Spontaneous seizures and altered gene expression in GABA signaling pathways in a mind bomb mutant zebrafish

Journal of Neuroscience

Volumn 30, Issue 41, 2010, Pages 13718-13728

  Hortopan, Gabriela A ^a   Dinday, Matthew T ^a   Baraban, Scott C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; MIND BOMB PROTEIN, ZEBRAFISH; UBIQUITIN PROTEIN LIGASE; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL METABOLISM; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EMBRYO; FEMALE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; IN SITU HYBRIDIZATION; MALE; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEIZURE; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; BRAIN; DNA MICROARRAY; ELECTROPHYSIOLOGY; GENETICS; METABOLISM; MOTOR ACTIVITY; NERVE CELL; PATHOPHYSIOLOGY; PHENOTYPE;

ANIMALS; BRAIN; ELECTROPHYSIOLOGY; FEMALE; GAMMA-AMINOBUTYRIC ACID; IN SITU HYBRIDIZATION; MALE; MOTOR ACTIVITY; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; SEIZURES; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77958050908     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1887-10.2010     Document Type: Article

References (91)

1. Akbarian S, Huang HS (2006) Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res Rev 52:293-304. (Pubitemid 44291805)
2. Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64:5245-5250.
3. Baraban SC, Hollopeter G, Erickson JC, Schwartzkroin PA, Palmiter RD (1997) Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J Neurosci 17:8927-8936.
4. Baraban SC, Taylor MR, Castro PA, Baier H (2005) Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131:759-768.
5. Baraban SC, Dinday MT, Castro PA, Chege S, Guyenet S, Taylor MR (2007) A large-scale mutagenesis screen to identify seizure-resistant zebrafish. Epilepsia 48:1151-1157.
6. Batista-Brito R, Machold R, Klein C, Fishell G (2008) Gene expression in cortical interneuron precursors is prescient of their mature function. Cereb Cortex 18:2306-2317.
7. Berghmans S, Hunt J, Roach A, Goldsmith P (2007) Zebrafish offer the potential for a primary screen to identify a wide variety of potential anticonvulsants. Epilepsy Res 75:18-28.
8. Bingham S, Chaudhari S, Vanderlaan G, Itoh M, Chitnis A, Chandrasekhar A (2003) Neurogenic phenotype of mind bomb mutants leads to severe patterning defects in the zebrafish hindbrain. Dev Dyn 228:451-463.
9. Blader P, Strähle U (2000) Zebrafish developmental genetics and central nervous system development. Hum Mol Genet 9:945-951. (Pubitemid 30216106)
10. Brooks-Kayal AR, Raol YH, Russek SJ (2009) Alteration of epileptogenesis genes. Neurotherapeutics 6:312-318.
11. Camprubí C, Guitart M, Gabau E, Coll MD, Villatoro S, Oltra S, Roselló M, Ferrer I, Monfort S, Orellana C, Martínez F (2009) Novel UBE3A mutations causing Angelman syndrome: different parental origin for single nucleotide changes and multiple nucleotide deletions or insertions. Am J Med Genet A 149A:343-348.
12. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical non-pyramidal cells. J Neurosci 17:3894-3906.
13. Chen W, Casey Corliss D (2004) Three modules of zebrafish Mind bomb work cooperatively to promote Delta ubiquitination and endocytosis. Dev Biol 267:361-373.
14. Chen YC, Kao SC, Chou HC, Lin WH, Wong FH, Chow WY (2008) A real-time PCR method for the quantitative analysis of RNA editing at specific sites. Anal Biochem 375:46-52.
15. Chitnis A, Henrique D, Lewis J, Ish-Horowicz D, Kintner C (1995) Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375:761-766.
16. Clayton-Smith J, Laan L (2003) Angelman syndrome: a review of the clinical and genetic aspects. J Med Genet 40:87-95.
17. Cowansage KK, LeDoux JE, Monfils MH (2010) Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 3:12-29.
18. Croll SD, Chesnutt CR, Greene NA, Lindsay RM, Wiegand SJ (1999) Peptide immunoreactivity in aged rat cortex and hippocampus as a function of memory and BDNF infusion. Pharmacol Biochem Behav 64:625-635.
19. de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossant J, Conlon RA (1997) Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124:1139-1148.
20. Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399-434.
