Blood-brain barrier dysfunction, TGFβ signaling, and astrocyte dysfunction in epilepsy

GLIA

Volumn 60, Issue 8, 2012, Pages 1251-1257

  Heinemann, Uwe ^a   Kaufer, Daniela ^b   Friedman, Alon ^c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Astroglia; Buffering; Connexins; Glutamate; Potassium channels

Indexed keywords

ALBUMIN; AQUAPORIN 4; GLUTAMIC ACID; POTASSIUM; POTASSIUM CHANNEL; PROTEINASE ACTIVATED RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD BRAIN BARRIER DYSFUNCTION; BRAIN DYSFUNCTION; BRAIN INJURY; DISEASE ASSOCIATION; DOWN REGULATION; EPILEPSY; EPILEPTOGENESIS; GAP JUNCTION; GLIA; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEIZURE; SIGNAL TRANSDUCTION; VASCULAR DISEASE;

ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; EPILEPSY; HUMANS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84862321002     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22311     Document Type: Review

References (90)

1. Abbott NJ, Ronnback L, Hansson E. 2006. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7: 41-53.
2. Aronica E, van Vliet EA, Mayboroda OA, Troost D, da Silva FH, Gorter JA. 2000. Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur J Neurosci 12: 2333-2344.
3. Barkai E, Golan H, Grossman Y, Gutnick MJ. 1990. Pentylenetetrazole-induced kindling is prevented by prior treatment with cysteamine. Eur J Pharmacol 182: 167-169.
4. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A. 2004. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7: 613-620.
5. Bien CG, Scheffer IE. 2011. Autoantibodies and epilepsy. Epilepsia 52 (Suppl 3): 18-22.
6. Binder DK, Steinhauser C. 2006. Functional changes in astroglial cells in epilepsy. Glia 54: 358-368.
7. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT. 2006. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53: 631-636.
8. Blobe GC, Schiemann WP, Lodish HF. 2000. Role of transforming growth factor beta in human disease. N Engl J Med 342: 1350-1358.
9. Bockenhauer D, Feather S, Stanescu HC, Bandulik S, Zdebik AA, Reichold M, Tobin J, Lieberer E, Sterner C, Landoure G, Arora R, Sirimanna T, Thompson D, Cross JH, van't Hoff W, Al MO, Tullus K, Yeung S, Anikster Y, Klootwijk E, Hubank M, Dillon MJ, Heitzmann D, Arcos-Burgos M, Knepper MA, Dobbie A, Gahl WA, Warth R, Sheridan E, Kleta R. 2009. Epilepsy, ataxia, sensorineural deafness, tubulopathy, and KCNJ10 mutations. N Engl J Med 360: 1960-1970.
10. Brionne TC, Tesseur I, Masliah E, Wyss-Coray T. 2003. Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 40: 1133-1145.
11. Cacheaux LP, Ivens S, David Y, Lakhter AJ, Bar-Klein G, Shapira M, Heinemann U, Friedman A, Kaufer D. 2009. Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J Neurosci 29: 8927-8935.
12. Cervos-Navarro J, Lafuente JV. 1991. Traumatic brain injuries: Structural changes. J Neurol Sci 103: 3-14.
13. Chaudhry FA, Lehre KP, Lookeren Campagne Mv, Ottersen OP, Danbolt NC, Storm-Mathisen J. 1995. Glutamate transporters in glial plasma membranes: Highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15: 711-720.
14. Cornford EM. 1999. Epilepsy and the blood brain barrier: Endothelial cell responses to seizures. Adv Neurol 79: 845-862.
15. Cornford EM, Oldendorf WH. 1986. Epilepsy and the blood-brain barrier. Adv Neurol 44: 787-812.
16. Curia G, Longo D, Biagini G, Jones RS, Avoli M. 2008. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172: 143-157.
