Gene Expression Profiling of a Hypoxic Seizure Model of Epilepsy Suggests a Role for mTOR and Wnt Signaling in Epileptogenesis

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Theilhaber, Joachim ^a   Rakhade, Sanjay N ^b   Sudhalter, Judy ^a   Kothari, Nayantara ^a   Klein, Peter ^c   Pollard, Jack ^a   Jensen, Frances E ^d  

^a MERSI   (United States)

^b GENZYME CORPORATION   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; CASEIN KINASE IALPHA; CD24 ANTIGEN; CYCLIN A2; DOUBLECORTIN; MAMMALIAN TARGET OF RAPAMYCIN; MINICHROMOSOME MAINTENANCE PROTEIN; MYC PROTEIN; NESTIN; NEUROFILAMENT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN HOMER 1; SOMATOMEDIN C; SYNAPSIN II; SYNAPTOBREVIN 1; VESICULAR GLUTAMATE TRANSPORTER 1; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APC GENE; ARTICLE; BETA CATENIN GENE; CASEIN KINASE 1 ALPHA GENE; CELL MATURATION; CONTROLLED STUDY; CYCLIN A2 GENE; DISEASE MODEL; DOWN REGULATION; ENZYME ACTIVATION; EPILEPTOGENESIS; GENE; GENE ACTIVITY; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GSK3B GENE; HYPOXIA; INTRACELLULAR SIGNALING; MBP GENE; MCM GENE; MOG GENE; MOLECULAR PATHOLOGY; MYCN GENE; NEFH GENE; NERVE CELL PLASTICITY; NFGB GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE MYC; PROTEIN FUNCTION; RAT; SEIZURE; STRUCTURAL GENE; TRANSCRIPTION REGULATION; UPREGULATION; WNT GENE;

ANIMALS; ANOXIA; BIOLOGICAL MARKERS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NEUROGENESIS; NEURONS; OLIGODENDROGLIA; ORGAN SPECIFICITY; QUINOXALINES; RATS; SEIZURES; TIME FACTORS; TOR SERINE-THREONINE KINASES; WNT SIGNALING PATHWAY;

EID: 84884680241     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074428     Document Type: Article

References (73)

