RNA-seq analysis of hippocampal tissues reveals novel candidate genes for drug refractory epilepsy in patients with MTLE-HS

Genomics

Volumn 107, Issue 5, 2016, Pages 178-188

  Dixit, Aparna Banerjee ^a   Banerjee, Jyotirmoy ^a   Srivastava, Arpna ^b   Tripathi, Manjari ^b   Sarkar, Chitra ^b   Kakkar, Aanchal ^b   Jain, Mukesh ^c   Chandra, P Sarat ^b  

^a NBRC   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^c JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

Drug refractory epilepsy; Epileptogenesis; Intrinsic severity hypothesis; MTLE HS; RNAseq analysis

Indexed keywords

AQP4 AS1 ANTISENSE RNA; COMPLEMENTARY RNA; KIRREL3 AS2 ANTISENSE RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; RNA;

ADULT; ARTICLE; CABP1 GENE; CALCIUM SIGNALING; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CSNK2B GENE; DOWN REGULATION; DRUG RESISTANT EPILEPSY; EPILEPTOGENESIS; FEMALE; FN1 GENE; GABAERGIC NEUROTRANSMISSION; GENE; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE ONTOLOGY; GENETIC ASSOCIATION; GENETIC LINKAGE; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; KIF5A GENE; MALE; MESIAL TEMPORAL LOBE EPILEPSY; MESIAL TEMPORAL LOBE EPILEPSY HIPPOCAMPAL SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NEUROD6 GENE; NEUROMODULATION; NEURONAL NETWORK MODULATION; NEUROSURGERY; NEUROTRANSMISSION; NLRP1 GENE; PRIORITY JOURNAL; RELN GENE; RNA SEQUENCE; SCN1B GENE; SCRT1 GENE; SYNAPTIC TRANSMISSION; TGF BETA R2 GENE; TRANSCRIPTOMICS; UPREGULATION; YOUNG ADULT; ADOLESCENT; GENETICS; METABOLISM; NERVE CELL NETWORK; PATHOLOGY; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS;

ADOLESCENT; ADULT; DRUG RESISTANT EPILEPSY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MALE; NERVE NET; PROTEIN BIOSYNTHESIS; RNA; SEQUENCE ANALYSIS, RNA;

EID: 84964237810     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2016.04.001     Document Type: Article

References (87)

