Epileptogenesis and reduced inward rectifier potassium current in tuberous sclerosis complex-1-deficient astrocytes

Epilepsia

Volumn 46, Issue 12, 2005, Pages 1871-1880

  Jansen, Laura A ^a,d   Uhlmann, Erik J ^a   Crino, Peter B ^c   Gutmann, David H ^a   Wong, Michael ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST LOUIS CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Epilepsy; Glia; Hamartin; Potassium channel; Seizure

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL; MESSENGER RNA; CDK2 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE 2; GLUTAMIC ACID; POTASSIUM; TUBEROUS SCLEROSIS COMPLEX 1 PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN SLICE; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; HIPPOCAMPUS; MOUSE; NERVE CELL CULTURE; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; TUBEROUS SCLEROSIS; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CYTOLOGY; EXTRACELLULAR SPACE; GENETICS; METABOLISM; MOUSE MUTANT; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR SUPPRESSOR GENE;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 2; EPILEPSY; EXTRACELLULAR SPACE; GENES, TUMOR SUPPRESSOR; GLUTAMIC ACID; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; POTASSIUM; POTASSIUM CHANNELS, INWARDLY RECTIFYING; TUBEROUS SCLEROSIS; TUMOR SUPPRESSOR PROTEINS;

EID: 33644812224     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2005.00289.x     Document Type: Article

References (60)

