Disruption of normal cytoskeletal dynamics may play a key role in the pathogenesis of epilepsy

Neuroscientist

Volumn 16, Issue 1, 2010, Pages 28-39

  Gardiner, John ^a   Marc, Jan ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Actin; Cytoskeleton; Epilepsy; Microtubule; Neurotrophic support; Seizure

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; ALPHA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; COLCHICINE; DOUBLECORTIN; FILAMIN A; FRAGILE X MENTAL RETARDATION PROTEIN; GELSOLIN; GROWTH ASSOCIATED PROTEIN; JASPAMIDE; LATRUNCULIN A; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE PROTEIN; NEUROTROPHIC FACTOR; PACLITAXEL; PAXILLIN; PHOSPHOPROTEIN PHOSPHATASE; REELIN; RNA BINDING PROTEIN; SIRTUIN 2; SPASTIN; SPINOPHILIN; TAU PROTEIN; THIOCOLCHICOSIDE; TUBULIN; UBIQUITIN PROTEIN LIGASE; VALPROIC ACID;

ACETYLATION; ACTIN FILAMENT; AGYRIA; CYTOSKELETON; DYNAMICS; EPILEPSY; EPILEPTIC STATE; FRAGILE X SYNDROME; FRAMESHIFT MUTATION; HUMAN; INTERMEDIATE FILAMENT; MICROTUBULE; MOSSY FIBER; MYOCLONUS EPILEPSY; NERVE EXCITABILITY; NONHUMAN; PATHOGENESIS; PERIVENTRICULAR HETEROTOPIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; REVIEW; SEIZURE;

ANIMALS; CYTOSKELETON; EPILEPSY; HUMANS; NEURONS;

EID: 77949543082     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858409334422     Document Type: Review

References (96)

