Inhibitory RNA in epilepsy: Research tools and therapeutic perspectives

Epilepsia

Volumn 51, Issue 9, 2010, Pages 1659-1668

  Boison, Detlev ^a  

^a LEGACY RESEARCH   (United States)

Author keywords

Adenosine; Gene therapy; Glia; RNA interference; RNAi

Indexed keywords

ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE KINASE; AMYLOID PRECURSOR PROTEIN; ATAXIN 1; HUNTINGTIN; LENTIVIRUS VECTOR; MICRORNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RNA INDUCED SILENCING COMPLEX; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; SODIUM CHANNEL NAV1.1; ANTICONVULSIVE AGENT;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ASTROCYTOSIS; EPILEPSY; EX VIVO GENE TRANSFER; FEBRILE CONVULSION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUNTINGTON CHOREA; IN VIVO GENE TRANSFER; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN TARGETING; PURKINJE CELL; REVIEW; RNA INTERFERENCE; RNA PROCESSING; SPINOCEREBELLAR DEGENERATION; STEM CELL; TRANSCRIPTION REGULATION; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; ANIMAL; BRAIN; DRUG EFFECTS; ENZYMOLOGY; GENE THERAPY; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROCEDURES;

ADENOSINE; ADENOSINE KINASE; ANIMALS; ANTICONVULSANTS; BRAIN; EPILEPSY; GENE EXPRESSION REGULATION; GENETIC THERAPY; HUMANS; MICE; MICRORNAS; RNA INTERFERENCE;

EID: 77956330494     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2010.02672.x     Document Type: Review

References (80)