1. Kwiatkowski DJ. Tuberous sclerosis: from tubers to mTOR. Ann Hum Genet 2003;67:87-96.
2. Tee AR, Fingar DC, Manning BD, et al. Tuberous sclerosis complex-1 and -2 products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. Proc Natl Acad Sci U S A 2002;99:13571-6.
3. Kenerson HL, Aicher LD, True LD, et al. Activated mammalian target of rapamycin pathway in the pathogenesis of tuberous sclerosis complex renal tumors. Cancer Res 2002;62:5645-50.
4. El-Hashemite N, Walker V, Zhang H, et al. Loss of Tsc1 or Tsc2 induces vascular endothelial growth factor production through mammalian target of rapamycin. Cancer Res 2003;63:5173-7.
5. Tee AR, Manning BD, Roux PP, et al. Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signalling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003;13:1259-68.
6. Uhlmann EJ, Li W, Scheidenhelm DK, et al. Loss of tuberous sclerosis complex 1 (Tsc1) expression results in increased Rheb/S6K pathway signalling important for astrocyte cell size regulation. Glia 2004;47:180-8.
7. Uhlmann EJ, Apicelli AJ, Baldwin RL, et al. Heterozygosity for the tuberous sclerosis complex (TSC) gene products results in increased astrocyte numbers and decreased p27-Kip1 expression in TSC2± cells. Oncogene 2002;21:4050-9.
8. Uhlmann EJ, Wong M, Baldwin RL, et al. Astrocyte-specific Tsc1 conditional knockout mice exhibit abnormal neuronal organization and seizures. Ann Neurol 2002;52:285-96.
9. Rosner M, Hengstschlager M. Tuberin binds p27 and negatively regulates its interaction with the SCF component Skp2. J Biol Chem 2004;279:48707-15.
10. Soucek T, Yeung RS, Hengstschlager M. Inactivation of the cyclin-dependent kinase inhibitor p27 upon loss of the tuberous sclerosis complex gene-2. Proc Natl Acad Sci U S A 1998;95:15654-8.
11. Curatolo P, Verdecchia M, Bombardieri R. Tuberous sclerosis complex: a review of neurological aspects. Eur J Paediatr Neurol 2002;6:15-23.
12. Crino PB, Henske EP. New developments in the neurobiology of the tuberous sclerosis complex. Neurology 1999;53:1384-90.
13. Kurosinski P, Götz J. Glial cells under physiologic and pathologic conditions. Arch Neurol 2002;59:1524-8.
14. Steinhäuser C, Seifert G. Glial membrane channels and receptors in epilepsy: impact for generation and spread of seizure activity. Eur J Pharmacol 2002;447:227-37.
15. Newman E. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 2003;26:536-42.
16. During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993;341:1607-10.
17. Sherwin A, Robitaille Y, Quesney F, et al. Excitatory amino acids are elevated in human epileptic cerebral cortex. Neurology 1998;38:920-3.
18. Tanaka K, Watase K, Manabe T, et al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 1997;276:1699-702.
19. Wong M, Ess KC, Uhlmann EJ, et al. Impaired glial glutamate transport in a mouse tuberous sclerosis epilepsy model. Ann Neurol 2003;54:251-6.
20. Kojufi P, Newman EA. Potassium buffering in the central nervous system. Neuroscience 2004;129:1043-54.
21. Bordey A, Sontheimer H. Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 1998;32:286-303.
22. Gabriel S, Eilers A, Kivi A, et al. Effects of barium on stimulus induced changes in extracellular potassium concentration in area CA1 of hippocampal slices from normal and pilocarpine-treated epileptic rats. Neurosci Lett 1998;242:9-12.
23. o and field potentials in dentate gyrus and area CA1 of human epileptic hippocampus. Neurosci Lett 1998;249:91-4.
24. Hinterkeuser S, Schröder W, Hagar G, et al. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 2000;12:2087-96.
25. Jauch R, Windmüller O, Lehmann T-N, et al. Effects of barium, furosemide, oubaine 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 2002;925:18-27.
26. + uptake in glia prevents long-term depression maintenance and causes epileptiform activity. J Neurosci 1997;17:2813-24.
27. Schröder W, Hinterkeuser S, Seifert G, et al. Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia 2000;41(suppl 6):S181-4.
28. Wong M, Yamada KA. Cyclosporine induces epileptiform activity in an in vitro seizure model. Epilepsia 2000;41:271-6.
29. Kacharmina JE, Crino PB, Eberwine J. Preparation of cDNA from single cells and subcellular regions. Methods Enzymol 1999;303:3-18.
30. White R, Hua Y, Scheithauer B, et al. Selective alterations in glutamate and GABA receptor subunit mRNA expression in dysplastic neurons and giant cells of cortical tubers. Ann Neurol 2001;49:67-78.
31. Sabers CJ, Martin MM, Brunn GJ, et al. Isolation of a protein target of the FKB12-rapamycin complex in mammalian cells. J Biol Chem 1995;270:815-22.
32. Meijer L, Borgne A, Mulner O, et al. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2, and cdk5. Eur J Biochem 1997;243:527-36.
33. Chen Q, Catharine Ross A. Retinoic acid regulates cell cycle progression and cell differentiation in human monocytic THP-1 cells. Exp Cell Res 2004;297:68-81.
34. Vuocolo S, Soprano DR, Soprano KJ. p27/Kip1 mediates retinoic acid-induced suppression of ovarian carcinoma cell growth. J Cell Physiol 2004;199:237-43.
35. Matsuo T, Seth P, Thiele CJ. Increased expression of p27Kip1 arrests neuroblastoma cell growth. Med Pediatr Oncol 2001;36:97-9.
36. Borriello A, Pietra VD, Criscuolo M, et al. p27Kip1 accumulation is associated with retinoic-induced neuroblastoma differentiation: evidence of a decreased proteasome-dependent degradation. Oncogene 2000;19:51-60.
37. +) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 2001;281:C922-31.
38. Li L, Head V, Timpe LC. Identification of an inward rectifier potassium channel gene expressed in mouse cortical astrocytes. Glia 2001;33:57-71.
39. + channel, Kir4.1, in the adult rat CNS. Glia 2000;30:362-72.
40. + channels in astrocytes on mouse hippocampus. Mol Cell Neurosci 2002;19:447-58.
41. Stonehouse AH, Pringle JH, Norman RI, et al. Characterisation of Kir2.0 proteins in the rat cerebellum and hippocampus by polyclonal antibodies. Histochem Cell Biol 1999;112:457-65.
42. Thomzig A, Wenzel M, Karschin C, et al. Kir6.1 is the principal poreforming subunit of astrocyte but not neuronal plasma membrane K-ATP channels. Mol Cell Neurosci 2001;18:671-90.
43. Jiang K, Shui Q, Xia Z, et al. Changes in the gene and protein expression of KATP channel subunits in the hippocampus of rats subjected to picrotoxin-induced kindling. Mol Brain Res 2004;128:83-9.
44. + channel subunits, Kir4.1 and Kir5.1, in brain astrocytes. J Biol Chem 2004;279:44065-73.
45. Traynelis SF, Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 1988;59:259-76.
46. McNamara JO. Cellular and molecular basis of epilepsy. J Neurosci 1994;14:3413-25.
47. Neusch C, Weishaupt JH, Bähr M. Kir channels in the CNS: emerging new roles and implications for neurological diseases. Cell Tissue Res 2003;311:131-8.
48. Walz W. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 2000;36:291-300.
49. Olsen ML, Sontheimer H. Mislocalization of Kir channels in malignant glia. Glia 2004;46:63-73.
50. MacFarlane SN, Sontheimer H. Electrophysiological changes that accompany reactive gliosis in vitro. J Neurosci 1997;17:7316-29.
51. Ess KC, Uhlmann EJ, Li W, et al. Expression profiling in tuberous sclerosis complex (TSC) knockout mouse astrocytes to characterize human TSC brain pathology. Glia 2004;46:28-40.
52. Bordey A, Lyons SA, Hablitz JJ, et al. Electrophysiological characteristics of reactive astrocytes in experimental cortical dysplasia. J Neurophysiol 2001;85:1719-31.
53. Bordey A, Sontheimer H. Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J Neurophysiol 1997;78:461-77.
54. MacFarlane SN, Sontheimer H. Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes. Glia 2000;30:39-48.
55. Perego C, Vanoni C, Bossi M, et al. The GLT-1 and GLAST glutamate transporters are expressed on morphologically distinct astrocytes and regulated by neuronal activity in primary hippocampal cocultures. J Neurochem 2000;75:1076-84.
56. Swanson RA, Liu J, Miller JW, et al. Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci 1997;17:932-40.
57. Sontheimer H, Trotter J, Schachner M, et al. Channel expression correlates with differentiation stage during the development of oligodendrocytes from their precursor cells in culture. Neuron 1989;2:1135-45.
58. + conductances in glial cells of mouse hippocampal brain slices. Glia 1995;15:173-87.
59. Bringmann A, Biedermann B, Reichenbach A. Expression of potassium channels during postnatal differentiation of rabbit Muller glial cells. Eur J Neurosci 1999;11:2883-96.
60. Kalsi AS, Greenwood K, Wilkin G, et al. Kir4.1 expression by astrocytes and oligodendrocytes in CNS white matter: a developmental study in the rat optic nerve. J Anat 2004;204:475-85.