Predicting novel histopathological microlesions in human epileptic brain through transcriptional clustering

Brain

Volumn 138, Issue 2, 2015, Pages 356-370

  Dachet, Fabien ^a,b   Bagla, Shruti ^b   Keren Aviram, Gal ^c   Morton, Andrew ^b   Balan, Karina ^b   Saadat, Laleh ^a   Valyi Nagy, Tibor ^a   Kupsky, William ^b   Song, Fei ^a,b   Dratz, Edward ^c   Loeb, Jeffrey A ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MONTANA STATE UNIVERSITY   (United States)

Author keywords

Epilepsy genetics; Epilepsy surgery; Localization related epilepsy; Refractory epilepsy; Transcriptomics

Indexed keywords

BIOLOGICAL MARKER; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NEURON SPECIFIC NUCLEAR PROTEIN; RNA;

ADOLESCENT; ADULT; ARTICLE; BRAIN DAMAGE; BRAIN REGION; CELL INTERACTION; CHILD; EPILEPSY; EPILEPTIC DISCHARGE; FEMALE; GENE CLUSTER; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MALE; MICROGLIA; NEOCORTEX; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SEIZURE; SIGNAL TRANSDUCTION; YOUNG ADULT; BRAIN; CLUSTER ANALYSIS; ELECTROENCEPHALOGRAPHY; GENETICS; INFANT; MICROARRAY ANALYSIS; MIDDLE AGED; NEUROSURGERY; PATHOLOGY;

ADOLESCENT; ADULT; BIOMARKERS; BRAIN; CHILD; CHILD, PRESCHOOL; CLUSTER ANALYSIS; ELECTROENCEPHALOGRAPHY; EPILEPSY; FEMALE; HUMANS; INFANT; MALE; MICROARRAY ANALYSIS; MIDDLE AGED; NEOCORTEX; NEUROSURGICAL PROCEDURES; RNA; TRANSCRIPTION, GENETIC; YOUNG ADULT;

EID: 84922350411     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu350     Document Type: Article

References (55)