17. David Y, Cacheaux LP, Ivens S, Lapilover E, Heinemann U, Kaufer D, Friedman A. 2009. Astrocytic dysfunction in epileptogenesis: Consequence of altered potassium and glutamate homeostasis? J Neurosci 29: 10588-10599.
18. Derouiche A, Frotscher M. 1991. Astroglial processes around identified glutamatergic synapses contain glutamine synthetase: Evidence for transmitter degradation. Brain Res 552: 346-350.
19. Dietzel I, Heinemann U, Lux HD. 1989. Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular volume changes during neuronal hyperactivity in cat brain. Glia 2: 25-44.
20. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD. 2007. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27: 11354-11365.
21. Dohgu S, Takata F, Yamauchi A, Nakagawa S, Egawa T, Naito M, Tsuruo T, Sawada Y, Niwa M, Kataoka Y. 2005. Brain pericytes contribute to the induction and up-regulation of blood-brain barrier functions through transforming growth factor-beta production. Brain Res 1038: 208-215.
22. Eid T, Ghosh A, Wang Y, Beckstrom H, Zaveri HP, Lee TS, Lai JC, Malthankar-Phatak GH, de Lanerolle NC. 2008. Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippocampus in rats. Brain 131: 2061-2070.
23. Friedman A, Kaufer D, Heinemann U. 2009. Blood-brain barrier breakdown-inducing astrocytic transformation: Novel targets for the prevention of epilepsy. Epilepsy Res 85: 142-149.
24. Futamachi KJ, Pedley TA. 1976. Glial cells and extracellular potassium: Their relationship in mammalian cortex. Brain Res 109: 311-322.
25. Gabriel S, Kivi A, Kovacs R, Lehmann TN, Lanksch WR, Meencke HJ, Heinemann U. 1998. Effects of barium on stimulus-induced changes in [K+]o and field potentials in dentate gyrus and area CA1 of human epileptic hippocampus. Neurosci Lett 249: 91-94.
26. Gardner-Medwin AR, Nicholson C. 1983. Changes of extracellular potassium activity induced by electric current through brain tissue in the rat. J Physiol 335: 375-392.
27. Gold LI, Parekh TV. 1999. Loss of growth regulation by transforming growth factor-beta (TGF-beta) in human cancers: Studies on endometrial carcinoma. Semin Reprod Endocrinol 17: 73-92.
28. Hablitz JJ, Heinemann U. 1987. Extracellular K+ and Ca2+ changes during epileptiform discharges in the immature rat neocortex. Brain Res 433: 299-303.
29. Halpern L. 1972. Chronically isolated aggregates of mammalian cerebral cortical neurons studied in-situ. In: Purpura D, Penry J, Tower D, Woodbury D, Walter R, editors. Experimental Models of Epilepsy. New York: Raven. pp 197-221.
30. Heinemann U, Gabriel S, Jauch R, Schulze K, Kivi A, Eilers A, Kovacs R, Lehmann TN. 2000. Alterations of glial cell function in temporal lobe epilepsy. Epilepsia 41 (Suppl 6): S185-S189.
31. Hoffman SN, Salin PA, Prince DA. 1994. Chronic neocortical epileptogenesis in vitro. J Neurophysiol 71: 1762-1773.
32. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, Seiffert E, Heinemann U, Friedman A. 2007. TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 130: 535-547.
33. Jabs R, Seifert G, Steinhauser C. 2008. Astrocytic function and its alteration in the epileptic brain. Epilepsia (49 Suppl 2): 3-12.
34. Jacobs KM, Hwang BJ, Prince DA. 1999. Focal epileptogenesis in a rat model of polymicrogyria. J Neurophysiol 81: 159-173.
35. Jauch R, Windmuller O, Lehmann TN, Heinemann U, Gabriel S. 2002. Effects of barium, furosemide, ouabaine and 4, 4′-diisothiocyanatostilbene-2, 2′-disulfonic acid (DIDS) on ionophoretically-induced changes in extracellular potassium concentration in hippocampal slices from rats and from patients with epilepsy. Brain Res 925: 18-27.