1. Das N, Dhanawat M, Shrivastava SK, (2012) An overview on antiepileptic drugs. Drug Discov Ther 6: 178-93.
2. Löscher W, Schmidt D, (2004) New horizons in the development of antiepileptic drugs: the search for new targets. Epilepsy Res 60: 77-159.
3. 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: 2218-27.
4. Newton SS, Collier EF, Hunsberger J, Adams D, Terwilliger R, et al. (2003) Gene profile of electroconvulsive seizures: induction of neurotrophic and angiogenic factors. J Neurosci 23: 10841-51.
5. 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.
6. Hendriksen H, Datson NA, Ghijsen WE, van Vliet EA, da Silva FH, et al. (2001) Altered hippocampal gene expression prior to the onset of spontaneous seizures in the rat post-status epilepticus model. Eur J Neurosci 14: 1475-84.
7. Borges K, Shaw R, Dingledine R, (2007) Gene expression changes after seizure preconditioning in the three major hippocampal cell layers. Neurobiol Dis 26: 66-77.
8. Morimoto K, Fahnestock M, Racine RJ, (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73: 1-60.
9. Lukasiuk K, Dabrowski M, Adach A, Pitkänen A, (2006) Epileptogenesis-related genes revisited. Prog Brain Res 158: 223-41.
10. Winden KD, Karsten SL, Bragin A, Kudo LC, Gehman L, et al. (2011) A systems level, functional genomics analysis of chronic epilepsy. PLoS One 6: e20763.
11. Laurén HB, Lopez-Picon FR, Brandt AM, Rios-Rojas CJ, Holopainen IE, (2010) Transcriptome analysis of the hippocampal CA1 pyramidal cell region after kainic acid-induced status epilepticus in juvenile rats. PLoS One 5: e10733.
12. Okamoto OK, Janjoppi L, Bonone FM, Pansani AP, da Silva AV, et al. (2010) Whole transcriptome analysis of the hippocampus: toward a molecular portrait of epileptogenesis. BMC Genomics 11: 230.
13. Jensen FE, Applegate CD, Holtzman D, Belin TR, Burchfiel JL, (1991) Epileptogenic effect of hypoxia in the immature rodent brain. Ann Neurol 29: 629-37.
14. Jensen FE, Wang C, Stafstrom CE, Liu Z, Geary C, et al. (1998) Acute and chronic increases in excitability in rat hippocampal slices after perinatal hypoxia In vivo. J Neurophysiol 79: 73-81.
15. Rakhade SN, Klein PM, Huynh T, Hilario-Gomez C, Kosaras B, et al. (2011) Development of later life spontaneous seizures in a rodent model of hypoxia-induced neonatal seizures. Epilepsia 52: 753-65.
16. Jensen FE, Blume H, Alvarado S, Firkusny I, Geary C, (1995) NBQX blocks acute and late epileptogenic effects of perinatal hypoxia. Epilepsia 36: 966-72.
17. Koh S, Tibayan FD, Simpson JN, Jensen FE, (2004) NBQX or topiramate treatment after perinatal hypoxia-induced seizures prevents later increases in seizure-induced neuronal injury. Epilepsia 45: 569-75.
18. Talos DM, Sun H, Zhou X, Fitzgerald EC, Jackson MC, et al. (2012) The Interaction between Early Life Epilepsy and Autistic-Like Behavioral Consequences: A Role for the Mammalian Target of Rapamycin (mTOR) Pathway. PLoS One 7: e35885.
19. Gene Expression Omnibus website. Available: http://www.ncbi.nlm.nih.gov/geo/. Accessed 2013 August 21.
20. Knoepfler PS, Kenney AM, (2006) Shh signaling regulates neural precursor cell cycle progression through N-Myc. Cell Cycle 5: 47-52.
21. Allen Brain Atlas website. Available: http://www.brain-map.org/. Accessed 2013 Aug 21.
22. Bayer SA, Altman J (1991) Neocortical Development. New York: Raven Press.
23. Rakhade SN, Zhou C, Aujla PK, Fishman R, Sucher NJ, et al. (2008) Early alterations of AMPA receptors mediate synaptic potentiation induced by neonatal seizures. J Neurosci 28: 7979-90.
24. Maguschak KA, Ressler KJ, (2012) The dynamic role of beta-catenin in synaptic plasticity. Neuropharmacology 62: 78-88.
25. Maguschak KA, Ressler KJ, (2011) Wnt signaling in amygdala-dependent learning and memory. J Neurosci 31: 13057-67.
26. Nuriya M, Huganir RL, (2006) Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem 97: 652-61.
27. GeneSigDb website. Available: http://compbio.dfci.harvard.edu/genesigdb/. Accessed 2013 Aug 21.
28. Baljinnyam B, Klauzinska M, Saffo S, Callahan R, Rubin JS, (2012) Recombinant R-spondin2 and Wnt3a up- and down-regulate novel target genes in C57MG mouse mammary epithelial cells. PLOS One 7: e29455.
29. Zeng LH, Rensing NR, Wong M, (2009) The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J Neurosci. 29: 6964-72.
30. Wong M, (2010) Mammalian target of rapamycin (mTOR) inhibition as a potential antiepileptogenic therapy: From tuberous sclerosis to common acquired epilepsies. Epilepsia 51: 27-36.
31. Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M, (2005) Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. J Neurosci 25: 11300-12.
32. Horwood JM, Dufour F, Laroche S, Davis S, (2006) Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur J Neurosci 23: 3375-84.
33. Jaworski J, Sheng M, (2006) The growing role of mTOR in neuronal development and plasticity. Mol Neurobiol 34: 205-19.
34. Zheng WH, Quirion R, (2004) Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J Neurochem 89: 844-52.
35. Tropea D, Kreiman G, Lyckman A, Mukherjee S, Yu H, et al. (2006) Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat Neurosci 9: 660-8.
36. Yoshii A, Constantine-Paton M, (2007) BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 10: 702-11.
37. Cuesto G, Enriquez-Barreto L, Caramés C, Cantarero M, Gasull X, et al. (2011) Phosphoinositide-3-kinase activation controls synaptogenesis and spinogenesis in hippocampal neurons. J Neurosci 31: 2721-33.