1. Ackman JB, Aniksztejn L., Crépel V., Becq H., Pellegrino C., Cardoso C., and others. 2009. Abnormal network activity in a targeted genetic model of human double cortex. J Neurosci 29: 313-327.
2. An SJ, See MO, Kim HS, Park SK, Hwang IK, Won MH, Kang TC 2003. Accumulation of microtubule-associated proteins in the hippocampal neurons of seizure-sensitive gerbils. Mol Cells 15: 200-207.
3. Barnes MI, Mitchell CL 1993. Decreased seizure threshold after intrahippocampal colchicine injection in rats. Brain Res Bull 31: 733-736.
4. Barton ME, Shannon HE 2005. The seizure-related phenotype of brain-derived neurotrophic factor knockdown mice. Neuroscience 136: 563-569.
5. Bellenchi GC, Gurniak CB, Perlas E., Middei S., Ammassari-Teule M., Witke W. 2007. N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev 21: 2347-2357.
6. Béraud-Dufour S., Gautier R., Albiges-Rizo C., Chardin P., Faurobert E. 2007. Krit 1 interactions with microtubules and membranes are regulated by Rap1 and integrin cytoplasmic domain associated protein-1. FEBS J 274: 5518-5532.
7. Bezgina EN, Moshkov DA, Echikov SN, Savina TA, Kalemenev SV, Morenkov ED, Shchipakina TG 2003. Morphological features of microtubule ultrastructure and MAP2 protein phosphorylation in hippocampal neurons of rats with predisposition to audiogenic epilepsy. Tsitologiia 45: 1005-1012.
8. Butowt R., von Bartheld CS 2007. Conventional kinesin-I motors participate in the anterograde axonal transport of neurotrophins in the visual system. J Neurosci Res 85: 2546-2556.
9. Campanella G., Filia A., De Michele G. 1978. Smell and taste acuity in epileptic syndromes. Eur Neurol 17: 136-141.
10. Cannell GR, Bailey MJ, Dickinson RG 2002. Inhibition of tubulin assembly and covalent binding to microtubular proteins by valproic acid glucuronide in vitro. Life Sci 71: 2633-2643.
11. Catalano MG, Poli R., Pugliese M., Fortunati N., Boccuzzi G. 2007. Valproic acid enhances tubulin acetylation and apoptotic activity of paclitaxel on anaplastic thyroid cancer cell lines. Endocr Relat Cancer 14: 839-845.
12. Catterall WA, Dib-Hall S., Meisler MH, Pietrobon D. 2008. Inherited neuronal ion channelopathies: new windows on complex neurological diseases. J Neurosci 28: 11768-11777.
13. Chai X., Forster E., Zhao S., Bock HH, Frotscher M. 2009. Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J Neurosci 29: 288-299.
14. Croll SD, Suri C., Compton DL, Simmons MV, Yancopoulos GD, Lindsay RM, and others. 1999. Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 93: 1491-1506.
15. Cronk M., Abraham R., Perrin L. 2004. Case report of a generalized seizure related to Paclitaxel infusion. J Natl Cancer Inst 96: 487.
16. Daou MC, Smith TW, Litofsky NS, Hsieh CC, Ross AH 2005. Doublecortin is preferentially expressed in invasive human brain tumors. Acta Neuropathol 110: 472-480.
17. de Nijs L., Lakaye B., Coumans B., Leon C., Ideda T., Delgado-Escueta A., and others. 2006. EFHC1, a protein mutated in juvenile myoclonic epilepsy, associates with the mitotic spindle through its N-terminus. Exp Cell Res 312: 2872-2879.
18. De Riu PL, Rosati G., Sotgiu S., Sechi G. 2001. Epileptic seizures after treatment with thiocolchicoside. Epilepsia 42: 1084-1086.
19. des Portes V., Pinard JM, Billuart P., Vinet MC, Koulakoff A., Carrié A., and others. 1998. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopias and lissencephaly syndrome. Cell 92: 51-61.
20. Deutsch SI, Rosse RB, Lakshman RM 2006. Dysregulation of tau phosphorylation is a hypothesized point of convergence in the pathogenesis of Alzheimer?s disease, frontotemporal dementia and schizophrenia with therapeutic implications. Prog Neuropsychopharmacol Biol Psychiatry 30: 1369-1380.
21. Dompierre JP, Godin JD, Charrin BC, Cordeliéres FP, King SJ, Humbert S., Saudou F. 2007. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington?s disease by increasing tubulin acetylation. J Neurosci 27: 3571-3583.
22. Estes PS, O?Shea M., Clasen S., Zarnescu DC 2008. Fragile X protein controls the efficacy of mRNA transport in Drosophila neurons. Mol Cell Neurosci 39: 170-179.
23. Fallet-Bianco C., Loeuillet L., Poirier K., Loget P., Chapon F., Pasquier L., and others. 2008. Neuropathological phenotype of a distinct form of lissencephaly associated with mutations in TUBA1A. Brain 131: 2304-2320.
24. Fox JW, Lamperti ED, Eksioglu YZ, Hong SE, Feng Y., Graham DA, and others. 1998. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopias. Neuron 21: 1315-1325.