1. Aaron J.C., Rajiv W. Calretinin: modulator of neuronal excitability. Int. J. Biochem. Cell Biol. 2009, 41(11):2118-2121.
2. Allen A.S., Berkovic S.F., Cossette P., Delanty N., Dlugos D., Eichler E.E., et al. De novo mutations in epileptic encephalopathies. Nature 2013, 12:501(7466):217-221.
3. Baglietto M.G., Caridi G., Gimelli G., Mancardi M., Prato G., Ronchetto P., Cuoco C., Tassano E. RORB gene and 9q21.13 microdeletion: report on a patient with epilepsy and mild intellectual disability. Eur. J. Med. Genet. 2014, 7(1):44-46. 10.1016/j.ejmg.2013.12.001.
4. Banerjee J., Tripathi M., Chandra P.S. Understanding complexities of synaptic transmission in medically intractable seizures: a paradigm of epilepsy research. Indian J. Neurosurgery. 2013, 2:71-76.
5. Banerjee J., Chandra P.S., Kurwale N., Tripathi M. Epileptogenic networks and drug-resistant epilepsy: present and future perspectives of epilepsy research-utility for the epileptologist and the epilepsy surgeon. Ann. Indian Acad. Neurol. Suppl. 2014, S1:134-140.
6. Baxter K.K., Uittenbogaard M., Chiaramello A. The neurogenic helix loop helix transcription factor NeuroD6 enhances mitochondrial biogenesis and bioenergetics to confer tolerance of neuronal PC12 NeuroD6 cells to the mitochondrial stressor rotenone. Exp. Cell Res. 2012, 318(17):2200-2214.
7. Becker A.J., Chen J., Zien A., Sochivko D., Normann S., Schramm J., et al. Correlated stage- and subfield-associated hippocampal gene expression patterns in experimental and human temporal lobe epilepsy. Eur. J. Neurosci. 2003, 18:2792-2802.
8. Bhalla K., Luo Y., Buchan T., Beachem M.A., Guzauskas G.F., Ladd S., et al. Alterations in CDH15 and KIRREL3 in patients with mild to severe intellectual disability. Am. J. Hum. Genet. 2008, 83(6):703-713.
9. Brehme H., Kirschstein T., Schulz R., Köhling R., et al. In vivo treatment with the casein kinase 2 inhibitor 4, 5, 6, 7-tetrabromotriazole augments the slow after hyperpolarizing potential and prevents acute epileptiform activity. Epilepsia 2014, 55(1):175-183.
10. Carvill G.L., Heavin S.B., Yendle S.C., McMahon J.M., O'Roak B.J., Cook J., Mefford H.C. Targeted resequencing in epileptic encephalopathies identifies de novo mutations in CHD2 and SYNGAP1. Nat. Genet. 2013, 45(7). (10.1038/ng.2646). 10.1038/ng.2646.
11. Chan C.H., Godinho L.N., Thomaidou D., Tan S.S., Gulisano M., Parnavelas J.G. Emx1 is a marker for pyramidal neurons of the cerebral cortex. Cereb. Cortex 2001, 11:1191-1198.
12. Chen A.J.,.J., Paus S., Normann S., Beck H., Elger C.E., Wiestler O.D., et al. Transcriptional profiling in human epilepsy: expression array and single cell real-time qRT-PCR analysis reveal distinct cellular gene regulation. Neuroreport 2002, 13:1327-1333.
13. Chen L., Zhang W., Yan W., Han L., Zhang K., Shi Z., et al. The putative tumor suppressor miR-524-5p directly targets Jagged-1 and Hes-1 in glioma. Carcinogenesis 2012, 33(11):2276-2282.
14. Dityatev A. Remodeling of extracellular matrix and epileptogenesis. Epilepsia 2010, 51(Suppl. 3):61-65. 10.1111/j.1528-1167.2010.02612.x.
15. Dixit A.B., Banerjee J., Tripathi M., Chandra P.S. Presurgical epileptogenic network analysis: a way to enhance epilepsy surgery outcome. Neurol. India 2015, (In press).
16. Epilepsy Fact Sheet, World Health Organization Accessed online from. http://www.who.int/mediacentre/factsheets/fs999/en/.
17. Fabene P.F., Bramanti P., Constantin G. The emerging role for chemokines in epilepsy. J. Neuroimmunol. 2010, 224:22-27.