21. Edwards JG, Michel WC (2002) Odor-stimulated glutamatergic neurotransmission in the zebrafish olfactory bulb. J Comp Neurol 454:294-309.
22. Edwards JG, Michel WC (2003) Pharmacological characterization of ionotropic glutamate receptors in the zebrafish olfactory bulb. Neuroscience 122:1037-1047.
23. Ekker SC (2000) Morphants: a new systematic vertebrate functional genomics approach. Yeast 17:302-306.
24. Ekström P, Reschke M, Steinbusch H, van Veen T (1986) Distribution of noradrenaline in the brain of the teleost Gasterosteus aculeatus L.: an immunohistochemical analysis. J Comp Neurol 254:297-313.
25. Elliott RC, Khademi S, Pleasure SJ, Parent JM, Lowenstein DH (2001) Differential regulation of basic helix-loop-helix mRNAs in the dentate gyrus following status epilepticus. Neuroscience 106:79-88.
26. Elliott RC, Miles MF, Lowenstein DH (2003) Overlapping microarray profiles of dentate gyrus gene expression during development-and epilepsy-associated neurogenesis and axon outgrowth. J Neurosci 23:2218-2227.
27. Engel J Jr (2006) ILAE classification of epilepsy syndromes. Epilepsy Res 70 [Suppl 1]:S5-S10.
28. Fatemi SH, Reutiman TJ, Folsom TD, Thuras PD (2009) GABA(A) receptor downregulation in brains of subjects with autism. J Autism Dev Disord 39:223-230.
29. Flood WD, Moyer RW, Tsykin A, Sutherland GR, Koblar SA (2004) Nxf and Fbxo33: novel seizure-responsive genes in mice. Eur J Neurosci 20:1819-1826.
30. Glessner JT, Wang K, Cai G, Korvatska O, Kim CE, Wood S, Zhang H, Estes A, Brune CW, Bradfield JP, Imielinski M, Frackelton EC, Reichert J, Crawford EL, Munson J, Sleiman PM, Chiavacci R, Annaiah K, Thomas K, Hou C, et al. (2009) Autism genome-wide copy number variation reveals ubiquitin and neuronal genes. Nature 459:569-573.
31. Golling G, Amsterdam A, Sun Z, Antonelli M, Maldonado E, Chen W, Burgess S, Haldi M, Artzt K, Farrington S, Lin SY, Nissen RM, Hopkins N (2002) Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat Genet 31:135-140.
32. Gorter JA, van Vliet EA, Aronica E, Breit T, Rauwerda H, Lopes da Silva FH, Wadman WJ (2006) Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J Neurosci 26:11083-11110.
33. Guerrini R, Marini C (2006) Genetic malformations of cortical development. Exp Brain Res 173:322-333.
34. Guo S, Brush J, Teraoka H, Goddard A, Wilson SW, Mullins MC, Rosenthal A (1999) Development of noradrenergic neurons in the zebrafish hindbrain requires BMP, FGF8, and the homeodomain protein soulless/Phox2a. Neuron 24:555-566.
35. Halpern ME, Rhee J, Goll MG, Akitake CM, Parsons M, Leach SD (2008) Gal4/UAS transgenic tools and their application to zebrafish. Zebrafish 5:97-110.
36. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10:40-68; image 45.
37. Hauptmann G, Gerster T (1994) Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet 10:266.
38. Hegde A, Qiu NC, Qiu X, Ho SH, Tay KQ, George J, Ng FS, Govindarajan KR, Gong Z, Mathavan S, Jiang YJ (2008) Genomewide expression analysis in zebrafish mind bomb alleles with pancreas defects of different severity identifies putative Notch responsive genes. PLoS One 3:e1479.
39. Hendriksen H, Datson NA, Ghijsen WE, van Vliet EA, da Silva FH, Gorter JA, Vreugdenhil E (2001) Altered hippocampal gene expression prior to the onset of spontaneous seizures in the rat post-status epilepticus model. Eur J Neurosci 14:1475-1484. (Pubitemid 35463714)
40. Hewapathirane DS, Dunfield D, Yen W, Chen S, Haas K (2008) In vivo imaging of seizure activity in a novel developmental seizure model. Exp Neurol 211:480-488.
41. Houser CR (1999) Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv Neurol 79:743-761.
42. Hunsberger JG, Bennett AH, Selvanayagam E, Duman RS, Newton SS (2005) Gene profiling the response to kainic acid induced seizures. Brain Res Mol Brain Res 141:95-112.