36. Kasantikul V, Brown WJ, Oldendorf WH, Crandall PC. 1983. Ultrastructural parameters of limbic microvasculature in human psychomotor epilepsy. Clin Neuropathol 2: 171-178.
37. Kivi A, Lehmann TN, Kovacs R, Eilers A, Jauch R, Meencke HJ, von Deimling A, Heinemann U, Gabriel S. 2000. Effects of barium on stimulus-induced rises of [K+]o in human epileptic non-sclerotic and sclerotic hippocampal area CA1. Eur J Neurosci 12: 2039-2048.
38. 2+ concentrations in the hippocampus. Can J Physiol Pharmacol 60: 1658-1671.
39. Löscher W. 2002. Animal models of epilepsy for the development of antiepileptogenic and disease-modifying drugs. A comparison of the pharmacology of kindling and post-status epilepticus models of temporal lobe epilepsy. Epilepsy Res 50: 105-123.
40. Lothman EW, Bennett JP, Perlin JB. 1987. Alterations in neurotransmitter amino acids in hippocampal kindled seizures. Epilepsy Res 1: 313-320.
41. Lux HD, Heinemann U, Dietzel I. 1986. Ionic changes and alterations in the size of the extracellular space during epileptic activity. Adv Neurol 44: 619-639.
42. 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.
43. Massague J, Wotton D. 2000. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 19: 1745-1754.
44. McNamara JO. 1988. Pursuit of the mechanisms of kindling. Trends Neurosci 11: 33-36.
45. McNeill H, Williams C, Guan J, Dragunow M, Lawlor P, Sirimanne E, Nikolics K, Gluckman P. 1994. Neuronal rescue with transforming growth factor-beta 1 after hypoxic-ischaemic brain injury. Neuroreport 5: 901-904.
46. Mesples B, Fontaine RH, Lelievre V, Launay JM, Gressens P. 2005. Neuronal TGF-beta1 mediates IL-9/mast cell interaction and exacerbates excitotoxicity in newborn mice. Neurobiol Dis 18: 193-205.
47. Nadal A, Fuentes E, Pastor J, McNaughton PA. 1995. Plasma albumin is a potent trigger of calcium signals and DNA synthesis in astrocytes. Proc Natl Acad Sci USA 92: 1426-1430.
48. Neuwelt EA. 2004. Mechanisms of disease: The blood-brain barrier. Neurosurgery 54: 131-140.
49. Opdam HI, Federico P, Jackson GD, Buchanan J, Abbott DF, Fabinyi GC, Syngeniotis A, Vosmansky M, Archer JS, Wellard RM, Bellomo R. 2002. A sheep model for the study of focal epilepsy with concurrent intracranial EEG and functional MRI. Epilepsia 43: 779-787.
50. Pasler D, Gabriel S, Heinemann U. 2007. Two-pore-domain potassium channels contribute to neuronal potassium release and glial potassium buffering in the rat hippocampus. Brain Res 1173: 14-26.
51. Perillan PR, Chen M, Potts EA, Simard JM. 2002. Transforming growth factor-beta 1 regulates Kir2.3 inward rectifier K+ channels via phospholipase C and protein kinase C-delta in reactive astrocytes from adult rat brain. J Biol Chem 277: 1974-1980.
52. Phillips DJ, Nguyen P, Adamides AA, Bye N, Rosenfeld JV, Kossmann T, Vallance S, Murray L, Morganti-Kossmann MC. 2006. Activin a release into cerebrospinal fluid in a subset of patients with severe traumatic brain injury. J Neurotrauma 23: 1283-1294.