25. Friocourt G., Liu JS, Antypa M., Rakic S., Walsh CA, Parnavelas JG 2007. Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci 27: 3875-3883.
26. Fujimoto T., Tanaka H., Kumamaru E., Okamura K., Miki N. 2004. Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule-associated protein 2 immunoreactivity in the dendrites. J Neurosci Res 76: 51-63.
27. Furukawa K., Fu W., Li Y., Witke W., Kwiatkowski DJ, Mattson MP 1997. The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons. J Neurosci 17: 8178-8186.
28. Gardiner J., Barton D., Vanslambrouk JM, Braet F., Hall D., Marc J., Overall R. 2008. Defects in tongue papillae and taste sensation indicate a problem with neurotrophic support in various neurological diseases. Neuroscientist 14: 240-250.
29. Gorter JA, van Vilet EA, Aronica E., Lopes da Silva FH 2001. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatinimmunoreactive neurons. Eur J Neurosci 13: 657-669.
30. Grabham PW, Seale GE, Bennecib M., Goldberg DJ, Vallee RB 2007. Cytoplasmic dynein and LIS1 are required for microtubule advance during growth cone remodelling and fast axonal outgrowth. J Neurosci 27: 5823-5834.
31. Gunel M., Laurans MS, Shin D., DiLuna ML, Voorhees J., Choate K., and others. 2002. KRIT1, a gene mutated in cerebral cavernous malformation, encodes a microtubule-associated protein. Proc Natl Acad Sci USA 99: 10677-10682.
32. Haas CA, Dudeck O., Kirsch M., Huszka C., Kann G., Pollak S., and others. 2002. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J Neurosci 22: 5797-5802.
33. Hoffmann K., Czapp M., L?scher W. 2008. Increase in antiepileptic efficacy during prolonged treatment with valproic acid: role of inhibition of histone deacetylases? Epilepsy Res 81: 107-113.
34. Jalava NS, Lopez-Picon FR, Kukko-Lukjanov TK, Holopainen IE 2007. Changes in microtubule-associated protein-2 (MAP2) expression during development and after status epilepticus in the immature rat hippocampus. Int J Dev Neurosci 25: 121-131.
35. Kanai Y., Okada Y., Tanaka Y., Harada A., Terada S., Hirokawa N. 2000. KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20: 6374-6384.
36. Khan N., Jeffers M., Kumar S., Hackett C., Boldog F., Khrantsov N., and others. 2008. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 409: 581-589.
37. King SM 2006. Axonemal protofilament ribbons, DM10 domains, and the link to juvenile myoclonic epilepsy. Cell Motil Cytoskeleton 63: 245-253.
38. Krimm RF 2007. Factors that regulate embryonic gustatory development. BMC Neurosci 8 Suppl 3: S4.
39. Kuromi H., Kidokoro Y. 2005. Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: lessons from the Drosophila neuromuscular junction. Neuroscientist 11: 138-147.
40. Lad Y., Jiang P., Ruskamo S., Harburger DS, Yl?Currency signnne J., Campbell ID, Calderwood DA 2008. Structural basis of the migfilin-filamin interaction and competition with integrin beta tails. J Biol Chem. Epub ahead of print.
41. L?Currency signhteinen S., Pitk?Currency signnan A., Saarelainen T., Nissinen J., Koponen E., Castrén E. 2002. Decreased BDNF signalling in transgenic mice reduces epileptogenesis. Eur J Neurosci 15: 721-734.
42. Lanthier J., Bouthiller A., Lapointe M., Demeule M., Beliveau R., Desrosiers RR 2002. Down-regulation of protein L-isoaspartyl methyltransferase in human epileptic hippocampus contributes to generation of damaged tubulin. J Neurochem 83: 581-591.
43. Lau CG, Zukin RS 2007. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8: 413-426.
44. Lee JM, Kim AS, Lee SJ, Cho SM, Lee DS, Choi SM, and others. 2006. A case of infantile Alexander disease accompanied by infantile spasms diagnosed by DNA analysis. J Korean Med Sci 21: 954-957.
45. Li R., Gundersen GG 2008. Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat Rec Mol Cell Biol 9: 860-873.
46. Limaye N., Revencu N., Van Regemorter N., Garzon M., Bonduelle M., Chung W., and others. 2007. Novel human pathological mutations. Gene symbol: KRIT1. Disease: cerebral cavernous malformation. Hum Genet 122: 552.
47. McGuire WP, Rowinsky EK, Rosenhein NB, Grumbine FC, Ettinger DS, Armstrong DK, Donehower RC 1989. Taxol: a unique antineoplastic agent with significant activity in advanced ovarian epithelial neoplasms. Ann Int Med 111: 273-279.
48. Mead SH, Proukakis C., Wood N., Crosby AH, Plant GT, Warner TT 2001. A large family with hereditary spastic paraparesis due to a frame shift mutation of the spastin (SPG4) gene: association with multiple sclerosis in two affected siblings and epilepsy in other affected family members. J Neurol Neurosurg Psychiatry 71: 788-791.