43. Hwang J, Kim HS, Seok JW, Kim JD, Koun S, Park SY, Lee J, Kim HS, Kim HS, Kim KS, Chang KT, Ryoo ZY, Wang SM, Huh TL, Lee S (2009) Transcriptome analysis of the zebrafish mind bomb mutant. Mol Genet Genomics 281:77-85.
44. Itoh M, Kim CH, Palardy G, Oda T, Jiang YJ, Maust D, Yeo SY, Lorick K, Wright GJ, Ariza-McNaughton L, Weissman AM, Lewis J, Chandrasekharappa SC, Chitnis AB (2003) Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 4:67-82.
45. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, Eichele G, Sweatt JD, Beaudet AL (1998) Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21:799-811.
46. Jiang YJ, Brand M, Heisenberg CP, Beuchle D, Furutani-Seiki M, Kelsh RN, Warga RM, Granato M, Haffter P, Hammerschmidt M, Kane DA, Mullins MC, Odenthal J, van Eeden FJ, Nüsslein-Volhard C (1996) Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123:205-216. (Pubitemid 27056748)
47. Kim CH, Ueshima E, Muraoka O, Tanaka H, Yeo SY, Huh TL, Miki N (1996) Zebrafish elav/ HuC homologue as a very early neuronal marker. Neurosci Lett 216:109-112.
48. Kim YJ, Nam RH, Yoo YM, Lee CJ (2004) Identification and functional evidence of GABAergic neurons in parts of the brain of adult zebrafish (Danio rerio). Neurosci Lett 355:29-32.
49. Kishino T, Lalande M, Wagstaff J (1997) UBE3A/E6-AP mutations cause Angelman syndrome. Nat Genet 15:70-73.
50. Krampfl K, Maljevic S, Cossette P, Ziegler E, Rouleau GA, Lerche H, Bufler J (2005) Molecular analysis of the A322D mutation in the GABA receptor alpha-subunit causing juvenile myoclonic epilepsy. Eur J Neurosci 22:10-20.
51. Kuebler D, Tanouye MA (2000) Modifications of seizure susceptibility in Drosophila. J Neurophysiol 83:998-1009.
52. Lai EC (2002) Protein degradation: four E3s for the notch pathway. Curr Biol 12:R74-R78.
53. Lawrence YA, Kemper TL, Bauman ML, Blatt GJ (2010) Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism. Acta Neurol Scand 121:99-108.
54. Lee J, Wu CF (2002) Electroconvulsive seizure behavior in Drosophila: analysis of the physiological repertoire underlying a stereotyped action pattern in bang-sensitive mutants. J Neurosci 22:11065-11079.
55. Legendre P (2001) The glycinergic inhibitory synapse. Cell Mol Life Sci 58:760-793.
56. Lin C, Spikings E, Zhang T, Rawson D (2009) Housekeeping genes for cryopreservation studies on zebrafish embryos and blastomeres. Theriogenology 71:1147-1155.
57. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
58. Lu Y, Wang F, Li Y, Ferris J, Lee JA, Gao FB (2009) The Drosophila homologue of the Angelman syndrome ubiquitin ligase regulates the formation of terminal dendritic branches. Hum Mol Genet 18:454-462.
59. Mack-Bucher JA, Li J, Friedrich RW (2007) Early functional development of interneurons in the zebrafish olfactory bulb. Eur J Neurosci 25:460-470.
60. Matsuura T, Sutcliffe JS, Fang P, Galjaard RJ, Jiang YH, Benton CS, Rommens JM, Beaudet AL (1997) De novo truncating mutations in E6-AP ubiquitin-protein ligase gene (UBE3A) in Angelman syndrome. Nat Genet 15:74-77.
61. Mellios N, Huang HS, Baker SP, Galdzicka M, Ginns E, Akbarian S (2009) Molecular determinants of dysregulated GABAergic gene expression in the prefrontal cortex of subjects with schizophrenia. Biol Psychiatry 65:1006-1014.
62. Mione M, Baldessari D, Deflorian G, Nappo G, Santoriello C (2008) How neuronal migration contributes to the morphogenesis of the CNS: insights from the zebrafish. Dev Neurosci 30:65-81.