1. Aronica E, Fluiter K, Iyer A, Zurolo E, Vreijling J, van Vliet EA, Baayen JC, Gorter JA 2010) Expression pattern of Mir-146a, an inflammation-associated microRNA, in experimental and human temporal lobe epilepsy. Eur J Neurosci 31 : 1100 1107.
2. Bartel DP 2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 : 281 297.
3. Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, Barzilai A, Einat P, Einav U, Meiri E, Sharon E, Spector Y, Bentwich Z 2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 37 : 766 770.
4. Boison D, Stoffel W 1994) Disruption of the compacted myelin sheath of axons of the central nervous system in proteolipid protein-deficient mice. Proc Natl Acad Sci U S A 91 : 11709 11713.
5. Boison D 2008a) Adenosine as a neuromodulator in neurological diseases. Curr Opin Pharmacol 8 : 2 7.
6. Boison D 2008b) The adenosine kinase hypothesis of epileptogenesis. Prog Neurobiol 84 : 249 262.
7. Boison D 2009a) Adenosine augmentation therapies (AATs) for epilepsy: prospect of cell and gene therapies. Epilepsy Res 85 : 131 141.
8. Boison D 2009b) Engineered adenosine-releasing cells for epilepsy therapy: human mesenchymal stem cells and human embryonic stem cells. Neurotherapeutics 6 : 278 283.
9. Boison D, Chen JF, Fredholm BB 2010) Adenosine signalling and function in glial cells. Cell Death Differ 17 : 1071 1082.
10. Burright EN, Clark HB, Servadio A, Matilla T, Feddersen RM, Yunis WS, Duvick LA, Zoghbi HY, Orr HT 1995) Sca1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell 82 : 937 948.
11. Catterall WA, Dib-Hajj S, Meisler MH, Pietrobon D 2008) Inherited neuronal ion channelopathies: new windows on complex neurological diseases. J Neurosci 28 : 11768 11777.
12. Chen K, Rajewsky N 2007) The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8 : 93 103.
13. Davidson BL, Boudreau RL 2007) RNA interference: a tool for querying nervous system function and an emerging therapy. Neuron 53 : 781 788.
14. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T 2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 : 494 498.
15. Esquela-Kerscher A, Slack FJ 2006) OncoMirs - microRNAs with a role in cancer. Nat Rev Cancer 6 : 259 269.
16. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC 1998) Potent and specific genetic interference by double-stranded RNA in caenorhabditis elegans. Nature 391 : 806 811.
17. Fredholm BB, Chen JF, Cunha RA, Svenningsson P, Vaugeois JM 2005) Adenosine and brain function. Int Rev Neurobiol 63 : 191 270.
18. Gonzalez-Alegre P, Paulson HL 2007) Technology insight: therapeutic RNA interference-how far from the neurology clinic? Nat Clin Pract Neurol 3 : 394 404.
19. Gray SJ, Blake BL, Criswell HE, Nicolson SC, Samulski RJ, McCown TJ 2010) Directed evolution of a novel adeno-associated virus (AAV) vector that crosses the seizure-compromised blood-brain barrier (BBB). Mol Ther 18 : 570 578.
20. Guarnieri DJ, DiLeone RJ 2008) MicroRNAs: a new class of gene regulators. Ann Med 40 : 197 208.
21. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, Chen W, Zhai P, Sufit RL, Siddique T 1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264 : 1772 1775.
22. Haberman R, Criswell H, Snowdy S, Ming Z, Breese G, Samulski R, McCown T 2002) Therapeutic liabilities of in vivo viral vector tropism: adeno-associated virus vectors, nmdar1 antisense, and focal seizure sensitivity. Mol Ther 6 : 495 500.
23. Hardy J, Selkoe DJ 2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 : 353 356.
24. Harper SQ, Staber PD, He X, Eliason SL, Martins IH, Mao Q, Yang L, Kotin RM, Paulson HL, Davidson BL 2005) RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc Natl Acad Sci U S A 102 : 5820 5825.
25. Hoelters J, Ciccarella M, Drechsel M, Geissler C, Gulkan H, Bocker W, Schieker M, Jochum M, Neth P 2005) Nonviral genetic modification mediates effective transgene expression and functional RNA interference in human mesenchymal stem cells. J Gene Med 7 : 718 728.
26. Huber A, Padrun V, Deglon N, Aebischer P, Mohler H, Boison D 2001) Grafts of adenosine-releasing cells suppress seizures in kindling epilepsy. Proc Natl Acad Sci U S A 98 : 7611 7616.
27. Kalev-Zylinska ML, Symes W, Young D, During MJ 2009) Knockdown and overexpression of nr1 modulates NMDA receptor function. Mol Cell Neurosci 41 : 383 396.
28. Khvorova A, Reynolds A, Jayasena SD 2003) Functional siRNAs and miRNAs exhibit strand bias. Cell 115 : 209 216.
