A systems level, functional genomics analysis of chronic epilepsy

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Winden, Kellen D ^a,b   Karsten, Stanislav L ^b,e   Bragin, Anatol ^a,b   Kudo, Lili C ^b,d   Gehman, Lauren ^a   Ruidera, Josephine ^b   Geschwind, Daniel H ^a,b,c   Engel Jr , Jerome ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NeuroInDx Inc   (United States)

^e HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN PROTEIN; ETIRACETAM; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR13; PROTEIN SV2A; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BDNF GENE; BIOINFORMATICS; BRAIN REGION; CELL MIGRATION; CELL PROTECTION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DRUG MECHANISM; DRUG TARGETING; EPILEPSY; EXPERIMENTAL DESIGN; FUNCTIONAL GENOMICS; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENETIC ASSOCIATION; GENOME ANALYSIS; GLIA CELL; HIPPOCAMPUS; KCNJ13 GENE; MALE; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROMOTER REGION; PROTEIN RNA BINDING; RAT; SV2A GENE; SYNAPSE VESICLE; UPREGULATION; ANIMAL; CHRONIC DISEASE; DISEASE MODEL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; GENOME; GENOMICS; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NERVE CELL; PATHOLOGY; PHENOTYPE; SEIZURE; SYSTEMS BIOLOGY; WISTAR RAT;

RATTUS;

ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; EPILEPSY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENETIC ASSOCIATION STUDIES; GENOME; GENOMICS; MALE; MOLECULAR SEQUENCE ANNOTATION; NEURONS; OXIDATIVE STRESS; PHENOTYPE; RATS; RATS, WISTAR; SEIZURES; SYNAPTIC VESICLES; SYSTEMS BIOLOGY; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 79958818494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020763     Document Type: Article

References (77)