63. Miura K, Kishino T, Li E, Webber H, Dikkes P, Holmes GL, Wagstaff J (2002) Neurobehavioral and electroencephalographic abnormalities in Ube3a maternal-deficient mice. Neurobiol Dis 9:149-159. (Pubitemid 34261211)
64. Muhle R, Trentacoste SV, Rapin I (2004) The genetics of autism. Pediatrics 113:e472-e486.
65. Murakami T, Morita Y, Ito H (1983) Extrinsic and intrinsic fiber connections of the telencephalon in a teleost, Sebastiscus marmoratus. J Comp Neurol 216:115-131.
66. Nam RH, Kim W, Lee CJ (2004) NMDA receptor-dependent long-term potentiation in the telencephalon of the zebrafish. Neurosci Lett 370:248-251.
67. Naumann EA, Kampff AR, Prober DA, Schier AF, Engert F (2010) Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 13:513-520.
68. Orger MB, Smear MC, Anstis SM, Baier H (2000) Perception of Fourier and non-Fourier motion by larval zebrafish. Nat Neurosci 3:1128-1133.
69. Park HC, Appel B (2003) Delta-Notch signaling regulates oligodendrocyte specification. Development 130:3747-3755.
70. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
71. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509-515.
72. Pitkänen A, Schwartzkroin PA, MoshéSL (2006) Models of seizures and epilepsy. Amsterdam: Elsevier Academic.
73. Rakhade SN, Yao B, Ahmed S, Asano E, Beaumont TL, Shah AK, Draghici S, Krauss R, Chugani HT, Sood S, Loeb JA (2005) A common pattern of persistent gene activation in human neocortical epileptic foci. Ann Neurol 58:736-747.
74. Sajovic P, Levinthal C (1983) Inhibitory mechanism in zebrafish optic tectum: visual response properties of tectal cells altered by picrotoxin and bicuculline. Brain Res 271:227-240.
75. Schier AF, Neuhauss SC, Harvey M, Malicki J, Solnica-Krezel L, Stainier DY, Zwartkruis F, Abdelilah S, Stemple DL, Rangini Z, Yang H, Driever W (1996) Mutations affecting the development of the embryonic zebrafish brain. Development 123:165-178. (Pubitemid 27056745)
76. Schwartzkroin PA, Walsh CA (2000) Cortical malformations and epilepsy. Ment Retard Dev Disabil Res Rev 6:268-280.
77. Sloviter RS (1996) Hippocampal pathology and pathophysiology in temporal lobe epilepsy. Neurologia 11 [Suppl 4]:S29-S32.
78. Tang R, Dodd A, Lai D, McNabb WC, Love DR (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin (Shanghai) 39:384-390.
79. Thom M, Martinian L, Parnavelas JG, Sisodiya SM (2004) Distribution of cortical interneurons in grey matter heterotopia in patients with epilepsy. Epilepsia 45:916-923.
80. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680.
81. Vanegas H, Ebbesson SO (1976) Telencephalic projections in two teleost species. J Comp Neurol 165:181-195.
82. van Kammen DP, Petty F, Kelley ME, Kramer GL, Barry EJ, Yao JK, Gurklis JA, Peters JL (1998) GABA and brain abnormalities in schizophrenia. Psychiatry Res 82:25-35.
83. Vezzani A, Sperk G, Colmers WF (1999) Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci 22:25-30.
84. Westerfield M (1993) The zebrafish book: a guide for the laboratory use of zebrafish (Brachydanio rerio). Eugene, OR: Westerfield.
85. 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.
86. Wu Y, Bolduc FV, Bell K, Tully T, Fang Y, Sehgal A, Fischer JA (2008) A Drosophila model for Angelman syndrome. Proc Natl Acad Sci U S A 105:12399-12404.
87. Wullimann MF, Rupp B, Reichert H (1996) Neuroanatomy of the zebrafish brain: a topological atlas. Basel: Birkhäuser Verlag.
88. Xi ZQ, Xiao F, Yuan J, Wang XF, Wang L, Quan FY, Liu GW (2009) Gene expression analysis on anterior temporal neocortex of patients with intractable epilepsy. Synapse 63:1017-1028.
89. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.
90. Yoshimura M, Nishi S (1982) Intracellular recordings from lateral horn cells of the spinal cord in vitro. J Auton Nerv Syst 6:5-11.
91. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406-3415.