49. Mitchison T., Kirschner M. 1984. Dynamic instability of microtubule growth. Nature 312: 237-242.
50. Mittal S., Dubey D., Yamakawa K., Ganesh S. 2007. Lafora disease proteins malin and laforin are recruited to aggresomes in response to proteasomal impairment. Hum Mol Genet 16: 753-762.
51. Moores CA, Perderiset M., Kappeler C., Kain S., Drummond D., Perkins SJ, and others. 2006. Distinct roles of doublecortin modulating the microtubule cytoskeleton. EMBO J 25: 4448-4457.
52. Morii H., Yamada T., Nakano I., Coulson JM, Mori N. 2006. Site-specific phosphorylation of SCG10 in neuronal plasticity: role of Ser73 phosphorylation by N-methyl D-aspartic acid receptor activation in rat hippocampus. Neurosci Lett 396: 241-246.
53. Nosten-Bertrand M., Kappeler C., Dinocourt C., Denis C., Germain J., Phan Dinh Tuy F., and others. 2008. Epilepsy in Dcx knockout mice associated with discrete lamination defects and enhanced excitability in the hippocampus. PLoS ONE 3: e2473.
54. Ohkawa N., Fujitani K., Tokunaga E., Furuya S., Inokuchi K. 2007. The microtubule destabilizer stathmin mediates the development of dendritic arbors in neuronal cells. J Cell Sci 120: 1447-1456.
55. Otani N., Nawashiro H., Fukui S., Ooigawa H., Ohsumi A., Toyooka T., and others. 2006. Enhanced hippocampal neurodegeneration after traumatic or kainite excitotoxicity in GFAP-null mice. J Clin Neurosci 13: 934-938.
56. Pantakani DV, Swapna LS, Srinivasan N., Mannan AU 2008. Spastin oligomerizes into a hexamer and the mutant spastin (E442Q) redistribute the wild-type spastin into filamentous microtubule. J Neurochem 106: 613-624.
57. Parrini E., Ramazzotti A., Dobyns WB, Mei D., Moro F., Veggiotti P., and others. 2006. Perventricular heterotopias: phenotypic heterogeneity and correlation with Filamin A mutations. Brain 129: 1892-1906.
58. Patrylo PR, Browning RA, Cranick S. 2006. Reeler homozygous mice exhibit enhanced susceptibility to epileptiform activity. Epilepsia 47: 257-266.
59. Pilz DT, Matsumoto N., Minnerath S., Mills P., Gleeson JG, Allen KM, and others. 1998. LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum Mol Genet 7: 2029-2037.
60. Poirier K., Keays DA, Francis F., Saillour Y., Bahi N., Manouvrier S., and others. 2007. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUB1A). Hum Mutat 28: 1055-1064.
61. Pollard H., Khrestchatisky M., Moreau J., Ben-Ari Y., Repressa A. 1994. Correlation between reactive sprouting and microtubule protein expression in epileptic hippocampus. Neuroscience 61: 773-787.
62. Popa-Wagner A., Fischer B., Schmoll H., Platt D., Kessler C. 1997. Increased expression of microtubule-associated protein 1B in the hippocampus, subiculum and perforant path of rats treated with a high dose of pentylenetetrazole. Exp Neurol 148: 73-82.
63. Proper EA, Oestreicher AB, Jansen GH, Veelen CW, van Rilen PC, Gispen WH, de Graan PN 2000. Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 123: 19-30.
64. Qiu LF, Hao YH, Li QZ, Xiong ZQ 2008. Fragile X syndrome and epilepsy. Neurosci Bull 24: 338-344.
65. Reed NA, Cai D., Blasius TL, Jih GT, Meyhofer E., Gaertig J., Verhey KJ 2006. Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16: 2166-2172.
66. Reid CA, Berkovic SF, Petrou S. 2008. Mechanisms of human inherited epilepsies. Prog Neurobiol. Epub ahead of print.
67. Reiner O., Sapoznik S., Sapir T. 2006. Lissencephaly 1 linking to multiple diseases: mental retardation, neurodegeneration, schizophrenia, male sterility, and more. Neuromolecular Med 8: 547-565.
68. Repressa A., Pollard H., Moreau J., Ghilini G., Khrestchatisky M., Ben-Ari Y. 1993. Mossy fiber sprouting in epileptic rats is associated with a transient increased expression of alpha-tubulin. Neurosci Lett 156: 149-152.
69. Roth SU, Sommer C., Mundel P., Kiessling M. 2001. Expression of synaptopodin, an actin-associated protein, in the rat hippocampus after limbic epilepsy. Brain Pathol 11: 169-181.
70. Sapir T., Horesh D., Caspi M., Atlas R., Burgess HA, Wolf SG, and others. 2000. Doublecortin mutations cluster in evolutionarily conserved functional domains. Hum Mol Genet 9: 703-712.
71. Sato K., Abe K. 2001. Increases in mRNA levels for Talpha1-tubulin in the rat kindling model of epilepsy. Brain Res 904: 157-160.
