Epilepsy: Optogenetic and potassium channel gene therapy in a rodent model of focal neocortical epilepsy

Science Translational Medicine

Volumn 4, Issue 161, 2012, Pages

  Wykes, Robert C ^a   Heeroma, Joost H ^a   Mantoan, Laura ^a   Zheng, Kaiyu ^a   MacDonald, Douglas C ^b   Deisseroth, Karl ^c   Hashemi, Kevan S ^d   Walker, Matthew C ^a   Schorge, Stephanie ^a   Kullmann, Dimitri M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Stanford University   (United States)

^d OpenSource Instruments Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE 67; HALORHODOPSIN; LENTIVIRUS VECTOR; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV1.1; TETANUS TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ELECTROENCEPHALOGRAM; EPILEPTIC FOCUS; EPILEPTOGENESIS; FOCAL EPILEPSY; GENE THERAPY; HIPPOCAMPUS; LOCOMOTION; MALE; MOTOR CORTEX; NEOCORTICAL EPILEPSY; NERVE CELL EXCITABILITY; NONHUMAN; OPTOGENETIC; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SEIZURE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DISEASE MODEL; ELECTROENCEPHALOGRAPHY; GENETICS; LENTIVIRINAE; METABOLISM; NEOCORTEX; NERVE CELL; OPTOGENETICS; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSIES, PARTIAL; GENETIC THERAPY; KV1.1 POTASSIUM CHANNEL; LENTIVIRUS; MALE; NEOCORTEX; NEURONS; OPTOGENETICS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; TETANUS TOXIN;

EID: 84869795204     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3004190     Document Type: Article

References (57)

