Status epilepticus, blood-brain barrier disruption, inflammation, and epileptogenesis

Epilepsy and Behavior

Volumn 49, Issue , 2015, Pages 13-16

  Gorter, Jan A ^a   Van Vliet, Erwin A ^b   Aronica, Eleonora ^a,b,c  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

Author keywords

Angiogenesis; Blood brain barrier; Epilepsy; Immune response; Inflammation; Leakage; Status epilepticus

Indexed keywords

CELL ADHESION MOLECULE; GLUTAMATE RECEPTOR; INTEGRIN; RAPAMYCIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; CELL ACTIVATION; CELL ADHESION; ENDOTHELIUM CELL; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; GLIA CELL; HUMAN; HYPERTENSION; MEMBRANE PERMEABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NECROSIS; NERVE SPROUTING; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; POTASSIUM TRANSPORT; PROTEIN BINDING; REVIEW; UPREGULATION; ANIMAL; INFLAMMATION; PATHOPHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD-BRAIN BARRIER; HUMANS; INFLAMMATION; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS;

EID: 84939582946     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2015.04.047     Document Type: Review

References (68)

1. Hesdorffer D.C., Logroscino G., Cascino G., Annegers J.F., Hauser W.A. Risk of unprovoked seizure after acute symptomatic seizure: effect of status epilepticus. Ann Neurol 1998, 44:908-912.
2. Chen J.W., Wasterlain C.G. Status epilepticus: pathophysiology and management in adults. Lancet Neurol 2006, 5:246-256.
3. Seiffert E., Dreier J.P., Ivens S., Bechmann I., Tomkins O., Heinemann U., et al. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 2004, 24:7829-7836.
4. Marchi N., Angelov L., Masaryk T., Fazio V., Granata T., Hernandez N., et al. Seizure-promoting effect of blood-brain barrier disruption. Epilepsia 2007, 48:732-742.
5. Oby E., Janigro D. The blood-brain barrier and epilepsy. Epilepsia 2006, 47:1761-1774.
6. van Vliet E.A., Aronica E., Gorter J.A. Blood-brain barrier dysfunction, seizures and epilepsy. Semin Cell Dev Biol 2015, 38:26-34.
7. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat Rev Neurol 2011, 7:31-40.
8. van Vliet E.A., Aronica E., Gorter J.A. Role of blood-brain barrier in temporal lobe epilepsy and pharmacoresistance. Neuroscience 2014, 277:455-473.
9. Abbott N.J., Friedman A. Overview and introduction: the blood-brain barrier in health and disease. Epilepsia 2012, 53(Suppl. 6):1-6.
10. Marchi N., Tierney W., Alexopoulos A.V., Puvenna V., Granata T., Janigro D. The etiological role of blood-brain barrier dysfunction in seizure disorders. Cardiovasc Psychiatry Neurol 2011, 2011:482415.
11. Frigerio F., Frasca A., Weissberg I., Parrella S., Friedman A., Vezzani A., et al. Long-lasting pro-ictogenic effects induced in vivo by rat brain exposure to serum albumin in the absence of concomitant pathology. Epilepsia 2012, 53:1887-1897.
12. Ndode-Ekane X.E., Hayward N., Grohn O., Pitkanen A. Vascular changes in epilepsy: functional consequences and association with network plasticity in pilocarpine-induced experimental epilepsy. Neuroscience 2010, 166:312-332.
13. van Vliet E.A., da Costa Araujo S., Redeker S., van Schaik R., Aronica E., Gorter J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007, 130:521-534.
14. Friedman A., Kaufer D., Heinemann U. Blood-brain barrier breakdown-inducing astrocytic transformation: novel targets for the prevention of epilepsy. Epilepsy Res 2009, 85:142-149.
15. Weissberg I., Wood L., Kamintsky L., Vazquez O., Milikovsky D.Z., Alexander A., et al. Albumin induces excitatory synaptogenesis through astrocytic TGF-β/ALK5 signaling in a model of acquired epilepsy following blood-brain barrier dysfunction. Neurobiol Dis 2015, 78:115-125.
16. Jeon S.B., Parikh G., Choi H.A., Lee K., Lee J.H., Schmidt J.M., et al. Acute cerebral microbleeds in refractory status epilepticus. Epilepsia 2013, 54:e66-e68.
17. Sloviter R.S., Bumanglag A.V. Defining "epileptogenesis" and identifying "antiepileptogenic targets" in animal models of acquired temporal lobe epilepsy is not as simple as it might seem. Neuropharmacology 2013, 69:3-15.
18. Sperk G., Lassmann H., Baran H., Kish S.J., Seitelberger F., Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience 1983, 10:1301-1315.
19. Jo A., Heo C., Schwartz T.H., Suh M. Nanoscale intracortical iron injection induces chronic epilepsy in rodent. J Neurosci Res 2014, 92:389-397.