1. Engel J Jr, (1996) Introduction to temporal lobe epilepsy. Epilepsy Res 26: 141-150.
2. Dudek FE, Sutula TP, (2007) Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res 163: 755-773.
3. Noebels JL, (2003) The biology of epilepsy genes. Annu Rev Neurosci 26: 599-625.
4. Kalachikov S, Evgrafov O, Ross B, Winawer M, Barker-Cummings C, et al. (2002) Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nat Genet 30: 335-341.
5. Hedera P, Blair MA, Andermann E, Andermann F, D'Agostino D, et al. (2007) Familial mesial temporal lobe epilepsy maps to chromosome 4q13.2-q21.3. Neurology 68: 2107-2112.
6. Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK, (1995) The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118 (Pt 1): 105-118.
7. Ottman R, (1989) Genetics of the partial epilepsies: a review. Epilepsia 30: 107-111.
8. Ottman R, Annegers JF, Hauser WA, Kurland LT, (1989) Seizure risk in offspring of parents with generalized versus partial epilepsy. Epilepsia 30: 157-161.
9. Pitkanen A, Kharatishvili I, Narkilahti S, Lukasiuk K, Nissinen J, (2005) Administration of diazepam during status epilepticus reduces development and severity of epilepsy in rat. Epilepsy Res 63: 27-42.
10. Lukasiuk K, Pirttila TJ, Pitkanen A, (2002) Upregulation of cystatin C expression in the rat hippocampus during epileptogenesis in the amygdala stimulation model of temporal lobe epilepsy. Epilepsia 43 (Suppl 5): 137-145.
11. Potschka H, Krupp E, Ebert U, Gumbel C, Leichtlein C, et al. (2002) Kindling-induced overexpression of Homer 1A and its functional implications for epileptogenesis. Eur J Neurosci 16: 2157-2165.
12. Gorter JA, van Vliet EA, Aronica E, Breit T, Rauwerda H, et al. (2006) Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J Neurosci 26: 11083-11110.
13. Bragin A, Engel J Jr, Wilson CL, Vizentin E, Mathern GW, (1999) Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia 40: 1210-1221.
14. Mathern GW, Cifuentes F, Leite JP, Pretorius JK, Babb TL, (1993) Hippocampal EEG excitability and chronic spontaneous seizures are associated with aberrant synaptic reorganization in the rat intrahippocampal kainate model. Electroencephalogr Clin Neurophysiol 87: 326-339.
15. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
16. Zhang B, Horvath S, (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4: Article17.
17. Oldham MC, Konopka G, Iwamoto K, Langfelder P, Kato T, et al. (2008) Functional organization of the transcriptome in human brain. Nat Neurosci 11: 1271-1282.
18. Winden KD, Oldham MC, Mirnics K, Ebert PJ, Swan CH, et al. (2009) The organization of the transcriptional network in specific neuronal classes. Mol Syst Biol 5: 291.
19. Langfelder P, Zhang B, Horvath S, (2008) Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 24: 719-720.
20. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, et al. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28: 264-278.
21. Choe SE, Boutros M, Michelson AM, Church GM, Halfon MS, (2005) Preferred analysis methods for Affymetrix GeneChips revealed by a wholly defined control dataset. Genome Biol 6: R16.
22. Konopka G, Bomar JM, Winden K, Coppola G, Jonsson ZO, et al. (2009) Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 462: 213-217.
23. Geschwind DH, Ou J, Easterday MC, Dougherty JD, Jackson RL, et al. (2001) A genetic analysis of neural progenitor differentiation. Neuron 29: 325-339.
24. Engel J Jr, Bragin A, Staba R, Mody I, (2009) High-frequency oscillations: what is normal and what is not? Epilepsia 50: 598-604.
25. Calvo JL, Carbonell AL, Boya J, (1991) Co-expression of glial fibrillary acidic protein and vimentin in reactive astrocytes following brain injury in rats. Brain Res 566: 333-336.
26. Oldham MC, Horvath S, Geschwind DH, (2006) Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci U S A 103: 17973-17978.
27. Li W, Kong AN, (2009) Molecular mechanisms of Nrf2-mediated antioxidant response. Mol Carcinog 48: 91-104.
28. Hubbs AF, Benkovic SA, Miller DB, O'Callaghan JP, Battelli L, et al. (2007) Vacuolar leukoencephalopathy with widespread astrogliosis in mice lacking transcription factor Nrf2. Am J Pathol 170: 2068-2076.
29. Faundez V, Horng JT, Kelly RB, (1997) ADP ribosylation factor 1 is required for synaptic vesicle budding in PC12 cells. J Cell Biol 138: 505-515.
30. Bolognani F, Tanner DC, Nixon S, Okano HJ, Okano H, et al. (2007) Coordinated expression of HuD and GAP-43 in hippocampal dentate granule cells during developmental and adult plasticity. Neurochem Res 32: 2142-2151.
31. Bolognani F, Contente-Cuomo T, Perrone-Bizzozero NI, (2010) Novel recognition motifs and biological functions of the RNA-binding protein HuD revealed by genome-wide identification of its targets. Nucleic Acids Res 38: 117-130.
32. Deschenes-Furry J, Perrone-Bizzozero N, Jasmin BJ, (2006) The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. Bioessays 28: 822-833.
33. Bolognani F, Perrone-Bizzozero NI, (2008) RNA-protein interactions and control of mRNA stability in neurons. J Neurosci Res 86: 481-489.
34. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
35. Zhu H, Zhou HL, Hasman RA, Lou H, (2007) Hu proteins regulate polyadenylation by blocking sites containing U-rich sequences. J Biol Chem 282: 2203-2210.
36. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, et al. (2006) Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 9: 99-107.
37. Burger C, Lopez MC, Baker HV, Mandel RJ, Muzyczka N, (2008) Genome-wide analysis of aging and learning-related genes in the hippocampal dentate gyrus. Neurobiol Learn Mem 89: 379-396.
38. Lynch BA, Lambeng N, Nocka K, Kensel-Hammes P, Bajjalieh SM, et al. (2004) The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci U S A 101: 9861-9866.
39. Li A, Horvath S, (2007) Network neighborhood analysis with the multi-node topological overlap measure. Bioinformatics 23: 222-231.
40. Benesch S, Lommel S, Steffen A, Stradal TE, Scaplehorn N, et al. (2002) Phosphatidylinositol 4,5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J Biol Chem 277: 37771-37776.
