Novel combinations of phenotypic biomarkers predict development of epilepsy in the lithium-pilocarpine model of temporal lobe epilepsy in rats

Epilepsy and Behavior

Volumn 53, Issue , 2015, Pages 98-107

  Bröer, Sonja ^a   Löscher, Wolfgang ^b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

Behavior; Epileptogenesis; Seizure threshold; Seizures; Status epilepticus

Indexed keywords

BIOLOGICAL MARKER; LITHIUM CHLORIDE; PENTETRAZOLE; PILOCARPINE; LITHIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; APPROACH RESPONSE TEST; ARTICLE; BEHAVIOR ASSESSMENT; BEHAVIOR CHANGE; BODY WEIGHT; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; EPILEPTIC STATE; EPILEPTOGENESIS; EXCITABILITY; FEMALE; FINGER SNAP TEST; NONHUMAN; PHENOTYPE; PICK UP TEST; PROSPECTIVE STUDY; RAT; RECEIVER OPERATING CHARACTERISTIC; SEIZURE; SEIZURE THRESHOLD; SENSITIVITY AND SPECIFICITY; SPONTANEOUS RECURRENT SEIZURE; TEMPORAL LOBE EPILEPSY; TOUCH RESPONSE TEST; ANIMAL; BRAIN; CHEMICALLY INDUCED; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; MALE; PATHOPHYSIOLOGY; REACTION TIME;

ANIMALS; BIOMARKERS; BRAIN; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; FEMALE; LITHIUM; MALE; PENTYLENETETRAZOLE; PILOCARPINE; PROSPECTIVE STUDIES; RATS; REACTION TIME; ROC CURVE; SEIZURES; STATUS EPILEPTICUS;

EID: 84946401137     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2015.09.028     Document Type: Article

References (50)