53. Pitkänen A. 2010. Therapeutic approaches to epileptogenesis-Hope on the horizon. Epilepsia 51 (Suppl 3): 2-17.
54. Pitkänen A, McIntosh TK. 2006. Animal models of post-traumatic epilepsy. J Neurotrauma 23: 241-261.
55. Plata-Salaman CR, Ilyin SE, Turrin NP, Gayle D, Flynn MC, Romanovitch AE, Kelly ME, Bureau Y, Anisman H, McIntyre DC. 2000. Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res Mol Brain Res 75: 248-258.
56. Prehn JH, Bindokas VP, Marcuccilli CJ, Krajewski S, Reed JC, Miller RJ. 1994. Regulation of neuronal Bcl2 protein expression and calcium homeostasis by transforming growth factor type beta confers wide-ranging protection on rat hippocampal neurons. Proc Natl Acad Sci USA 91: 12599-12603.
57. Prehn JH, Peruche B, Unsicker K, Krieglstein J. 1993. Isoform-specific effects of transforming growth factors-beta on degeneration of primary neuronal cultures induced by cytotoxic hypoxia or glutamate. J Neurochem 60: 1665-1672.
58. Prince DA, Tseng GF. 1993. Epileptogenesis in chronically injured cortex: In vitro studies. J Neurophysiol 69: 1276-1291.
59. Prince DA, Wilder BJ. 1967. Control mechanisms in cortical epileptogenic foci. Surround inhibition. Arch Neurol 16: 194-202.
60. Pumain R, Heinemann U. 1985. Stimulus- and amino acid-induced calcium and potassium changes in rat neocortex. J Neurophysiol 53: 1-16.
61. Rigau V, Morin M, Rousset MC, de BF, Lebrun A, Coubes P, Picot MC, Baldy-Moulinier M, Bockaert J, Crespel A, Lerner-Natoli M. 2007. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 130: 1942-1956.
62. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW. 1994. Localization of neuronal and glial glutamate transporters. Neuron 13: 713-725.
63. Schilling T, Eder C. 2003. Effects of kinase inhibitors on TGF-beta induced upregulation of Kv1.3 K+ channels in brain macrophages. Pflugers Arch 447: 312-315.
64. Schroder W, Hinterkeuser S, Seifert G, Schramm J, Jabs R, Wilkin GP, Steinhauser C. 2000. Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia 41 (Suppl 6): S181-S184.
65. Schuchmann S, Heinemann U. 2000. Diminished glutathione levels cause spontaneous and mitochondria-mediated cell death in neurons from trisomy 16 mice: A model of Down's syndrome. J Neurochem 74: 1205-1214.
66. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, Friedman A. 2004. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 24: 7829-7836.
67. Shi Y, Massague J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
68. Shlosberg D, Benifla M, Kaufer D, Friedman A. 2010. Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat Rev Neurol 6: 393-403.
69. Stewart TH, Eastman CL, Groblewski PA, Fender JS, Verley DR, Cook DG, D'Ambrosio R. 2010. Chronic dysfunction of astrocytic inwardly rectifying K+ channels specific to the neocortical epileptic focus after fluid percussion injury in the rat. J Neurophysiol 104: 3345-3360.
70. Strohschein S, Huttmann K, Gabriel S, Binder DK, Heinemann U, Steinhauser C. 2011. Impact of aquaporin-4 channels on K+ buffering and gap junction coupling in the hippocampus. Glia 59: 973-980.
71. Su ZZ, Leszczyniecka M, Kang DC, Sarkar D, Chao W, Volsky DJ, Fisher PB. 2003. Insights into glutamate transport regulation in human astrocytes: cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc Natl Acad Sci U S A 100: 1955-1960.
72. Szelenyi J. 2001. Cytokines and the central nervous system. Brain Res Bull 54: 329-338.
73. Theis M, Jauch R, Zhuo L, Speidel D, Wallraff A, Doring B, Frisch C, Sohl G, Teubner B, Euwens C, Huston J, Steinhauser C, Messing A, Heinemann U, Willecke K. 2003. Accelerated hippocampal spreading depression and enhanced locomotory activity in mice with astrocyte-directed inactivation of connexin 43. J Neurosci 23: 766-776.
