAUMATIC BRAIN INJURY; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; PSYCHOLOGIC ASSESSMENT; RECOGNITION; TRAUMATIC BRAIN INJURY; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN INJURIES; COMPLICATION; DRUG EFFECTS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALIA; MUS;

AMNESIA; ANIMALS; BRAIN INJURIES; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE; MICE, INBRED ICR; PYRROLES; QUINAZOLINES; RECEPTOR, PAR-1; THROMBIN;

EID: 84899912346     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-013-0200-8     Document Type: Article

References (44)

1. Aronovich R, Gurwitz D, Kloog Y, Chapman J (2005) Antiphospholipid antibodies, thrombin and LPS activate brain endothelial cells and Ras-dependent pathways through distinct mechanisms. Immunobiology 210:781-788 (Pubitemid 41683863)
2. Beilin O, Gurwitz D, Korczyn AD, Chapman J (2001) Quantitative measurements of mouse brain thrombin-like and thrombin inhibition activities. Neuroreport 12:2347-2351 (Pubitemid 32682185)
3. Beilin O, Karussis DM, Korczyn AD, Gurwitz D, Aronovich R, Hantai D, Grigoriadis N, Mizrachi-Kol R, Chapman J (2005) Increased thrombin inhibition in experimental autoimmune encephalomyelitis. J Neurosci Res 79:351-359 (Pubitemid 40278349)
4. Beilin O, Karussis DM, Korczyn AD, Gurwitz D, Aronovich R, Mizrachi-Kol R, Chapman J (2007) Increased KPI containing amyloid precursor protein in experimental autoimmune encephalomyelitis brains. Neuroreport 18:581-584 (Pubitemid 46594919)
5. Benson RR, Gattu R, Sewick B, Kou Z, Zakariah N, Cavanaugh JM, Haacke EM (2012) Detection of hemorrhagic and axonal pathology in mild traumatic brain injury using advanced MRI: implications for neurorehabilitation. NeuroRehabilitation 31:261-279
6. Chapman J (2006) Thrombin in inflammatory brain diseases. Autoimmun Rev 5:528-531
7. Dix SL, Aggleton JP (1999) Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res 99:191-200 (Pubitemid 29083445)
8. Donovan FM, Cunningham DD (1998) Signaling pathways involved in thrombin-induced cell protection. J Biol Chem 273:12746-12752 (Pubitemid 28246827)
9. Feinsod M, Langer KG(2012) The philosopher's swoon - the concussion of Michel de Montaigne: a historical vignette.World Neurosurg 78: 371-374
10. Friedmann I, Faber-Elman A, Yoles E, Schwartz M (1999) Injury-induced gelatinase and thrombin-like activities in regenerating and nonregenerating nervous systems. FASEB J 13:533-543 (Pubitemid 29115571)
11. Friedmann I, Hauben E, Yoles E, Kardash L, Schwartz M (2001a) T cell-mediated neuroprotection involves antithrombin activity. J Neuroimmunol 121:12-21 (Pubitemid 34008446)
12. Friedmann I, Yoles E, Schwartz M (2001b) Thrombin attenuation is neuroprotective in the injured rat optic nerve. J Neurochem 76: 641-649 (Pubitemid 32126063)
13. Han KS,MannaioniG, Hamill CE, Lee J, Junge CE, Lee CJ, Traynelis SF (2011) Activation of protease activated receptor 1 increases the excitability of the dentate granule neurons of hippocampus. Mol Brain 4:32
14. Korn A, Golan H,Melamed I, Pascual-Marqui R, Friedman A (2005) Focal cortical dysfunction and blood-brain barrier disruption in patients with Postconcussion syndrome. J Clin Neurophysiol 22:1-9 (Pubitemid 40194694)
15. Lee KR, Drury I, Vitarbo E, Hoff JT (1997) Seizures induced by intracerebral injection of thrombin: a model of intracerebral hemorrhage. J Neurosurg 87:73-78 (Pubitemid 27271030)
16. Lee CJ, Mannaioni G, Yuan H, Woo DH, Gingrich MB, Traynelis SF (2007) Astrocytic control of synaptic NMDA receptors. J Physiol 581:1057-1081 (Pubitemid 46887980)
17. Luo W, Wang Y, Reiser G (2007) Protease-activated receptors in the brain: receptor expression, activation, and functions in neurodegeneration and neuroprotection. Brain Res Rev 56:331-345 (Pubitemid 350176599)
18. Maggio N, Segal M (2012) Cellular basis of a rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices. Hippocampus 22:267-275
19. Maggio N, Shavit E, Chapman J, Segal M (2008) 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. J Neurosci 28:732-736 (Pubitemid 351159017)
20. Maggio N, Blatt I, Vlachos A, Tanne D, Chapman J, Segal M (2013a) Treating seizures and epilepsy with anticoagulants? Front Cell Neurosci 7:19
21. Maggio N, Cavaliere C, Papa M, Blatt I, Chapman J, Segal M (2013b) Thrombin regulation of synaptic transmission: implications for seizure onset. Neurobiol Dis 50:171-178