1. A. K. Ngugi, C. Bottomley, I. Kleinschmidt, J. W. Sander, C. R. Newton, Estimation of the burden of active and life-time epilepsy: A meta-analytic approach. Epilepsia 51, 883-890 (2010).
2. P. Kwan, S. C. Schachter, M. J. Brodie, Drug-resistant epilepsy. N. Engl. J. Med. 365, 919-926 (2011).
3. J. F. Annegers, W. A. Hauser, L. R. Elveback, Remission of seizures and relapse in patients with epilepsy. Epilepsia 20, 729-737 (1979).
4. Jasper's Basic Mechanisms of the Epilepsies-NCBI Bookshelf; http://www.ncbi.nlm.nih.gov/books/NBK50785/.
5. F. Rosenow, H. Lüders, Presurgical evaluation of epilepsy. Brain 124, 1683-1700 (2001).
6. S. U. Schuele, H. O. Lüders, Intractable epilepsy: Management and therapeutic alternatives. Lancet Neurol. 7, 514-524 (2008).
7. J. de Tisi, G. S. Bell, J. L. Peacock, A. W. McEvoy, W. F. Harkness, J. W. Sander, J. S. Duncan, The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: A cohort study. Lancet 378, 1388-1395 (2011).
8. P. Kahane, A. Depaulis, Deep brain stimulation in epilepsy: What is next? Curr. Opin. Neurol. 23, 177-182 (2010).
9. E. H. Kossoff, A. L. Hartman, Ketogenic diets: New advances for metabolism-based therapies. Curr. Opin. Neurol. 25, 173-178 (2012).
10. P. Boon, R. Raedt, V. de Herdt, T. Wyckhuys, K. Vonck, Electrical stimulation for the treatment of epilepsy. Neurotherapeutics 6, 218-227 (2009).
11. O. Devinsky, Sudden, unexpected death in epilepsy. N. Engl. J. Med. 365, 1801-1811 (2011).
12. C. Hoppe, C. E. Elger, Depression in epilepsy: A critical review from a clinical perspective. Nat. Rev. Neurol. 7, 462-472 (2011).
13. C. Richichi, E. J. Lin, D. Stefanin, D. Colella, T. Ravizza, G. Grignaschi, P. Veglianese, G. Sperk, M. J. During, A. Vezzani, Anticonvulsant and antiepileptogenic effects mediated by adenoassociated virus vector neuropeptide Y expression in the rat hippocampus. J. Neurosci. 24, 3051-3059 (2004).
14. D. P. Woldbye, M. Angehagen, C. R. Gøtzsche, H. Elbrønd-Bek, A. T. Sørensen, S. H. Christiansen, M. V. Olesen, L. Nikitidou, T. V. Hansen, I. Kanter-Schlifke, M. Kokaia, Adeno-associated viral vector-induced overexpression of neuropeptide Y Y2 receptors in the hippocampus suppresses seizures. Brain 133, 2778-2788 (2010).
15. R. P. Haberman, R. J. Samulski, T. J. McCown, Attenuation of seizures and neuronal death by adeno-associated virus vector galanin expression and secretion. Nat. Med. 9, 1076-1080 (2003).
16. E. J. D. Lin, D. Young, K. Baer, H. Herzog, M. J. During, Differential actions of NPY on seizure modulation via Y1 and Y2 receptors: Evidence from receptor knockout mice. Epilepsia 47, 773-780 (2006).
17. T. J. McCown, Adeno-associated virus-mediated expression and constitutive secretion of galanin suppresses limbic seizure activity in vivo. Mol. Ther. 14, 63-68 (2006).
18. I. Kanter-Schlifke, B. Georgievska, D. Kirik, M. Kokaia, Seizure suppression by GDNF gene therapy in animal models of epilepsy. Mol. Ther. 15, 1106-1113 (2007).
19. R. Bovolenta, S. Zucchini, B. Paradiso, D. Rodi, F. Merigo, G. Navarro Mora, F. Osculati, E. Berto, P. Marconi, A. Marzola, P. F. Fabene, M. Simonato, Hippocampal FGF-2 and BDNF overexpression attenuates epileptogenesis-associated neuroinflammation and reduces spontaneous recurrent seizures. J. Neuroinflammation 7, 81 (2010).
20. F. Noè, A. H. Pool, J. Nissinen, M. Gobbi, R. Bland, M. Rizzi, C. Balducci, F. Ferraguti, G. Sperk, M. J. During, A. Pitkänen, A. Vezzani, Neuropeptide Y gene therapy decreases chronic spontaneous seizures in a rat model of temporal lobe epilepsy. Brain 131, 1506-1515 (2008).
21. E. D. Louis, P. D. Williamson, T. M. Darcey, Chronic focal epilepsy induced by microinjection of tetanus toxin into the cat motor cortex. Electroencephalogr. Clin. Neurophysiol. 75, 548-557 (1990).
22. K. E. Nilsen, M. C. Walker, H. R. Cock, Characterization of the tetanus toxin model of refractory focal neocortical epilepsy in the rat. Epilepsia 46, 179-187 (2005).
23. O. C. Cockerell, J. Rothwell, P. D. Thompson, C. D. Marsden, S. D. Shorvon, Clinical and physiological features of epilepsia partialis continua. Cases ascertained in the UK. Brain 119 (Pt. 2), 393-407 (1996).
24. P. Chang, K. S. Hashemi, M. C. Walker, A novel telemetry system for recording EEG in small animals. J. Neurosci. Methods 201, 106-115 (2011).
25. J. A. Blanco, M. Stead, A. Krieger, W. Stacey, D. Maus, E. Marsh, J. Viventi, K. H. Lee, R. Marsh, B. Litt, G. A. Worrell, Data mining neocortical high-frequency oscillations in epilepsy and controls. Brain 134, 2948-2959 (2011).
26. S. J. Korn, J. L. Giacchino, N. L. Chamberlin, R. Dingledine, Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. J. Neurophysiol. 57, 325-340 (1987).
27. G. Hagemann, M. Hoeller, C. Bruehl, M. Lutzenburg, O. W. Witte, Effects of tetanus toxin on functional inhibition after injection in separate cortical areas in rat. Brain Res. 818, 127-134 (1999).
28. M. Vreugdenhil, S. P. Hack, A. Draguhn, J. G. Jefferys, Tetanus toxin induces long-term changes in excitation and inhibition in the rat hippocampal CA1 area. Neuroscience 114, 983-994 (2002).
29. M. Mainardi, M. Pietrasanta, E. Vannini, O. Rossetto, M. Caleo, Tetanus neurotoxin-induced epilepsy in mouse visual cortex. Epilepsia 53, e132-e136 (2012).