18. Faghihi M.A., Zhang M., Huang J., Modarresi F., Van der Brug M.P., Nalls M.A., et al. Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol. 2010, 11(5):R56. 10.1186/gb-2010-11-5-r56.
19. Gomez-Ferreria M.A., Rath U., Buster D.W., Chanda S.K., Caldwell J.S., Rines D.R., et al. Human Cep192 is required for mitotic centrosome and spindle assembly. Curr. Biol. 2007, 20, 17(22):1960-1966.
20. Gupta S., Burckhardt G., Hagos Y. SLC22 transporter family proteins as targets for cytostatic uptake into tumor cells. Biol. Chem. 2011, 392:117-124.
21. Hansen K.F., Sakamoto K., Pelz C., Impey S., Obrietan K. Profiling status epilepticus-induced changes in hippocampal RNAexpression using high-throughput RNAsequencing. Sci. Rep. 2014, 4:6930. 10.1038/srep06930.
22. Harris M.A., Clark J., Ireland A., Lomax J., Ashburner M., Foulger R., et al. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 2004, 32:D258-D261.
23. Harteneck C., Leuner K. TRP Channels in Neuronal and Glial Signal Transduction, Neurochemistry. InTech 2014, 10.5772/58232. D.T. Heinbockel (Ed.).
24. Huang D.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 2009, 4(1):44-57.
25. Ibberson D., Benes V., Muckenthaler M.U., Castoldi M. RNA degradation compromises the reliability of microRNA expression profiling. BMC Biotechnol. 2009, 9:102. 10.1186/1472-6750-9-102.
26. Jamali S., Bartolomei F., Robaglia-Schlupp A., Massacrier A., Peragut J.C., Regis J., et al. Large-scale expression study of human mesial temporal lobe epilepsy: evidence for dysregulation of the neurotransmission and complement systems in the entorhinal cortex. Brain 2006, 129:625-641.
27. Kabos P., Kabosova A., Neuman T. Blocking HES1 Expression Initiates GABAergic Differentiation and Induces the Expression of p21CIP1/WAF1 in Human Neural Stem Cells. J. Biol. Chem. 2002, 277:8763-8766.
28. Kadler K.E., Hill A., Canty-Laird E.G. Collagen fibrillogenesis: fibronectin, integrins, and minor collagens as organizers and nucleators. Curr. Opn. Cell Biol. 2008, 20(5-24):495-501. 10.1016/j.ceb.2008.06.008.
29. Kan A.A., van Erp S., Derijck A.A., de Wit M., Hessel E.V., O'Duibhir E., et al. Genome-wide microRNA profiling of human temporal lobe epilepsy identifies modulators of the immune response. Cell. Mol. Life Sci. 2012, 69:3127-3145.
30. Katja K., Ina J., Michelle H., Jan H., Eric H., Rolf B., et al. Increased reelin promoter methylation is associated with granule cell dispersion in human temporal lobe epilepsy. J. Neuropathol. Exp. Neurol. 2009, 68:356-364.
31. Katnb-Karabay A., Yu W., Solowska J.M., Baird D.H., Baas P.W. Axonal growth is sensitive to the levels of katanin, a protein that severs microtubules. J. Neurosci. 2004, 24:5778-5788.
32. Kauffman M.A., Consalvo D., Gonzalez M.D., Kochen S. Transcriptionally less active prodynorphin promoter alleles are associated with temporal lobe epilepsy: a case-control study and meta-analysis. Dis. Markers 2008, 24:135-140.
33. Khatri N., Man H.Y. Synaptic activity and bioenergy homeostasis: implications in brain trauma and neurodegenerative diseases. Front. Neurol. 2013, 11(4):199. 10.3389/fneur.2013.00199.
34. Kiernan M.C., Krishnan A.V., Lin C.S., Burke D., Berkovic S.F. Mutation in the Na + channel subunit SCN1B produces paradoxical changes in peripheral nerve excitability. Brain 2005, 128:1841-1846.
35. Kolodkin A.L., Levengood D.V., Rowe E.G., Tai Y.T., Giger R.J., Ginty D.D. Neuropilin is a semaphorin III receptor. Cell 1997, 90:753-762.