38. Lee CC, Huang CC, Hsu KS, (2011) Insulin promotes dendritic spine and synapse formation by the PI3K/Akt/mTOR and Rac1 signaling pathways. Neuropharmacology 61: 867-79.
39. Kelly A, Lynch MA (2000) Long-term potentiation in dentate gyrus of the rat is inhibited by the phosphoinositide 3-kinase inhibitor, wortmannin. Neuropharmacology 39, 643-651.
40. Opazo P, Watabe AM, Grant SG, O'Dell TJ, (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23: 3679-88.
41. Yang PC, Yang CH, Huang CC, Hsu KS, (2008) Phosphatidylinositol 3-kinase activation is required for stress protocol-induced modification of hippocampal synaptic plasticity. J Biol Chem 283: 2631-43.
42. Sui L, Wang J, Li BM, (2008) Role of the phosphoinositide 3-kinase-Akt-mammalian target of the rapamycin signaling pathway in long-term potentiation and trace fear conditioning memory in rat medial prefrontal cortex. Learn Mem 15: 762-76.
43. Yu X, Malenka RC, (2003) Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6: 1169-77.
44. Murase S, Mosser E, Schuman EM, (2002) Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35: 91-105.
45. Chen J, Park CS, Tang SJ, (2006) Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J Biol Chem 281: 11910-6.
46. Madsen TM, Newton SS, Eaton ME, Russell DS, Duman RS, (2003) Chronic electroconvulsive seizure up-regulates beta-catenin expression in rat hippocampus: role in adult neurogenesis. Biol Psychiatry 54: 1006-14.
47. Zhang B, Wong M, (2012) Pentylenetetrazole-induced seizures cause acute, but not chronic, mTOR pathway activation in rat. Epilepsia 53: 506-11.
48. Buckmaster PS, Ingram EA, Wen X, (2009) Inhibition of the mammalian target of rapamycin signaling pathway suppresses dentate granule cell axon sprouting in a rodent model of temporal lobe epilepsy. J Neurosci 29: 8259-69.
49. Huang X, Zhang H, Yang J, Wu J, McMahon J, et al. (2010) Pharmacological inhibition of the mammalian target of rapamycin pathway suppresses acquired epilepsy. Neurobiol Dis 40: 193-9.
50. Zeng LH, Xu L, Gutmann DH, Wong M, (2008) Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Annals Neur 63: 444-453.
51. Zeng LH, McDaniel S, Rensing NR, Wong M, (2010) Regulation of cell death and epileptogenesis by the mammalian target of rapamycin (mTOR): a double-edged sword? Cell Cycle 9: 2281-5.
52. Tavazoie SF, Alvarez VA, Ridenour DA, Kwiatkowski DJ, Sabatini BL, (2005) Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat Neurosci 8: 1727-34.
53. Bateup HS, Takasaki KT, Saulnier JL, Denefrio CL, Sabatini BL, (2011) Loss of Tsc1 in vivo impairs hippocampal mGluR-LTD and increases excitatory synaptic function. J Neurosci 31: 8862-9.
54. Zeng LH, Rensing NR, Wong M, (2009) Developing Antiepileptogenic Drugs for Acquired Epilepsy: Targeting the Mammalian Target of Rapamycin (mTOR) Pathway. Mol Cell Pharmacol 1: 124-129.
55. McDaniel SS, Wong M, (2011) Therapeutic role of mammalian target of rapamycin (mTOR) inhibition in preventing epileptogenesis. Neurosci Lett 497: 231-9.
56. Everolimus (RAD001) Therapy for Epilepsy in Patients With Tuberous Sclerosis Complex (TSC). http://ClinicalTrials.gov NCT01070316.
57. (2012).A Placebo-controlled Study of Efficacy & Safety of 2 Trough-ranges of Everolimus as Adjunctive Therapy in Patients With Tuberous Sclerosis Complex (TSC) & Refractory Partial-onset Seizures (EXIST-3). http://ClinicalTrials.gov NCT01713946.
58. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, et al. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461: 614-20.
59. Chen B, Dodge ME, Tang W, Lu J, Ma Z, et al. (2009) Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 5: 100-7.
60. Gould TD, Manji HK, (2002) The Wnt signaling pathway in bipolar disorder. Neuroscientist 8: 497-511.
61. Affymetrix HT Rat Focus Array [HT_Rat-Focus] website. http://www.affymetrix.com/support/technical/byproduct.affx?product=ht_rat-focus_set. Accessed 2013 Aug 21.
62. Affymetrix Statistical Algorithms Description Document (2002) Website http://media.affymetrix.com/support/technical/whitepapers/sadd_whitepaper.pdf.Accessed 2013 Aug 21.
63. Theilhaber J, Ulyanov A, Malanthara A, Cole J, Xu D, et al. (2004) GECKO: a complete large-scale gene expression analysis platform. BMC Bioinformatics 5: 195.
64. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Website http://www.R-project.org. Accessed 2013 Aug 21.
65. Theilhaber J, Bushnell S, Jackson A, Fuchs R, (2001) Bayesian estimation of fold-changes in the analysis of gene expression: the PFOLD algorithm. J Comput Biol 8: 585-614.
66. Keeping ES (1995) Introduction to Statistical Inference. New York:Dover, New York. p. 256.
67. 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: 15545-50.
68. National Library of Medicine website. Available: http://www.ncbi.nlm.nih.gov/pubmed. Accessed 2013 Aug 21.
69. Broad Institute Molecular Signatures Database v3.0 website. Available: http://www.broadinstitute.org/gsea/msigdb/index.jsp. Accessed 2013 Aug 21.
70. The Gene Ontology website. Available: http://www.geneontology.org/. Accessed 2013 Aug 21.
71. Connectivity Map 02, Broad Institute (2012). Available: http://www.broadinstitute.org/cmap/.
72. NextBio analysis platform website. Available: http://www.nextbio.com. Accessed 2013 Aug 21.
73. Haberman RP, Lee HJ, Colantuoni C, Koh MT, Gallagher M, (2008) Rapid encoding of new information alters the profile of plasticity-related mRNA transcripts in the hippocampal CA3 region. Proc Natl Acad Sci U S A 105: 10601-6.