Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model

Experimental Neurology

Volumn 182, Issue 1, 2003, Pages 21-34

  Borges, Karin ^a   Gearing, Marla ^b   McDermott, Dayna L ^a   Smith, Amy B ^a   Almonte, Antoine G ^a   Wainer, Bruce H ^b   Dingledine, Raymond ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Amyloid precursor protein; Astrocyte; Axonal degeneration; Epilepsy; Hippocampus; Microglia; Neurodegeneration; Neuropeptide Y; Seizure; Thalamus; 2 Microglobulin

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA 2 MICROGLOBULIN; NEUROPEPTIDE Y; PILOCARPINE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN NERVE CELL; CELL DEATH; CONTROLLED STUDY; EPILEPTIC STATE; EPILEPTOGENESIS; HIPPOCAMPUS; IMMUNOREACTIVITY; MICROGLIA; MOSSY FIBER; MOUSE; NERVE FIBER DEGENERATION; NERVE SPROUTING; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEIZURE; THALAMUS; UPREGULATION;

EID: 0038434119     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00086-4     Document Type: Article

References (53)

1. Andersson P.B., Perry V.H., Gordon S. The kinetics and morphological characteristics of the macrophage-microglial response to kainic acid-induced neuronal degeneration. Neuroscience. 42:1991;201-214.
2. Aschner M., Allen J.W., Kimelberg H.K., LoPachin R.M., Streit W.J. Glial cells in neurotoxicity development. Annu. Rev. Pharmacol. Toxicol. 39:1999;151-173.
3. Baraban S.C., Hollopeter G., Erickson J.C., Schwartzkroin P.A., Palmiter R.D. Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J. Neurosci. 17:1997;8927-8936.
4. Barone P., Morelli M., Cicarelli G., Cozzolino A., DeJoanna G., Campanella G., DiChiara G. Expression of c-fos protein in the experimental epilepsy induced by pilocarpine. Synapse. 14:1993;1-9.
5. Barres B.A., Barde Y. Neuronal and glial cell biology. Curr. Opin. Neurobiol. 10:2000;642-648.
6. Beach T.G., Woodhurst W.B., MacDonald D.B., Jones M.W. Reactive microglia in hippocampal sclerosis associated with human temporal lobe epilepsy. Neurosci. Lett. 191:1995;27-30.
7. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid mechanisms and relevance to human temporal lobe epilepsy . Neuroscience. 14:1985;375-403.
8. Berkeley J.L., Decker M.J., Levey A.I. The role of muscarinic acetylcholine receptor-mediated activation of extracellular signal-regulated kinase 1/2 in pilocarpine-induced seizures. J. Neurochem. 82:2002;192-201.
9. Bouilleret V., Loup F., Kiener T., Marescaux C., Fritschy J.M. Early loss of interneurons and delayed subunit-specific changes in GABA(A)-receptor expression in a mouse model of mesial temporal lobe epilepsy. Hippocampus. 10:2000;305-324.
10. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy . Neuroscience. 89:1999;717-729.
11. Buckmaster P.S., Dudek F.E. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol. 385:1997;385-404.
12. Buckmaster P.S., Otero-Corchon V., Rubinstein M., Low M.J. Heightened seizure severity in somatostatin knockout mice. Epilepsy Res. 48:2002;43-56.
13. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., Turski W.A., Ikonomidou C., Turski L. Long-term effects of pilocarpine in rats structural damage of the brain triggers kindling and spontaneous recurrent seizures . Epilepsia. 32:1991;778-782.
14. Cavalheiro E.A., Santos N.F., Priel M.R. The pilocarpine model of epilepsy in mice. Epilepsia. 37:1996;1015-1019.
15. Chafetz R.S., Nahm W.K., Noebels J.L. Aberrant expression of neuropeptide Y in hippocampal mossy fibers in the absence of local cell injury following the onset of spike-wave synchronization. Brain Res. Mol. Brain Res. 31:1995;111-121.
16. Covolan L., Mello L.E. Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res. 39:2000;133-152.
17. Deasy N.P., Jarosz J.M., Elwes R.C., Polkey C.E., Cox T.C. Thalamic changes with mesial temporal sclerosis MRI . Neuroradiology. 42:2000;346-351.