36. Kumar A., Tripathi M., Pandey R.M., Ramakrishnan L., Srinivas M., Luthra K. Apolipoprotein E in temporal lobe epilepsy: a case- control study. Dis. Markers 2006, 22(5-6):335-342.
37. Kwan P., Brodie M.J. Early identification of refractory epilepsy. N. Engl. J. Med. 2000, 342:314-319.
38. Kwan P., Poon W.S., Ng H.K., Kang D.E., Wong V., Ng P.W., et al. Multidrug resistance in epilepsy and polymorphisms in the voltage-gated sodium channel genes SCN1A, SCN2A, and SCN3A: correlation among phenotype, genotype, and mRNA expression. Pharmacogenet. Genomics 2008, 18:98-9998.
39. Labasque M., Devaux J.J., Lévêque C., Faivre-Sarrailh C. Fibronectin type III-like domains of Neurofascin-186 protein mediate gliomedin binding and its clustering at the developing nodes of Ranvier. J. Biol. Chem. 2011, 286(49):42426-42434.
40. Lee T.S., Eid T., Mane S., Kim J.H., Spencer D.D., Ottersen O.P., et al. Aquaporin-4 is increased in the sclerotic hippocampus in human temporal lobe epilepsy. ActaNeuropathol. (Berl.) 2004, 108:493-502.
41. Li J.Y., Chai B., Zhang W., Wu X., Zhang C., Fritze D., et al. Ankyrin repeat and SOCS box containing protein 4 (Asb-4) colocalizes with insulin receptor substrate 4 (IRS4) in the hypothalamic neurons and mediates IRS4 degradation. BMC Neurosci. 2011, 28(12):95. 10.1186/1471-2202-12-95.
42. Liu Z., Xiang Y., Sun G. KCTD family of proteins: structure, function, disease relevance. Cell Biosci. 2013, 24, 3(1):45. 10.1186/2045-3701-3-45.
43. Liu X., Yang Z., Yin Y., Deng X. Increased expression of Notch1 in temporal lobe epilepsy: animal models and clinical evidence. Neurol. Regen Res. 2014, 9(5):526-533.
44. Mahler M., Ben-Ari Y., Represa A. Differential expression of fibronectin, tenascin-C and NCAMs in cultured hippocampal astrocytes activated by kainate, bacterial lipopolysaccharide or basic fibroblast growth factor. Brain Res. 1997, 775(1-2):63-73.
45. Martijn P.L., Michelle L.G., Cristel M.S., Richard P.H., Rachel H.G., Emile E.V., Michael O. Tumor suppression by the von Hippel-Lindau protein requires. Phosphorylation of the acidic domain. J. Biol. Chem. 2005, 280(23):22205-22211.
46. Maurer-Morelli C.V., de Vasconcellos J.F., Reis-Pinto F.C., Rocha Cde S., Domingues R.R., Yasuda C.L., et al. A comparison between different reference genes for expression studies in human hippocampal tissue. J. Neurosci. Methods 2012, 208:44-47.
47. McCall R.D. HPNS seizure risk: a role for the Golgi-associated retrograde protein complex?. Undersea Hyperb. Med. 2011, 38(1):3-9.
48. Michael A.R. The intrinsic severity hypothesis of pharmacoresistance to antiepileptic drugs. Epilepsia 2013, 54(Suppl. S2):33-40.
49. Michaud J.L., Lachance M., Hamdan F.F., Carmant L., Lortie A., Diadori P., et al. The genetic landscape of infantile spasms. Hum. Mol. Genet. 2014, 23(18):4846-4858.
50. Miller-Delaney S.F., Das S., Sano T., Jimenez-Mateos E.M., Bryan K., Buckley P.G., Stallings R.L., Henshall D.C. Differential DNA methylation patterns define status epilepticus and epileptic tolerance. J. Neurosci. 2012, 32(5):1577-1588.
51. Mirza N., Vasieva O., Marson A.G., Pirmohamed M. Exploring the genomic basis of pharmacoresistance in epilepsy: an integrative analysis of large-scale gene expression profiling studies on brain tissue from epilepsy surgery. Hum. Mol. Genet. 2011, 20(22):4381-4394.