30. A. Groh, H. S. Meyer, E. F. Schmidt, N. Heintz, B. Sakmann, P. Krieger, Cell-type specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. Cereb. Cortex 20, 826-836 (2010).
31. H. Beck, Y. Yaari, Plasticity of intrinsic neuronal properties in CNS disorders. Nat. Rev. Neurosci. 9, 357-369 (2008).
32. J. Tønnesen, A. T. Sørensen, K. Deisseroth, C. Lundberg, M. Kokaia, Optogenetic control of epileptiform activity. Proc. Natl. Acad. Sci. U.S.A. 106, 12162-12167 (2009).
33. F. Zhang, L. P. Wang, M. Brauner, J. F. Liewald, K. Kay, N. Watzke, P. G. Wood, E. Bamberg, G. Nagel, A. Gottschalk, K. Deisseroth, Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639 (2007).
34. J. V. Raimondo, L. Kay, T. J. Ellender, C. J. Akerman, Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission. Nat. Neurosci. 15, 1102-1104 (2012).
35. A. E. Metz, N. Spruston, M. Martina, Dendritic D-type potassium currents inhibit the spike after depolarization in rat hippocampal CA1 pyramidal neurons. J. Physiol. 581, 175-187 (2007).
36. J. F. van Brederode, J. M. Rho, R. Cerne, B. L. Tempel, W. J. Spain, Evidence of altered inhibition in layer V pyramidal neurons from neocortex of Kcna1-null mice. Neuroscience 103, 921-929 (2001).
37. J. M. Bekkers, A. J. Delaney, Modulation of excitability by a-dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons. J. Neurosci. 21, 6553-6560 (2001).
38. J. H. Heeroma, C. Henneberger, S. Rajakulendran, M. G. Hanna, S. Schorge, D. M. Kullmann, Episodic ataxia type 1 mutations differentially affect neuronal excitability and transmitter release. Dis. Model Mech. 2, 612-619 (2009).
39. A. S. Galanopoulou, P. S. Buckmaster, K. J. Staley, S. L. Moshé, E. Perucca, J. Engel Jr., W. Löscher, J. L. Noebels, A. Pitkänen, J. Stables, H. S. White, T. J. O'Brien, M. Simonato; American Epilepsy Society Basic Science Committee And The International League Against Epilepsy Working Group On Recommendations For Preclinical Epilepsy Drug Discovery, Identification of new epilepsy treatments: Issues in preclinical methodology. Epilepsia 53, 571-582 (2012).
40. A. Bragin, J. Engel Jr., R. J. Staba, High-frequency oscillations in epileptic brain. Curr. Opin. Neurol. 23, 151-156 (2010).
41. G. A. Worrell, L. Parish, S. D. Cranstoun, R. Jonas, G. Baltuch, B. Litt, High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 127, 1496-1506 (2004).
42. S. M. Rothman, The therapeutic potential of focal cooling for neocortical epilepsy. Neurotherapeutics 6, 251-257 (2009).
43. J. D. Heiss, S. Walbridge, A. R. Asthagiri, R. R. Lonser, Image-guided convection-enhanced delivery of muscimol to the primate brain. J. Neurosurg. 112, 790-795 (2010).
44. E. M. Slimko, S. McKinney, D. J. Anderson, N. Davidson, H. A. Lester, Selective electrical silencing of mammalian neurons in vitro by the use of invertebrate ligand-gated chloride channels. J. Neurosci. 22, 7373-7379 (2002).
45. G. G. Turrigiano, The self-tuning neuron: Synaptic scaling of excitatory synapses. Cell 135, 422-435 (2008).
46. G. Schiavo, F. Benfenati, B. Poulain, O. Rossetto, P. Polverino de Laureto, B. R. DasGupta, C. Montecucco, Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835 (1992).
47. 2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J. Neurosci. 22, 3645-3655 (2002).
48. M. M. Shah, A. E. Anderson, V. Leung, X. Lin, D. Johnston, Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44, 495-508 (2004).
49. C. Bernard, A. Anderson, A. Becker, N. P. Poolos, H. Beck, D. Johnston, Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532-535 (2004).
50. P. A. Castro, E. C. Cooper, D. H. Lowenstein, S. C. Baraban, Hippocampal heterotopia lack functional Kv4.2 potassium channels in the methylazoxymethanol model of cortical malformations and epilepsy. J. Neurosci. 21, 6626-6634 (2001).
51. P. C. Bush, D. A. Prince, K. D. Miller, Increased pyramidal excitability and NMDA conductance can explain posttraumatic epileptogenesis without disinhibition: A model. J. Neurophysiol. 82, 1748-1758 (1999).
52. L. Topolnik, M. Steriade, I. Timofeev, Hyperexcitability of intact neurons underlies acute development of trauma-related electrographic seizures in cats in vivo. Eur. J. Neurosci. 18, 486-496 (2003).
53. M.M. Jagodic, S. Pathirathna, M. T. Nelson, S. Mancuso, P. M. Joksovic, E. R. Rosenberg, D. A. Bayliss, V. Jevtovic-Todorovic, S. M. Todorovic, Cell-specific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons. J. Neurosci. 27, 3305-3316 (2007).
54. H. J. Hu, Y. Carrasquillo, F. Karim, W. E. Jung, J. M. Nerbonne, T. L. Schwarz, R. W. Gereau IV, The kv4.2 potassium channel subunit is required for pain plasticity. Neuron 50, 89-100 (2006).
55. R. Wykes, A. Kalmbach, M. Eliava, J. Waters, Changes in the physiology of CA1 hippocampal pyramidal neurons in preplaque CRND8 mice. Neurobiol. Aging 33, 1609-1623 (2012).
56. D. C. Rogers, C. A. Campbell, J. L. Stretton, K. B. Mackay, Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 28, 2060-2065 (1997).
57. T. Hedrick, J. Waters, Spiking patterns of neocortical L5 pyramidal neurons in vitro change with temperature. Front. Cell. Neurosci. 5, 1 (2011).