74. Tian GF, Azmi H, Takano T, Xu QW, Peng WG, Lin J, Oberheim N, Lou NH, Wang XH, Zielke HR, Kang J, Nedergaard M. 2005. An astrocytic basis of epilepsy. Nat Med 11: 973-981.
75. Tigyi G, Hong L, Yakubu M, Parfenova H, Shibata M, Leffler CW. 1995. Lysophosphatidic acid alters cerebrovascular reactivity in piglets. Am J Physiol 268: H2048-H2055.
76. Tomkins O, Feintuch A, Benifla M, Cohen A, Friedman A, Shelef I. 2011. Blood-brain barrier breakdown following traumatic brain injury: A possible role in posttraumatic epilepsy. Cardiovasc Psychiatry Neurol 765923: 1-11.
77. Tomkins O, Friedman O, Ivens S, Reiffurth C, Major S, Dreier JP, Heinemann U, Friedman A. 2007. Blood-brain barrier disruption results in delayed functional and structural alterations in the rat neocortex. Neurobiol Dis 25: 367-377.
78. Tomkins O, Kaufer D, Korn A, Shelef I, Golan H, Reichenthal E, Soreq H, Friedman A. 2001. Frequent blood-brain barrier disruption in the human cerebral cortex. Cell Mol Neurobiol 21: 675-691.
79. Tomkins O, Shelef I, Kaizerman I, Eliushin A, Afawi Z, Misk A, Gidon M, Cohen A, Zumsteg D, Friedman A. 2008. Blood-brain barrier disruption in post-traumatic epilepsy. J Neurol Neurosurg Psychiatry 79: 774-777.
80. Turski L, Cavalheiro EA, Czuczwar SJ, Turski WA, Kleinrok Z. 1987. The seizures induced by pilocarpine: Behavioral, electroencephalographic and neuropathological studies in rodents. Pol J Pharmacol Pharm 39: 545-555.
81. van Vliet EA, da Costa AS, Redeker S, van SR, Aronica E, Gorter JA. 2007. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 130: 521-534.
82. Vincent A, Irani SR, Lang B. 2010. The growing recognition of immunotherapy-responsive seizure disorders with autoantibodies to specific neuronal proteins. Curr Opin Neurol. 23: 144-150.
83. Vitkovic L, Maeda S, Sternberg E. 2001. Anti-inflammatory cytokines: Expression and action in the brain. Neuroimmunomodulation 9: 295-312.
84. Wallraff A, Kohling R, Heinemann U, Theis M, Willecke K, Steinhauser C. 2006. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26: 5438-5447.
85. Wang Y, Moges H, Bharucha Y, Symes A. 2007. Smad3 null mice display more rapid wound closure and reduced scar formation after a stab wound to the cerebral cortex. Exp Neurol 203: 168-184.
86. Wetherington J, Serrano G, Dingledine R. 2008. Astrocytes in the epileptic brain. Neuron 58: 168-178.
87. Willoughby JO. 2000. Mechanisms underlying partial (focal, or lesional) epilepsy. J Clin Neurosci 7: 291-294.
88. Wong M. 2009. Animal models of focal cortical dysplasia and tuberous sclerosis complex: Recent progress toward clinical applications. Epilepsia 50 (Suppl 9): 34-44.
89. Zhu Y, Roth-Eichhorn S, Braun N, Culmsee C, Rami A, Krieglstein J. 2000. The expression of transforming growth factor-beta1 (TGF-beta1) in hippocampal neurons: A temporary upregulated protein level after transient forebrain ischemia in the rat. Brain Res 866: 286-298.
90. Zhu Y, Yang GY, Ahlemeyer B, Pang L, Che XM, Culmsee C, Klumpp S, Krieglstein J. 2002. Transforming growth factor-beta 1 increases bad phosphorylation and protects neurons against damage. J Neurosci 22: 3898-3909.