52. Nakajima K., Yin X., Takei Y., Seog D.H., Homma N., Hirokawa N. Molecular motor KIF5A is essential for GABA(A) receptor transport, and KIF5A deletion causes epilepsy. Neuron 2012, 76(5):945-961.
53. Niquet J., Jorquera I., Ben-Ari Y., Represa A. Proliferative astrocytes may express fibronectin-like protein in the hippocampus of epileptic rats. Neurosci. Lett. 1994, 180(1):13-16.
54. Okamoto M., Sakiyama J., Mori S., Kurazono S., Usui S., Hasegawa M., et al. Kainic acid-induced convulsions cause prolonged changes in the chondroitin sulfate proteoglycansneurocan and phosphacan in the limbic structures. Exp. Neurol. 2003, 184(1):179-195.
55. Olivé M., Abdul-Hussein S., Oldfors A., González-Costello J., van der Ven P.F., Fürst D.O., et al. New cardiac and skeletal protein aggregate myopathy associated with combined MuRF1 and MuRF3 mutations. Hum. Mol. Genet. 2015, 1; 24(13):3638-3650.
56. Ozbas-Gerceker F., Redeker S., Boer K., Ozguc M., Saygi S., Dalkara T., et al. Serial analysis of gene expression in the hippocampus of patients with mesial temporal lobe epilepsy. Neuroscience 2006, 138:457-474.
57. Ozkara C., Altintas A., Yilmaz E., Eskazan E., Erkol G., Ozyurt E., Erdogan E., Kuday C. An association between mesial temporal lobe epilepsy with hippocampal sclerosis and human leukocyte antigens. Epilepsia 2002, 43(3):236-239.
58. Patel R.K., Jain M. NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 2012, 7(2):e30619. (NGSQCTookit v2.0).
59. Pirker S., Gasser E., Czech T., Baumgartner C., Schuh E., Feucht M., Sperk G. Dynamic up-regulation of prodynorphin transcription in temporal lobe epilepsy. Hippocampus 2009, 19(11):1051-1054.
60. Proper E.A., Hoogland G., Kappen S.M., Jansen G.H., Rensen M.G., Schrama L.H., et al. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 2002, 125:32-43.
61. Radhakrishnana A., Menon R.N., Hariharan S., Radhakrishnana K. The evolving electroclinical syndrome of "epilepsy with ring chromosome 20". Seizure 2012, 21(2):92-97.
62. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140. 10.1093/bioinformatics/btp616.
63. Rocha L., Alonso-Vanegas M., Martínez-Juárez I.E., Orozco-Suárez S., Escalante-Santiago D., Feria-Romero I.A. GABAergic alterations in neocortex of patients with pharmacoresistant temporal lobe epilepsy can explain the comorbidity of anxiety and depression: the potential impact of clinical factors. Front. Cell. Neurosci. 2015, 5(8):442.
64. Rogawski M.A. The intrinsic severity hypothesis of pharmacoresistance to antiepileptic drugs. Epilepsia 2013, 54(Suppl. S2):33-40.
65. Rogawski M.A., Loscher W. The neurobiology of antiepileptic drugs. Nat. Rev. Neurosci. 2004, 5:553-564.
66. Santhakumar V., Aradi I., Soltesz I. Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J. Neurophysiol. 2005, 93:437-453.
67. Scotti A.L., Bollag O., Kalt G., Nitsch C. Loss of perikaryal parvalbumin immunoreactivity from surviving GABAergic neurons in the CA1 field of epileptic gerbils. Hippocampus 1997, 7:524-535.
68. Sun M., Gewirtz J.C., Bofenkamp L., Wickham R.J., Ge H., O'Connor M.B. Canonical TGF- signaling is required for balance of excitatory/inhibitory transmission within the hippocampus and prepulse inhibition of acoustic startle. J. Neurosci. 2010, 30(17):6025-6035.
69. Takashi F., Yataro D., Koichi M., Koji U., Yusuke N. Critical Function for Nuclear Envelope Protein TMEM209 in Human Pulmonary Carcinogenesis 2012, June 19. 10.1158/0008-5472.