20. Willmore L.J., Sypert G.W., Munson J.B. Recurrent seizures induced by cortical iron injection: a model of posttraumatic epilepsy. Ann Neurol 1978, 4:329-336.
21. Tishler D.M., Weinberg K.I., Hinton D.R., Barbaro N., Annett G.M., Raffel C. MDR1 gene expression in brain of patients with medically intractable epilepsy. Epilepsia 1995, 36:1-6.
22. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F., et al. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci 1999, 19:5054-5065.
23. Sokrab T.E., Kalimo H., Johansson B.B. Parenchymal changes related to plasma protein extravasation in experimental seizures. Epilepsia 1990, 31:1-8.
24. Pont F., Collet A., Lallement G. Early and transient increase of rat hippocampal blood-brain barrier permeability to amino acids during kainic acid-induced seizures. Neurosci Lett 1995, 184:52-54.
25. Lassmann H., Petsche U., Kitz K., Baran H., Sperk G., Seitelberger F., et al. The role of brain edema in epileptic brain damage induced by systemic kainic acid injection. Neuroscience 1984, 13:691-704.
26. Roch C., Leroy C., Nehlig A., Namer I.J. Magnetic resonance imaging in the study of the lithium-pilocarpine model of temporal lobe epilepsy in adult rats. Epilepsia 2002, 43:325-335.
27. Rigau V., Morin M., Rousset M.C., de Bock F., Lebrun A., Coubes P., et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007, 130:1942-1956.
28. van Vliet E.A., Otte W.M., Gorter J.A., Dijkhuizen R.M., Wadman W.J. Longitudinal assessment of blood-brain barrier leakage during epileptogenesis in rats. A quantitative MRI study. Neurobiol Dis 2014, 63:74-84.
29. Stanimirovic D.B., Friedman A. Pathophysiology of the neurovascular unit: disease cause or consequence?. J Cereb Blood Flow Metab 2012, 32:1207-1221.
30. Friedman A., Heinemann U. Role of blood-brain barrier dysfunction in epileptogenesis. editors. Jasper's Basic Mechanisms of the Epilepsies 2012, Oxford University Press, USA. 4th ed. J.L. Noebels, M. Avoli, M.A. Rogawski, R.W. Olsen, A.V. Delgado-Escueta (Eds.).
31. Ivens S., Kaufer D., Flores L.P., Bechmann I., Zumsteg D., Tomkins O., et al. TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 2007, 130:535-547.
32. Cacheaux L.P., Ivens S., David Y., Lakhter A.J., Bar-Klein G., Shapira M., et al. Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J Neurosci 2009, 29:8927-8935.
33. Bar-Klein G., Cacheaux L.P., Kamintsky L., Prager O., Weissberg I., Schoknecht K., et al. Losartan prevents acquired epilepsy via TGF-beta signaling suppression. Ann Neurol 2014, 75:864-875.
34. Krizbai I.A., Deli M.A., Pestenacz A., Siklos L., Szabo C.A., Andras I., et al. Expression of glutamate receptors on cultured cerebral endothelial cells. J Neurosci Res 1998, 54:814-819.
35. Neuhaus W., Freidl M., Szkokan P., Berger M., Wirth M., Winkler J., et al. Effects of NMDA receptor modulators on a blood-brain barrier in vitro model. Brain Res 2011, 1394:49-61.
36. Ueda Y., Yokoyama H., Nakajima A., Tokumaru J., Doi T., Mitsuyama Y. Glutamate excess and free radical formation during and following kainic acid-induced status epilepticus. Exp Brain Res 2002, 147:219-226.
37. Rowley H.L., Martin K.F., Marsden C.A. Decreased GABA release following tonic-clonic seizures is associated with an increase in extracellular glutamate in rat hippocampus in vivo. Neuroscience 1995, 68:415-422.
38. Sharp C.D., Houghton J., Elrod J.W., Warren A., Jackson, Jawahar A., et al. N-methyl-D-aspartate receptor activation in human cerebral endothelium promotes intracellular oxidant stress. Am J Physiol Heart Circ Physiol 2005, 288:H1893-H1899.
39. Lothman E. The biochemical basis and pathophysiology of status epilepticus. Neurology 1990, 40:13-23.
40. Meldrum B.S., Horton R.W. Physiology of status epilepticus in primates. Arch Neurol 1973, 28:1-9.
41. Petito C.K., Schaefer J.A., Plum F. Ultrastructural characteristics of brain and blood-brain-barrier in experimental seizures. Brain Res 1977, 127:251-267.
42. Oztas B., Kaya M. The effect of acute hypertension on blood-brain barrier permeability to albumin during experimentally induced epileptic seizures. Pharmacol Res 1991, 23:41-46.
43. Girouard H., Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 2006, 100:328-335.