22. Maggio N, Itsekson Z, Dominissini D, Blatt I, Amariglio N, Rechavi G, Tanne D, Chapman J (2013c) Thrombin regulation of synaptic plasticity: implications for physiology and pathology. Exp Neurol 247:595-604
23. Mhatre M, Nguyen A, Kashani S, Pham T, Adesina A, Grammas P (2004) Thrombin, a mediator of neurotoxicity and memory impairment. Neurobiol Aging 25:783-793 (Pubitemid 38698252)
24. Milman A, Rosenberg A, Weizman R, Pick CG (2005) Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J Neurotrauma 22:1003-1010 (Pubitemid 41362066)
25. Mott TF, Mcconnon ML, Rieger BP (2012) Subacute to chronic mild traumatic brain injury. Am Fam Physician 86:1045-1051
26. Movsesyan VA, Yakovlev AG, Fan L, Faden AI (2001) Effect of serine protease inhibitors on posttraumatic brain injury and neuronal apoptosis. Exp Neurol 167:366-375 (Pubitemid 32150894)
27. Pan W, Kastin AJ, Rigai T, Mclay R, Pick CG (2003) Increased hippocampal uptake of tumor necrosis factor alpha and behavioral changes in mice. Exp Brain Res 149:195-199 (Pubitemid 36315369)
28. Povlishock JT, Christman CW (1995) The pathobiology of traumatically induced axonal injury in animals and humans: a review of current thoughts. J Neurotrauma 12:555-564
29. Povlishock JT, Jenkins LW (1995) Are the pathobiological changes evoked by traumatic brain injury immediate and irreversible? Brain Pathol 5:415-426
30. Reeves TM, Lyeth BG, Povlishock JT (1995) Long-term potentiation deficits and excitability changes following traumatic brain injury. Exp Brain Res 106:248-256
31. Rubovitch V, Ten-Bosch M, Zohar O, Harrison CR, Tempel-Brami C, Stein E, Hoffer BJ, Balaban CD, Schreiber S, Chiu WT, Pick CG (2011) A mouse model of blast-induced mild traumatic brain injury. Exp Neurol 232:280-289
32. Shavit E, Beilin O, Korczyn AD, Sylantiev C, Aronovich R, Drory VE, Gurwitz D, Horresh I, Bar-Shavit R, Peles E, Chapman J (2008) Thrombin receptor PAR-1 on myelin at the node of Ranvier: a new anatomy and physiology of conduction block. Brain 131:1113-1122 (Pubitemid 351499419)
33. Shavit E,Michaelson DM, Chapman J (2011) Anatomical localization of protease-activated receptor-1 and protease-mediated neuroglial crosstalk on peri-synaptic astrocytic endfeet. J Neurochem 119: 460-473
34. Shaw NA (2002) The neurophysiology of concussion. Prog Neurobiol 67:281-344
35. Tashlykov V, Katz Y, Gazit V, Zohar O, Schreiber S, Pick CG (2007) Apoptotic changes in the cortex and hippocampus following minimal brain trauma in mice. Brain Res 1130:197-205 (Pubitemid 46084834)
36. Tashlykov V, Katz Y, Volkov A, Gazit V, Schreiber S, Zohar O, Pick CG (2009) Minimal traumatic brain injury induce apoptotic cell death in mice. J Mol Neurosci 37:16-24
37. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350-4354 (Pubitemid 9256559)
38. Tricoci P, Huang Z, Held C, Moliterno DJ, Armstrong PW, Van DeWerf F, White HD, Aylward PE, Wallentin L, Chen E, Lokhnygina Y, Pei J, Leonardi S, Rorick TL, Kilian AM, Jennings LH, Ambrosio G, Bode C, Cequier A, Cornel JH, Diaz R, Erkan A, Huber K, Hudson MP, Jiang L, Jukema JW, Lewis BS, Lincoff AM, Montalescot G, Nicolau JC, Ogawa H, Pfisterer M, Prieto JC, Ruzyllo W, Sinnaeve PR, Storey RF, Valgimigli M, Whellan DJ, Widimsky P, Strony J, Harrington RA, Mahaffey KW(2012) Thrombin-receptor antagonist vorapaxar in acute coronary syndromes. N Engl J Med 366:20-33
39. Tweedie D,Milman A, Holloway HW, Li Y, Harvey BK, Shen H, Pistell PJ, Lahiri DK, Hoffer BJ, Wang Y, Pick CG, Greig NH (2007) Apoptotic and behavioral sequelae of mild brain trauma in mice. J Neurosci Res 85:805-815 (Pubitemid 46426080)
40. Ucar T, Tanriover G, Gurer I, Onal MZ, Kazan S (2006) Modified experimental mild traumatic brain injury model. J Trauma 60:558-565
41. Xue M, Del Bigio MR (2001) Acute tissue damage after injections of thrombin and plasmin into rat striatum. Stroke 32:2164-2169
42. Zohar O, Schreiber S, Getslev V, Schwartz JP, Mullins PG, Pick CG (2003) Closed-head minimal traumatic brain injury produces long-term cognitive deficits in mice. Neuroscience 118: 949- 955
43. Zohar O, Getslev V, Miller AL, Schreiber S, Pick CG (2006) Morphine protects for head trauma induced cognitive deficits in mice. Neurosci Lett 394:239-242
44. Zohar O, Rubovitch V, Milman A, Schreiber S, Pick CG (2011) Behavioral consequences of minimal traumatic brain injury in mice. Acta Neurobiol Exp (Wars) 71:36-45