29. Lazarowski A, Czornyj L, Lubienieki F, Girardi E, Vazquez S, D'Giano C 2007) ABC transporters during epilepsy and mechanisms underlying multidrug resistance in refractory epilepsy. Epilepsia 48 (suppl 5 140 149.
30. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN 2004a) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23 : 4051 4060.
31. Lee YS, Nakahara K, Pham JW, Kim K, He Z, Sontheimer EJ, Carthew RW 2004b) Distinct roles for drosophila dicer-1 and dicer-2 in the siRNA/miRNA silencing pathways. Cell 117 : 69 81.
32. Li T, Lan JQ, Fredholm BB, Simon RP, Boison D 2007) Adenosine dysfunction in astrogliosis: cause for seizure generation? Neuron Glia Biol 3 : 353 366.
33. Li T, Lan JQ, Boison D 2008a) Uncoupling of astrogliosis from epileptogenesis in adenosine kinase (ADK) transgenic mice. Neuron Glia Biol 4 : 91 99.
34. Li T, Ren G, Lusardi T, Wilz A, Lan JQ, Iwasato T, Itohara S, Simon RP, Boison D 2008b) Adenosine kinase is a target for the prediction and prevention of epileptogenesis in mice. J Clin Invest 118 : 571 582.
35. Li T, Ren G, Kaplan DL, Boison D 2009) Human mesenchymal stem cell grafts engineered to release adenosine reduce chronic seizures in a mouse model of ca3-selective epileptogenesis. Epilepsy Res 84 : 238 241.
36. Lingor P, Bahr M 2007) Targeting neurological disease with RNAi. Mol Biosyst 3 : 773 780.
37. Lipman DJ 1997) Making (anti)sense of non-coding sequence conservation. Nucleic Acids Res 25 : 3580 3583.
38. Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X, Turner RJ, Jickling G, Sharp FR 2010) Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 30 : 92 101.
39. Loscher W 2007) Drug transporters in the epileptic brain. Epilepsia 48 (suppl 1 8 13.
40. Loscher W, Gernert M, Heinemann U 2008) Cell and gene therapies in epilepsy - promising avenues or blind alleys? Trends Neurosci 31 : 62 73.
41. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U 2004) Nuclear export of microRNA precursors. Science 303 : 95 98.
42. Lusardi TA, Farr CD, Faulkner CL, Pignataro G, Yang T, Lan J, Simon RP, Saugstad JA 2010) Ischemic preconditioning regulates expression of microRNAs and a predicted target, mecp2, in mouse cortex. J Cereb Blood Flow Metab 30 : 744 756.
43. Martin MS, Dutt K, Papale LA, Dube CM, Dutton SB, de Haan G, Shankar A, Tufik S, Meisler MH, Baram TZ, Goldin AL, Escayg A 2010) Altered function of the scn1a voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. J Biol Chem 285 : 9823 9834.
44. McBride JL, Boudreau RL, Harper SQ, Staber PD, Monteys AM, Martins I, Gilmore BL, Burstein H, Peluso RW, Polisky B, Carter BJ, Davidson BL 2008) Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: implications for the therapeutic development of RNAi. Proc Natl Acad Sci U S A 105 : 5868 5873.
45. McCown TJ 2009) Adeno-associated virus vector-mediated expression and constitutive secretion of galanin suppresses limbic seizure activity. Neurotherapeutics 6 : 307 311.
46. McManus MT, Sharp PA 2002) Gene silencing in mammals by small interfering RNAs. Nat Rev Genet 3 : 737 747.
47. Montgomery MK, Xu S, Fire A 1998) RNA as a target of double-stranded RNA-mediated genetic interference in caenorhabditis elegans. Proc Natl Acad Sci U S A 95 : 15502 15507.
48. Nahid MA, Pauley KM, Satoh M, Chan EK 2009) Mir-146a is critical for endotoxin-induced tolerance: implication in innate immunity. J Biol Chem 284 : 34590 34599.
49. Nellen W, Lichtenstein C 1993) What makes an mRNA anti-sense-itive? Trends Biochem Sci 18 : 419 423.
50. Noe F, Frasca A, Balducci C, Carli M, Sperk G, Ferraguti F, Pitkanen A, Bland R, Fitzsimons H, During M, Vezzani A 2009) Neuropeptide y overexpression using recombinant adeno-associated viral vectors. Neurotherapeutics 6 : 300 306.
51. Paradis S, Harrar DB, Lin Y, Koon AC, Hauser JL, Griffith EC, Zhu L, Brass LF, Chen C, Greenberg ME 2007) An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53 : 217 232.
52. Paul CP, Good PD, Winer I, Engelke DR 2002) Effective expression of small interfering RNA in human cells. Nat Biotechnol 20 : 505 508.
53. Paulson HL, Bonini NM, Roth KA 2000) Polyglutamine disease and neuronal cell death. Proc Natl Acad Sci U S A 97 : 12957 12958.
54. Pillai RS, Bhattacharyya SN, Filipowicz W 2007) Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol 17 : 118 126.
55. Provost P, Dishart D, Doucet J, Frendewey D, Samuelsson B, Radmark O 2002) Ribonuclease activity and RNA binding of recombinant human dicer. EMBO J 21 : 5864 5874.