44. Tomlinson F.H., Anderson R.E., Meyer F.B. Effect of arterial blood pressure and serum glucose on brain intracellular pH, cerebral and cortical blood flow during status epilepticus in the white New Zealand rabbit. Epilepsy Res 1993, 14:123-137.
45. Sokrab T.E., Johansson B.B., Kalimo H., Olsson Y. A transient hypertensive opening of the blood-brain barrier can lead to brain damage. Extravasation of serum proteins and cellular changes in rats subjected to aortic compression. Acta Neuropathol 1988, 75:557-565.
46. Nitsch C., Klatzo I. Regional patterns of blood-brain barrier breakdown during epileptiform seizures induced by various convulsive agents. J Neurol Sci 1983, 59:305-322.
47. Cornford E.M., Hyman S., Cornford M.E., Landaw E.M., Delgado-Escueta A.V. Interictal seizure resections show two configurations of endothelial Glut1 glucose transporter in the human blood-brain barrier. J Cereb Blood Flow Metab 1998, 18:26-42.
48. Abbott N.J., Ronnback L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53.
49. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.
50. Librizzi L., Noe F., Vezzani A., de Curtis M., Ravizza T. Seizure-induced brain-borne inflammation sustains seizure recurrence and blood-brain barrier damage. Ann Neurol 2012, 72:82-90.
51. Devinsky O., Vezzani A., Najjar S., De Lanerolle N.C., Rogawski M.A. Glia and epilepsy: excitability and inflammation. Trends Neurosci 2013, 36:174-184.
52. Maroso M., Balosso S., Ravizza T., Liu J., Bianchi M.E., Vezzani A. Interleukin-1 type 1 receptor/Toll-like receptor signalling in epilepsy: the importance of IL-1beta and high-mobility group box 1. J Intern Med 2011, 270:319-326.
53. Maroso M., Balosso S., Ravizza T., Iori V., Wright C.I., French J., et al. Interleukin-1beta biosynthesis inhibition reduces acute seizures and drug resistant chronic epileptic activity in mice. Neurotherapeutics 2011, 8:304-315.
54. Zeng L.H., Rensing N.R., Wong M. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J Neurosci 2009, 29:6964-6972.
55. Galanopoulou A.S., Gorter J.A., Cepeda C. Finding a better drug for epilepsy: the mTOR pathway as an antiepileptogenic target. Epilepsia 2012, 53:1119-1130.
56. Ljungberg M.C., Bhattacharjee M.B., Lu Y., Armstrong D.L., Yoshor D., Swann J.W., et al. Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia. Ann Neurol 2006, 60:420-429.
57. van Vliet E.A., Forte G., Holtman L., den Burger J.C., Sinjewel A., de Vries H.E., et al. Inhibition of mammalian target of rapamycin reduces epileptogenesis and blood-brain barrier leakage but not microglia activation. Epilepsia 2012, 53:1254-1263.
58. Huang X., Zhang H., Yang J., Wu J., McMahon J., Lin Y., et al. Pharmacological inhibition of the mammalian target of rapamycin pathway suppresses acquired epilepsy. Neurobiol Dis 2010, 40:193-199.
59. Macias M., Blazejczyk M., Kazmierska P., Caban B., Skalecka A., Tarkowski B., et al. Spatiotemporal characterization of mTOR kinase activity following kainic acid induced status epilepticus and analysis of rat brain response to chronic rapamycin treatment. PLoS One 2013, 8:e64455.
60. Buckmaster P.S., Lew F.H. Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. J Neurosci 2011, 31:2337-2347.
61. Gorter J.A., van Vliet E.A., Aronica E., Breit T., Rauwerda H., Lopes da Silva F.H., et al. Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J Neurosci 2006, 26:11083-11110.
62. Duffy B.A., Choy M., Riegler J., Wells J.A., Anthony D.C., Scott R.C., et al. Imaging seizure-induced inflammation using an antibody targeted iron oxide contrast agent. Neuroimage 2012, 60:1149-1155.
63. Fabene P.F., Navarro M.G., Martinello M., Rossi B., Merigo F., Ottoboni L., et al. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med 2008, 14:1377-1383.
64. Fabene P.F., Laudanna C., Constantin G. Leukocyte trafficking mechanisms in epilepsy. Mol Immunol 2013, 55:100-104.
65. Zattoni M., Mura M.L., Deprez F., Schwendener R.A., Engelhardt B., Frei K., et al. Brain infiltration of leukocytes contributes to the pathophysiology of temporal lobe epilepsy. J Neurosci 2011, 31:4037-4050.
66. Ravizza T., Gagliardi B., Noe F., Boer K., Aronica E., Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 2008, 29:142-160.
67. Croll S.D., Ransohoff R.M., Cai N., Zhang Q., Martin F.J., Wei T., et al. VEGF-mediated inflammation precedes angiogenesis in adult brain. Exp Neurol 2004, 187:388-402.
68. Marchi N., Lerner-Natoli M. Cerebrovascular remodeling and epilepsy. Neuroscientist 2013, 19:304-312.