1. Annegers J. The treatment of epilepsy: principles and practices. Philadelphia, PA: Lea &Febiger; 1993.
2. Aronica E, Gorter JA, Redeker S, Ramkema M, Spliet WG, van Rijen PC, et al. Distribution, characterization and clinical significance of microglia in glioneuronal tumours from patients with chronic intractable epilepsy. Neuropathol Appl Neurobiol 2005; 31: 280-91.
3. Asano E, Muzik O, Shah A, Juhasz C, Chugani DC, Sood S, et al. Quantitative interictal subdural EEG analyses in children with neocortical epilepsy. Epilepsia 2003; 44: 425-34.
4. Barkmeier DT, Senador D, Leclercq K, Pai D, Hua J, Boutros NN, et al. Electrical, molecular and behavioral effects of interictal spiking in the rat. Neurobiol Dis 2012a; 47: 92-101.
5. Barkmeier DT, Shah AK, Flanagan D, Atkinson MD, Agarwal R, Fuerst DR, et al. High inter-reviewer variability of spike detection on intracranial EEG addressed by an automated multi-channel algorithm. Clin Neurophysiol 2012b; 123: 1088-95.
6. Bautista RE, Cobbs MA, Spencer DD, Spencer SS. Prediction of surgical outcome by interictal epileptiform abnormalities during intracranial EEG monitoring in patients with extrahippocampal seizures. Epilepsia 1999; 40: 880-90.
7. Beaumont TL, Yao B, Shah A, Kapatos G, Loeb JA. Layer-Specific CREB target gene induction in human neocortical epilepsy. J Neurosci 2012; 32: 14389-401.
8. Bentivoglio M, Tassi L, Pech E, Costa C, Fabene PF, Spreafico R. Cortical development and focal cortical dysplasia. Epileptic Disord 2003; 5 (Suppl 2): S27-S34.
9. Boer K, Spliet WG, van Rijen PC, Redeker S, Troost D, Aronica E. Evidence of activated microglia in focal cortical dysplasia. J Neuroimmunol 2006; 173: 188-95.
10. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 2008; 28: 264-78.
11. Cersosimo R, Flesler S, Bartuluchi M, Soprano AM, Pomata H, Caraballo R. Mesial temporal lobe epilepsy with hippocampal sclerosis: study of 42 children. Seizure 2011; 20: 131-7.
12. Cho RJ, Campbell MJ, Winzeler EA, Steinmetz L, Conway A, Wodicka L, et al. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 1998; 2: 65-73.
13. Choi J, Nordli DR Jr, Alden TD, DiPatri A Jr, Laux L, Kelley K, et al. Cellular injury and neuroinflammation in children with chronic intractable epilepsy. J Neuroinflammation 2009; 6.
14. Dent MA, Segura-Anaya E, Alva-Medina J, Aranda-Anzaldo A. NeuN/Fox-3 is an intrinsic component of the neuronal nuclear matrix. FEBS Lett 2010; 584: 2767-71.
15. Draghici S, Khatri P, Eklund AC, Szallasi Z. Reliability and reproducibility issues in DNA microarray measurements. Trends Genet 2006; 22: 101-9.
16. Fabene PF, Bramanti P, Constantin G. The emerging role for chemokines in epilepsy. J Neuroimmunol 2010; 224: 22-7.
17. Fonseca LC, Tedrus GM, Moraes C, Vicente Machado A, Almeida MP, Oliveira DO. Epileptiform abnormalities and quantitative EEG in children with attention-deficit/hyperactivity disorder. Arq Neuropsiquiatr 2008; 66: 462-7.
18. Gotman J. Relationships between interictal spiking and seizures: human and experimental evidence. Can J Neurol Sci 1991; 18 (Suppl 4): 573-6.
19. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 2012; 489: 391-9.
20. Holmes GL. Seizure-induced neuronal injury: animal data. Neurology 2002; 59 (9 Suppl 5): S3-S6
21. Hubbell E, Liu WM, Mei R. Robust estimators for expression analysis. Bioinformatics 2002; 18: 1585-92.
22. Kanazawa O, Blume WT, Girvin JP. Significance of spikes at temporal lobe electrocorticography. Epilepsia 1996; 37: 50-5.
23. Kim KK, Adelstein RS, Kawamoto S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 2009; 284: 31052-61.
24. Kleen JK, Scott RC, Holmes GL, Lenck-Santini PP. Hippocampal interictal spikes disrupt cognition in rats. Ann Neurol 2010; 67: 250-7.
25. Lee SA, Spencer DD, Spencer SS. Intracranial EEG seizure-onset patterns in neocortical epilepsy. Epilepsia 2000; 41: 297-307.
26. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 2001; 98: 31-6.
27. Lipovich L, Dachet F, Cai J, Bagla S, Balan K, Jia H, et al. Activitydependent human brain coding/non-coding gene regulatory networks. Genetics 2012; 192: 1133-48.
28. Lockhart DJ, Dong H, Byrne MC, Follettie MT, Gallo MV, Chee MS, et al. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat Biotechnol 1996; 14: 1675-80.