1. Löscher W., Brandt C. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev 2010, 62:668-700.
2. Pitkänen A., Lukasiuk K. Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol 2011, 10:173-186.
3. Löscher W., Klitgaard H., Twyman R.E., Schmidt D. New avenues for antiepileptic drug discovery and development. Nat Rev Drug Discov 2013, 12:757-776.
4. Pitkänen A., Engel J. Past and present definitions of epileptogenesis and its biomarkers. Neurotherapeutics 2014, 11:231-241.
5. Engel J., Pitkänen A., Loeb J.A., Dudek F.E., Bertram E.H., Cole A.J., et al. Epilepsy biomarkers. Epilepsia 2013, 54(Suppl. 4):61-69.
6. Humpel C. Identifying and validating biomarkers for Alzheimer's disease. Trends Biotechnol 2011, 29:26-32.
7. Valdes P.A., Kim A., Leblond F., Conde O.M., Harris B.T., Paulsen K.D., et al. Combined fluorescence and reflectance spectroscopy for in vivo quantification of cancer biomarkers in low- and high-grade glioma surgery. J Biomed Opt 2011, 16:116007.
8. Atluri G., Padmanabhan K., Fang G., Steinbach M., Petrella J.R., Lim K., et al. Complex biomarker discovery in neuroimaging data: finding a needle in a haystack. Neuroimage Clin 2013, 3:123-131.
9. Rosen C., Hansson O., Blennow K., Zetterberg H. Fluid biomarkers in Alzheimer's disease - current concepts. Mol Neurodegener 2013, 8:20.
10. Diaz-Arrastia R., Wang K.K., Papa L., Sorani M.D., Yue J.K., Puccio A.M., et al. Acute biomarkers of traumatic brain injury: relationship between plasma levels of ubiquitin C-terminal hydrolase-L1 and glial fibrillary acidic protein. J Neurotrauma 2014, 31:19-25.
11. Di Battista A.P., Buonora J.E., Rhind S.G., Hutchison M.G., Baker A.J., Rizoli S.B., et al. Blood biomarkers in moderate-to-severe traumatic brain injury: potential utility of a multi-marker approach in characterizing outcome. Front Neurol 2015, 6:110.
12. Rattka M., Brandt C., Bankstahl M., Bröer S., Löscher W. Enhanced susceptibility to the GABA antagonist pentylenetetrazole during the latent period following a pilocarpine-induced status epilepticus in rats. Neuropharmacology 2011, 60:505-512.
13. Rattka M., Brandt C., Löscher W. Do proconvulsants modify or halt epileptogenesis? Pentylenetetrazole is ineffective in two rat models of temporal lobe epilepsy. Eur J Neurosci 2012, 36:2505-2520.
14. Töllner K., Brandt C., Töpfer M., Brunhofer G., Erker T., Gabriel M., et al. A novel prodrug-based strategy to increase effects of bumetanide in epilepsy. Ann Neurol 2014, 75:550-562.
15. Brandt C., Töllner K., Klee R., Bröer S., Löscher W. Effective termination of status epilepticus by rational polypharmacy in the lithium-pilocarpine model in rats: window of opportunity to prevent epilepsy and prediction of epilepsy by biomarkers. Neurobiol Dis 2015, 75:78-90.
16. Löscher W. Preclinical assessment of proconvulsant drug activity and its relevance for predicting adverse events in humans. Eur J Pharmacol 2009, 610:1-11.
17. Kharatishvili I., Pitkänen A. Association of the severity of cortical damage with the occurrence of spontaneous seizures and hyperexcitability in an animal model of posttraumatic epilepsy. Epilepsy Res 2010, 90:47-59.
18. Bolkvadze T., Pitkänen A. Development of post-traumatic epilepsy after controlled cortical impact and lateral fluid-percussion-induced brain injury in the mouse. J Neurotrauma 2012, 29:789-812.
19. Brima T., Otahal J., Mares P. Increased susceptibility to pentetrazol-induced seizures in developing rats after cortical photothrombotic ischemic stroke at P7. Brain Res 2013, 1507:146-153.
20. Mishra A.M., Bai X., Sanganahalli B.G., Waxman S.G., Shatillo O., Grohn O., et al. Decreased resting functional connectivity after traumatic brain injury in the rat. PLoS One 2014, 9:e95280.
21. So N., Gloor P., Quesney L.F., Jones-Gotman M., Olivier A., Andermann F. Depth electrode investigations in patients with bitemporal epileptiform abnormalities. Ann Neurol 1989, 25:423-431.
22. Kandratavicius L., Balista P.A., Lopes-Aguiar C., Ruggiero R.N., Umeoka E.H., Garcia-Cairasco N., et al. Animal models of epilepsy: use and limitations. Neuropsychiatr Dis Treat 2014, 10:1693-1705.
23. Kücker S., Töllner K., Piechotta M., Gernert M. Kindling as a model of temporal lobe epilepsy induces bilateral changes in spontaneous striatal activity. Neurobiol Dis 2010, 37:661-672.
24. Curia G., Longo D., Biagini G., Jones R.S., Avoli M. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 2008, 172:143-157.
25. Glien M., Brandt C., Potschka H., Voigt H., Ebert U., Löscher W. Repeated low-dose treatment of rats with pilocarpine: low mortality but high proportion of rats developing epilepsy. Epilepsy Res 2001, 46:111-119.
26. Rice A.C., Floyd C.L., Lyeth B.G., Hamm R.J., DeLorenzo R.J. Status epilepticus causes long-term NMDA receptor-dependent behavioral changes and cognitive deficits. Epilepsia 1998, 39:1148-1157.