70. Tammimies K1., Vitezic M., Matsson H., Le Guyader S., TR Bürglin, Ohman T., Strömblad S., Daub C.O., Nyman T.A., Kere J., Tapia-Páez I. Molecular networks of DYX1C1 gene show connection to neuronal migration genes and cytoskeletal proteins. Biol. Psychiatry 2013, 73(6):583-590.
71. Tan C.C., Zhang J.G., Tan M.S., Chen H., Meng D.W., Jiang T., et al. NLRP1 inflammasome is activated in patients with medial temporal lobe epilepsy and contributes to neuronal pyroptosis in amygdala kindling-induced rat model. J. Neuroinflammation 2015, 12(1):18. 10.1186/s12974-014-0233-0.
72. Tóth K., Maglóczky Z. The vulnerability of calretinin-containing hippocampal interneurons to temporal lobe epilepsy. Front. Neuroanat. 2014, 29(8):100. eCollection 2014. 10.3389/fnana.2014.00100.
73. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-seq. Bioinformatics 2009, 25(9):1105-1111.
74. Trimbuch T., Beed P., Vogt J., Schuchmann S., Maier N., Kintscher M., et al. Synaptic PRG-1 modulates excitatory transmission via lipid phosphate-mediated signaling. Cell 2009, 18, 138(6):1222-1235.
75. Valles-Ortega J., Duran J., Garcia-Rocha M., Bosch C., Saez I., Pujadas L., Guinovart J.J. Neurodegeneration and functional impairments associated with glycogen synthase accumulation in a mouse model of Lafora disease. EMBO Mol. Med. 2011, 3(11):667-681.
76. vanGassen K.L., de Wit M., Koerkamp M.J., Rensen M.G., van Rijen P.C., Holstege F.C., et al. Possible role of the innate immunity in temporal lobe epilepsy. Epilepsia 2008, 49:1055-1065.
77. Veeramah K.R., Johnstone L., Karafet T.M., Wolf D., Sprissler R., Salogiannis J., et al. Exome sequencing reveals new causal mutations in children with epileptic encephalopathies. Epilepsia 2013, 54:1270-1281.
78. Venugopal A.K., Sameer, Kumar G.S., Mahadevan A., Selvan L.D., Marimuthu A., Dikshit J.B., et al. Transcriptomic profiling of medial temporal lobe epilepsy. J. Proteomics Bioinform. 2012, 5(2). (pii: 1000210).
79. Vezzani A., Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 2005, 46:1724-1743.
80. Wang J., Yin L., Chen Z. Neuroprotective role of fibronectin in neuron-glial extrasynaptic transmission. Neural Regen Res. 2013, 8(4):376-382.
81. Xi Z.Q., Xiao F., Yuan J., Wang X.F., Wang L., Quan F.Y., et al. Gene expression analysis on anterior temporal neocortex of patients with intractable epilepsy. Synapse 2009, 63:1017-1028.
82. Xi Z.Q., Wang X., Luo J., Wang W., Xiao F., Chen D., Wang S., Li M., Wang L. Fibronectin is a potential cerebrospinal fluid and serum epilepsy biomarker. Epilepsy Behav. 2015, 48:66-69.
83. Xiao F., Wang X.F., Li J.M., Xi Z.Q., Lu Y., Wang L., et al. Overexpression of N-WASP in the brain of human epilepsy. Brain Res. 2008, 1233:168-175.
84. Xue Z., Ye Q., Anson S.R., Yang J., Xiao G., Kowbel D., et al. Transcriptional interference by antisense RNA is required for circadian clock function. Nature 2014, 30,514(7524):650-653.
85. Zarbalis K., Choe Y., Siegenthaler J.A., Orosco L.A., Pleasure S.J. Meningeal defects alter the tangential migration of cortical interneurons in Foxc1hith/hith mice. Neural Dev. 2012, 7(2). 10.1186/1749-8104-7-2.
86. Zhan S., Chan C.C., Serdar B., Rockey D.C. Fibronectin stimulates endothelin-1 synthesis in rat hepatic myofibroblasts via a Src/ERK-regulated signaling pathway. Gastroenterology 2009, 136(7):2345-2355.
87. Zheng Y., McFarland B.C., Drygin D., Yu H., Bellis S.L., Kim H., Bredel M., Benveniste E.N. Targeting protein kinase CK2 suppresses prosurvival signaling pathways and growth of glioblastoma. Clin. Cancer Res. 2013, 19(23):6484-6494.