56. Ralph GS, Radcliffe PA, Day DM, Carthy JM, Leroux MA, Lee DC, Wong LF, Bilsland LG, Greensmith L, Kingsman SM, Mitrophanous KA, Mazarakis ND, Azzouz M 2005) Silencing mutant sod1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med 11 : 429 433.
57. Raol YH, Lund IV, Bandyopadhyay S, Zhang G, Roberts DS, Wolfe JH, Russek SJ, Brooks-Kayal AR 2006) Enhancing GABA(a) receptor alpha 1 subunit levels in hippocampal dentate gyrus inhibits epilepsy development in an animal model of temporal lobe epilepsy. J Neurosci 26 : 11342 11346.
58. Raoul C, Abbas-Terki T, Bensadoun JC, Guillot S, Haase G, Szulc J, Henderson CE, Aebischer P 2005) Lentiviral-mediated silencing of sod1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat Med 11 : 423 428.
59. Ren G, Li T, Lan JQ, Wilz A, Simon RP, Boison D 2007) Lentiviral RNAi-induced downregulation of adenosine kinase in human mesenchymal stem cell grafts: a novel perspective for seizure control. Exp Neurol 208 : 26 37.
60. Riban V, Fitzsimons HL, During MJ 2009) Gene therapy in epilepsy. Epilepsia 50 : 24 32.
61. Rodriguez-Lebron E, Paulson HL 2006) Allele-specific RNA interference for neurological disease. Gene Ther 13 : 576 581.
62. Rodriguez-Lebron E, Gouvion CM, Moore SA, Davidson BL, Paulson HL 2009) Allele-specific RNAi mitigates phenotypic progression in a transgenic model of Alzheimer's disease. Mol Ther 17 : 1563 1573.
63. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD 2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115 : 199 208.
64. Sebastiao AM, Ribeiro JA 2009) Tuning and fine-tuning of synapses with adenosine. Curr Neuropharmacol 7 : 180 194.
65. Silva JM, Li MZ, Chang K, Ge W, Golding MC, Rickles RJ, Siolas D, Hu G, Paddison PJ, Schlabach MR, Sheth N, Bradshaw J, Burchard J, Kulkarni A, Cavet G, Sachidanandam R, McCombie WR, Cleary MA, Elledge SJ, Hannon GJ 2005) Second-generation shRNA libraries covering the mouse and human genomes. Nat Genet 37 : 1281 1288.
66. Singer O, Marr RA, Rockenstein E, Crews L, Coufal NG, Gage FH, Verma IM, Masliah E 2005) Targeting bace1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat Neurosci 8 : 1343 1349.
67. Stafstrom CE 2009) Severe epilepsy syndromes of early childhood: the link between genetics and pathophysiology with a focus on scn1a mutations. J Child Neurol 24 : 15S 23S.
68. Sugiyama O, An DS, Kung SPK, Feeley BT, Gamradt S, Liu NQ, Chen ISY, Lieberman JR 2005) Lentivirus-mediated gene transfer induces long-term transgene expression of bmp-2 in vitro and new bone formation in vivo. Mol Ther 11 : 390 398.
69. Sui G, Soohoo C, Affar el B, Gay F, Shi Y, Forrester WC 2002) A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc Natl Acad Sci U S A 99 : 5515 5520.
70. Taganov KD, Boldin MP, Chang KJ, Baltimore D 2006) NF-kappaB-dependent induction of microRNA mir-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A 103 : 12481 12486.
71. Tian L, Chen L, Yang T, Zhang Q, Zhou D 2009) RNAi inhibits Coriaria lactone-induced mdr1b overexpression in rat brain microvascular endothelial cells. J Mol Neurosci 39 : 284 293.
72. Totsugawa T, Kobayashi N, Okitsu T, Noguchi H, Watanabe T, Matsumura T, Maruyama M, Fujiwara T, Sakaguchi M, Tanaka N 2002) Lentiviral transfer of the LacZ gene into human endothelial cells and human bone marrow mesenchymal stem cells. Cell Transplant 11 : 481 488.
73. Tuschl T, Zamore PD, Lehmann R, Bartel DP, Sharp PA 1999) Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 13 : 3191 3197.
74. Vajda FJE 2007) Pharmacotherapy of epilepsy: new armamentarium, new issues. J Clin Neurosci 14 : 813 823.
75. Vashlishan AB, Madison JM, Dybbs M, Bai J, Sieburth D, Ch'ng Q, Tavazoie M, Kaplan JM 2008) An RNAi screen identifies genes that regulate GABA synapses. Neuron 58 : 346 361.
76. Wang Q, Carmichael GG 2004) Effects of length and location on the cellular response to double-stranded RNA. Microbiol Mol Biol Rev 68 : 432 452.
77. Wieser HG 2004) ILAE commission report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45 : 695 714.
78. Wolff JA, Budker V 2005) The mechanism of naked DNA uptake and expression. Adv Genet 54 : 3 20.
79. Xia H, Mao Q, Eliason SL, Harper SQ, Martins IH, Orr HT, Paulson HL, Yang L, Kotin RM, Davidson BL 2004) RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat Med 10 : 816 820.
80. Xiao X, Li J, McCown TJ, Samulski RJ 1997) Gene transfer by adeno-associated virus vectors into the central nervous system. Exp Neurol 144 : 113 124.