29. Loeb JA. A human systems biology approach to discover new drug targets in epilepsy. Epilepsia 2010; 51 (Suppl 3): 171-7.
30. Loeb JA. Identifying targets for preventing epilepsy using systems biology. Neurosci Lett 2011; 497: 205-12.
31. Morin-Brureau M, Lebrun A, Rousset MC, Fagni L, Bockaert J, de Bock F, et al. Epileptiform activity induces vascular remodeling and zonula occludens 1 downregulation in organotypic hippocampal cultures: role of VEGF signaling pathways. J Neurosci 2011; 31: 10677-88.
32. Morris J, Singh JM, Eberwine JH. Transcriptome analysis of single cells. J Vis Exp 2011; 50: 2634.
33. Palmini A, Andermann F, Olivier A, Tampieri D, Robitaille Y. Focal neuronal migration disorders and intractable partial epilepsy: results of surgical treatment. Ann Neurol 1991; 30: 750-7.
34. Palmini A, Najm I, Avanzini G, Babb T, Guerrini R, Foldvary-Schaefer N, et al. Terminology and classification of the cortical dysplasias. Neurology 2004; 62 (6 Suppl 3): S2-8.
35. Parakalan R, Jiang B, Nimmi B, Janani M, Jayapal M, Lu J, et al. Transcriptome analysis of amoeboid and ramified microglia isolated from the corpus callosum of rat brain. BMC Neurosci 2012; 13: 64.
36. Pitkanen A, Sutula TP. Is epilepsy a progressive disorder. Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 2002; 1: 173-81.
37. Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P. Genetic disruption of cortical interneuron development causes region-and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 2003; 23: 622-31.
38. Pressler RM, Robinson RO, Wilson GA, Binnie CD. Treatment of interictal epileptiform discharges can improve behavior in children with behavioral problems and epilepsy. J Pediatr 2005; 146: 112-7.
39. Rakhade SN, Shah AK, Agarwal R, Yao B, Asano E, Loeb JA. Activity-dependent gene expression correlates with interictal spiking in human neocortical epilepsy. Epilepsia 2007; 48 (Suppl 5): 86-95.
40. Rakhade SN, Yao B, Ahmed S, Asano E, Beaumont TL, Shah AK, et al. A common pattern of persistent gene activation in human neocortical epileptic foci. Ann Neurol 2005; 58: 736-47.
41. Schaeren-Wiemers N, Andre E, Kapfhammer JP, Becker-Andre M. The expression pattern of the orphan nuclear receptor RORbeta in the developing and adult rat nervous system suggests a role in the processing of sensory information and in circadian rhythm. Eur J Neurosci 1997; 9: 2687-701.
42. Seo JH, Noh BH, Lee JS, Kim DS, Lee SK, Kim TS, et al. Outcome of surgical treatment in non-lesional intractable childhood epilepsy. Seizure 2009; 18: 625-9.
43. Shen-Orr SS, Tibshirani R, Khatri P, Bodian DL, Staedtler F, Perry NM, et al. Cell type-specific gene expression differences in complex tissues. Nat Methods 2010; 7: 287-9.
44. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011; 27: 431-2.
45. Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children. Lancet Neurol 2008; 7: 525-37.
46. Staley K, Hellier JL, Dudek FE. Do interictal spikes drive epileptogenesis. Neuroscientist 2005; 11: 272-6.
47. Staley KJ, White A, Dudek FE. Interictal spikes: harbingers or causes of epilepsy. Neurosci Lett 2011; 497: 247-50.
48. Sutula TP, Hagen J, Pitkanen A. Do epileptic seizures damage the brain. Curr Opin Neurol 2003; 16: 189-95.
49. Thom M, Mathern GW, Cross JH, Bertram EH. Mesial temporal lobe epilepsy: how do we improve surgical outcome. Ann Neurol 2010; 68: 424-34.
50. Trapp BD, Wujek JR, Criste GA, Jalabi W, Yin X, Kidd GJ, et al. Evidence for synaptic stripping by cortical microglia. Glia 2007; 55: 360-8.
51. Unal-Cevik I, Kilinc M, Gursoy-Ozdemir Y, Gurer G, Dalkara T. Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 2004; 1015: 169-74.
52. Vezzani A, French J, Bartfai T, Baram TZ. The role of inflammation in epilepsy. Nat Rev Neurol 2011; 7: 31-40.
53. Zahurak M, Parmigiani G, Yu W, Scharpf RB, Berman D, Schaeffer E, et al. Pre-processing Agilent microarray data. BMC Bioinformatics 2007; 8: 142.
54. Zeng H, Shen EH, Hohmann JG, Oh SW, Bernard A, Royall JJ, et al. Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 2012; 149: 483-96.
55. Zhou JL, Lenck-Santini PP, Zhao Q, Holmes GL. Effect of interictal spikes on single-cell firing patterns in the hippocampus. Epilepsia 2007; 48: 720-31