72. Schek HT 3rd, Gardner MK, Cheng J., Odde DJ, Hunt AJ 2007. Microtubule assembly dynamics at the nanoscale. Curr Biol 17: 1445-1455.
73. Schmoll H., Badan I., Grecksch G., Walker L., Kessler C., Popa-Wagner A. 2003. Kindling status in Sprague-dawley rats induced by pentylenetetrazole: involvement of a critical development period. Am J Pathol 162: 1027-1034.
74. Sechi G., De Riu P., Mameli O., Deiana GA, Cocco GA, Rosati G. 2003. Focal and secondarily generalised convulsive status epilepticus induced by thiocolchicoside in the rat. Seizure 12: 508-515.
75. Sierra-Paredes G., Oreiro-Garcia T., Nunez-Rodriguez A., Vazquez-Lopez A., Sierra-Marcuno G. 2006. Seizures induced by in vivo latrunculin a and jasplakinolide microperfusion in the rat hippocampus. J Mol Neurosci 28: 151-160.
76. Stein JM, Bergman W., Fang Y., Davison L., Brensinger C., Robinson MB, and others. 2006. Behavioral and neuro-chemical alterations in mice lacking the RNA-binding protein translin. J Neurosci 26: 2184-2196.
77. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. 1989. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 26: 321-330.
78. Sutula TP, Dudek FE 2007. Unmasking recurrent excitation generated by mossy fiber sprouting in the epileptic dentate gyrus: an emergent property of a complex system. Prog Brain Res 163: 541-563.
79. Taylor KR, Holzer AK, Bazan JF, Walsh CA, Gleeson JG 2000. Patient mutations in doublecortin define a repeated tubulin-binding domain. J Biol Chem 275: 34442-34450.
80. Tian G., Kong XP, Jaglin XH, Chelly J., Keays D., Cowan NJ 2008. A pachygyria-causing alpha-tubulin mutation results in inefficient cycling with CCT and a deficient interaction with TBCB. Mol Biol Cell 19: 1152-1161.
81. Tsukada M., Prokscha A., Ungewickell E., Eichele G. 2005. Doublecortin association with actin filaments is regulated by neurabin II. J Biol Chem 280: 11361-11368.
82. Vzquez-L?3pez A., Sierra-Paredez G., Sierra-Marcuno G. 2005. Seizures induced by microperfusion of glutamate and glycine in the hippocampus of rats pretreated with latrunculin A. Neurosci Lett 388: 81-85.
83. Walmod PS, Skladchikova G., Kawa A., Berezin V., Bock E. 1999. Antiepileptic teratogen valproic acid (VPA) modulates organisation and dynamics of the actin cytoskeleton. Cell Motil Cytoskeleton 42: 241-255.
84. Wang L., Wang X., Yuan J., Xi Z., Xue T., Li Y., Xiao Z. 2008. Nestin in the temporal neocortex of the intractable epilepsy patients. Neurochem Res. Epub ahead of print.
85. Wang Y., Baraban SC 2007. Granule cell dispersion and aberrant neurogenesis in the adult hippocampus of an LIS1 mutant mouse. Dev Neurosci 29: 91-98.
86. Wang Y., Baraban SC 2008. Aberrant dentate gyrus cytoarchitecture and fiber lamination in Lis1 mutant mice. Hippocampus 18: 758-765.
87. Williams SN, Locke CJ, Braden AL, Caldwell KA, Caldwell GA 2004. Epileptic-like convulsions associated with LIS-1 in the cytoskeletal control of neurotransmitter signaling in Caenorhabditis elegans. Hum Mol Genet 13: 2043-2059.
88. Witte H., Bradke F. 2008. The role of the cytoskeleton during neuronal polarization. Curr Opin Neurbiol 18: 479-487.
89. Wong M. 2008. Stabilizing dendritic structure as a novel therapeutic approach for epilepsy. Expert Rev Neurother 8: 907-915.
90. Xia CH, Roberts EA, Her LS, Liu X., Williams DS, Cleveland DW, Goldstein LS 2003. Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J Cell Biol 161: 55-66.
91. Xiao F., Wang XF, Li JM, Xi ZQ, Lu Y., Wang L., and others. 2008. Overexpression of N-WASP in the brain of human epilepsy. Brain Res 1233: 168-175.
92. Yamada M., Toba S., Yoshida Y., Haratani K., Mori D., Yano Y., and others. 2008. LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J 27: 2471-2483.
93. Yamauchi J., Miyamoto Y., Kusakawa S., Torii T., Mizutani R., Sanbe A., and others. 2008. Neurofibromatosis 2 tumor suppressor, the gene induced by valproic acid, mediates neurite outgrowth through interaction with paxillin. Exp Cell Res 314: 2279-2288.
94. Yang JW, Czech T., Felizardo M., Baumgartner C., Lubec G. 2006. Aberrant expression of cytoskeleton proteins in hippocampus from patients with mesial temporal lobe epilepsy. Amino Acids 30: 477-493.
95. Yu W., Qiang L., Solowska JM, Karabay A., Korulu S., Baas PW 2008. The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19: 1485-1498.
96. Zeng LH, Xu L., Rensing NR, Sinatra PM, Rothman SM, Wong M. 2007. Kainate seizures cause acute dendritic injury and actin depolymerisation in vivo. J Neurosci 27: 11604-11613.