27. Bröer S., Zolkowska D., Gernert M., Rogawski M.A. Proconvulsant actions of intrahippocampal botulinum neurotoxin B in the rat. Neuroscience 2013, 252:253-261.
28. Rattka M., Brandt C., Löscher W. The intrahippocampal kainate model of temporal lobe epilepsy revisited: epileptogenesis, behavioral and cognitive alterations, pharmacological response, and hippoccampal damage in epileptic rats. Epilepsy Res 2013, 103:135-152.
29. Bröer S., Backofen-Wehrhahn B., Bankstahl M., Gey L., Gernert M., Löscher W. Vigabatrin for focal drug delivery in epilepsy: bilateral microinfusion into the subthalamic nucleus is more effective than intranigral or systemic administration in a rat seizure model. Neurobiol Dis 2012, 46:362-376.
30. Pollack G.M., Shen D.D. A timed intravenous pentylenetetrazol infusion seizure model for quantitating the anticonvulsant effect of valproic acid in the rat. J Pharmacol Methods 1985, 13:135-146.
31. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Elsevier, Amsterdam. 6th ed.
32. Soreide K. Receiver-operating characteristic curve analysis in diagnostic, prognostic and predictive biomarker research. J Clin Pathol 2009, 62:1-5.
33. Brandt C., Nozadze M., Heuchert N., Rattka M., Löscher W. Disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy. J Neurosci 2010, 30:8602-8612.
34. Honndorf S., Lindemann C., Tollner K., Gernert M. Female Wistar rats obtained from different breeders vary in anxiety-like behavior and epileptogenesis. Epilepsy Res 2011, 94:26-38.
35. Langer M., Brandt C., Löscher W. Marked strain and substrain differences in induction of status epilepticus and subsequent development of neurodegeneration, epilepsy, and behavioral alterations in rats. Epilepsy Res 2011, 96:207-224.
36. Choy M., Dube C.M., Patterson K., Barnes S.R., Maras P., Blood A.B., et al. A novel, noninvasive, predictive epilepsy biomarker with clinical potential. J Neurosci 2014, 34:8672-8684.
37. Immonen R., Kharatishvili I., Grohn O., Pitkanen A. MRI biomarkers for post-traumatic epileptogenesis. J Neurotrauma 2013, 30:1305-1309.
38. Pitkänen A., Bolkvadze T. Head trauma and epilepsy. Jasper's Basic Mechanisms of the Epilepsies 2012, 1-14. National Center for Biotechnology Information, Bethesda (MD). 4th ed. J.L. Noebels, M. Avoli, M.A. Rogawski, R.W. Olsen, A.V. Delgado-Escueta (Eds.).
39. Gloor P. Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. Brain 1990, 113(Pt 6):1673-1694.
40. Fish D.R., Gloor P., Quesney F.L., Olivier A. Clinical responses to electrical brain stimulation of the temporal and frontal lobes in patients with epilepsy. Pathophysiological implications. Brain 1993, 116(Pt 2):397-414.
41. Cherlow D.G., Dymond A.M., Crandall P.H., Walter R.D., Serafetinides E.A. Evoked response and after-discharge thresholds to electrical stimulation in temporal lobe epileptics. Arch Neurol 1977, 34:527-531.
42. Kanner A.M., Mazarati A., Koepp M. Biomarkers of epileptogenesis: psychiatric comorbidities (?). Neurotherapeutics 2014, 11:358-372.
43. Schwarzbold M., Diaz A., Martins E.T., Rufino A., Amante L.N., Thais M.E., et al. Psychiatric disorders and traumatic brain injury. Neuropsychiatr Dis Treat 2008, 4:797-816.
44. Brandt C., Gastens A.M., Sun M.Z., Hausknecht M., Löscher W. Treatment with valproate after status epilepticus: effect on neuronal damage, epileptogenesis, and behavioral alterations in rats. Neuropharmacology 2006, 51:789-804.
45. Faure J.B., Akimana G., Carneiro J.E., Cosquer B., Ferrandon A., Geiger K., et al. A comprehensive behavioral evaluation in the lithium-pilocarpine model in rats: effects of carisbamate administration during status epilepticus. Epilepsia 2013, 54:1203-1213.
46. Grund B., Sabin C. Analysis of biomarker data: logs, odds ratios, and receiver operating characteristic curves. Curr Opin HIV AIDS 2010, 5:473-479.
47. White H.S., Löscher W. Searching for the ideal antiepileptogenic agent in experimental models: single treatment versus combinatorial treatment strategies. Neurotherapeutics 2014, 11:373-384.
48. Kimiskidis V.K., Valentin A., Kalviainen R. Transcranial magnetic stimulation for the diagnosis and treatment of epilepsy. Curr Opin Neurol 2014, 27:236-241.
49. Bauer P.R., Kalitzin S., Zijlmans M., Sander J.W., Visser G.H. Cortical excitability as a potential clinical marker of epilepsy: a review of the clinical application of transcranial magnetic stimulation. Int J Neural Syst 2014, 24:1430001.
50. Hsieh T.H., Dhamne S.C., Chen J.J., Pascual-Leone A., Jensen F.E., Rotenberg A. A new measure of cortical inhibition by mechanomyography and paired-pulse transcranial magnetic stimulation in unanesthetized rats. J Neurophysiol 2012, 107:966-972.