41. Murshid A, Srivastava A, Kumar R, Presley JF, (2006) Characterization of the localization and function of NECAP 1 in neurons. J Neurochem 98: 1746-1762.
42. Lukasiuk K, Pitkanen A, (2004) Large-scale analysis of gene expression in epilepsy research: is synthesis already possible? Neurochem Res 29: 1169-1178.
43. Curran T, Morgan JI, (1995) Fos: an immediate-early transcription factor in neurons. J Neurobiol 26: 403-412.
44. Watanabe Y, Johnson RS, Butler LS, Binder DK, Spiegelman BM, et al. (1996) Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy. J Neurosci 16: 3827-3836.
45. Zhang J, Zhang D, McQuade JS, Behbehani M, Tsien JZ, et al. (2002) c-fos regulates neuronal excitability and survival. Nat Genet 30: 416-420.
46. Shetty AK, Zaman V, Shetty GA, (2003) Hippocampal neurotrophin levels in a kainate model of temporal lobe epilepsy: a lack of correlation between brain-derived neurotrophic factor content and progression of aberrant dentate mossy fiber sprouting. J Neurochem 87: 147-159.
47. Liu H, Mazarati AM, Katsumori H, Sankar R, Wasterlain CG, (1999) Substance P is expressed in hippocampal principal neurons during status epilepticus and plays a critical role in the maintenance of status epilepticus. Proc Natl Acad Sci U S A 96: 5286-5291.
48. Keating GL, Kuhar MJ, Rye DB, (2008) High dose CART peptide induces abnormal EEG activity and behavioral seizures. Neuropeptides 42: 199-204.
49. Hattiangady B, Shetty AK, (2009) Decreased neuronal differentiation of newly generated cells underlies reduced hippocampal neurogenesis in chronic temporal lobe epilepsy. Hippocampus.
50. Hattiangady B, Shetty AK, (2008) Implications of decreased hippocampal neurogenesis in chronic temporal lobe epilepsy. Epilepsia 49 (Suppl 5): 26-41.
51. Kraft AD, Lee JM, Johnson DA, Kan YW, Johnson JA, (2006) Neuronal sensitivity to kainic acid is dependent on the Nrf2-mediated actions of the antioxidant response element. J Neurochem 98: 1852-1865.
52. Jarrett SG, Liang LP, Hellier JL, Staley KJ, Patel M, (2008) Mitochondrial DNA damage and impaired base excision repair during epileptogenesis. Neurobiol Dis 30: 130-138.
53. Liang LP, Patel M, (2004) Mitochondrial oxidative stress and increased seizure susceptibility in Sod2(-/+) mice. Free Radic Biol Med 36: 542-554.
54. Patel M, (2004) Mitochondrial dysfunction and oxidative stress: cause and consequence of epileptic seizures. Free Radic Biol Med 37: 1951-1962.
55. Trotti D, Danbolt NC, Volterra A, (1998) Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol Sci 19: 328-334.
56. Arabadzisz D, Antal K, Parpan F, Emri Z, Fritschy JM, (2005) Epileptogenesis and chronic seizures in a mouse model of temporal lobe epilepsy are associated with distinct EEG patterns and selective neurochemical alterations in the contralateral hippocampus. Exp Neurol 194: 76-90.
57. Kim DS, Kwak SE, Kim JE, Won MH, Choi HC, et al. (2005) Bilateral enhancement of excitation via up-regulation of vesicular glutamate transporter subtype 1, not subtype 2, immunoreactivity in the unilateral hypoxic epilepsy model. Brain Res 1055: 122-130.
58. Hovorka J, Langmeier M, Mares P, Koryntova H, (1997) Synaptic vesicle size and shape profile in the kindling model of epileptogenesis. Epilepsy Res 28: 225-231.
59. Goussakov IV, Fink K, Elger CE, Beck H, (2000) Metaplasticity of mossy fiber synaptic transmission involves altered release probability. J Neurosci 20: 3434-3441.
60. Heuvingh J, Franco M, Chavrier P, Sykes C, (2007) ARF1-mediated actin polymerization produces movement of artificial vesicles. Proc Natl Acad Sci U S A 104: 16928-16933.
61. Faundez V, Horng JT, Kelly RB, (1998) A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93: 423-432.
62. Zhu Y, Xu J, Heinemann SF, (2009) Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron 61: 397-411.
63. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, et al. (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51: 71-84.
64. Salazar G, Craige B, Wainer BH, Guo J, De Camilli P, et al. (2005) Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol Biol Cell 16: 3692-3704.
65. Scheuber A, Rudge R, Danglot L, Raposo G, Binz T, et al. (2006) Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc Natl Acad Sci U S A 103: 16562-16567.
66. Westmark CJ, Gourronc FA, Bartleson VB, Sayin U, Bhattacharya S, et al. (2005) HuR mRNA ligands expressed after seizure. J Neuropathol Exp Neurol 64: 1037-1045.
67. Bolognani F, Qiu S, Tanner DC, Paik J, Perrone-Bizzozero NI, et al. (2007) Associative and spatial learning and memory deficits in transgenic mice overexpressing the RNA-binding protein HuD. Neurobiol Learn Mem 87: 635-643.
68. Tanner DC, Qiu S, Bolognani F, Partridge LD, Weeber EJ, et al. (2008) Alterations in mossy fiber physiology and GAP-43 expression and function in transgenic mice overexpressing HuD. Hippocampus 18: 814-823.
69. Edwalds-Gilbert G, Veraldi KL, Milcarek C, (1997) Alternative poly(A) site selection in complex transcription units: means to an end? Nucleic Acids Res 25: 2547-2561.
70. An JJ, Gharami K, Liao GY, Woo NH, Lau AG, et al. (2008) Distinct role of long 3′ UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134: 175-187.
71. Crowder KM, Gunther JM, Jones TA, Hale BD, Zhang HZ, et al. (1999) Abnormal neurotransmission in mice lacking synaptic vesicle protein 2A (SV2A). Proc Natl Acad Sci U S A 96: 15268-15273.
72. Chang WP, Sudhof TC, (2009) SV2 renders primed synaptic vesicles competent for Ca2+-induced exocytosis. J Neurosci 29: 883-897.
73. Albert R, Jeong H, Barabasi AL, (2000) Error and attack tolerance of complex networks. Nature 406: 378-382.
74. Jeong H, Mason SP, Barabasi AL, Oltvai ZN, (2001) Lethality and centrality in protein networks. Nature 411: 41-42.
75. Horvath S, Zhang B, Carlson M, Lu KV, Zhu S, et al. (2006) Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc Natl Acad Sci U S A 103: 17402-17407.
76. Yildirim MA, Goh KI, Cusick ME, Barabasi AL, Vidal M, (2007) Drug-target network. Nat Biotechnol 25: 1119-1126.
77. Bragin A, Azizyan A, Almajano J, Wilson CL, Engel J Jr, (2005) Analysis of chronic seizure onsets after intrahippocampal kainic acid injection in freely moving rats. Epilepsia 46: 1592-1598.