18. Dolinak D., Smith C., Graham D.I. Global hypoxia per se is an unusual cause of axonal injury. Acta Neuropathol. 100:2000;553-560.
19. Frankel W.N., Taylor L., Beyer B., Tempel B.L., White H.S. Electroconvulsive thresholds of inbred mouse strains. Genomics. 74:2001;306-312.
20. Furtinger S., Pirker S., Czech T., Baumgartner C., Ransmayr G., Sperk G. Plasticity of Y1 and Y2 receptors and neuropeptide Y fibers in patients with temporal lobe epilepsy. J. Neurosci. 21:2001;5804-5812.
21. Gearing M., Wilson R.W., Unger E.R., Shelton E.R., Chan H.W., Masters C.L., Beyrcuther K., Mirra S.S. Amyloid precursor protein (APP) in the striatum in Alzheimer's disease an immunohistochemical study . J. Neuropathol. Exp. Neurol. 52:1993;22-30.
22. Gorter J.A., van Vliet E.A., Aronica E., Lopes da Silva F.H. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur. J. Neurosci. 13:2001;657-669.
23. Hanisch U.K. Microglia as a source and target of cytokines. Glia. 40:2002;140-155.
24. Hof P., Young W.G., Bloom F.E., Belichenko P.V., Celio M.R. Comparative Cytoarchitonic Atlas of the C57BL/6 and 129/Sv Mouse Brains. 2000;Elsevier, New York.
25. Houser C.R. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res. Suppl. 7:1992;223-234.
26. Jankowsky J.L., Patterson P.H. The role of cytokines and growth factors in seizures and their sequelae. Prog. Neurobiol. 63:2001;125-149.
27. Kawarabayashi T., Shoji M., Harigaya Y., Yamaguchi H., Hirai S. Expression of APP in the early stage of brain damage. Brain Res. 563:1991;334-338.
28. Magloczky Z., Wittner L., Borhegyi Z., Halasz P., Vajda J., Czirjak S., Freund T.F. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience. 96:2000;7-25.
29. Martin J.L., Sloviter R.S. Focal inhibitory interneuron loss and principal cell hyperexcitability in the rat hippocampus after microinjection of a neurotoxic conjugate of saporin and a peptidase-resistant analog of Substance P. J. Comp. Neurol. 436:2001;127-152.
30. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy cell loss and mossy fiber sprouting . Epilepsia. 34:1993;985-995.
31. Mraovitch S., Calando Y. Interactions between limbic, thalamo-striatal-cortical, and central autonomic pathways during epileptic seizure progression. J. Comp. Neurol. 411:1999;145-161.
32. Penkowa M., Molinero A., Carrasco J., Hidalgo J. Interleukin-6 deficiency reduces the brain inflammatory response and increases oxidative stress and neurodegeneration after kainic acid-induced seizures. Neuroscience. 102:2001;805-818.
33. Peredery O., Persinger M.A., Parker G., Mastrosov L. Temporal changes in neuronal dropout following inductions of lithium/pilocarpine seizures in the rat. Brain Res. 881:2000;9-17.
34. Pfrieger F.W., Barres B.A. New views on synapse-glia interactions. Curr. Opin. Neurobiol. 6:1996;615-621.
35. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32:1972;281-294.
36. Rogove A.D., Tsirka S.E. Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr. Biol. 8:1998;19-25.
37. Scharfman H.E., Goodman J.H., Sollas A.L. Actions of brain-derived neurotrophic factor in slices from rats with spontaneous seizures and mossy fiber sprouting in the dentate gyrus. J. Neurosci. 19:1999;5619-5631.
38. Schauwecker P.E. Complications associated with genetic background effects in models of experimental epilepsy. Prog. Brain Res. 135:2002;139-148.
39. Schauwecker P.E., Steward O. Genetic determinants of susceptibility to excitotoxic cell death implications for gene targeting approaches . Proc. Natl. Acad. Sci. USA. 94:1997;4103-4108.
40. Schell M.J., Molliver M.E., Snyder S.H. D-serine, an endogenous synaptic modulator localization to astrocytes and glutamate-stimulated release . Proc. Natl. Acad. Sci. USA. 92:1995;3948-3952.
41. Schwarzer C., Williamson J.M., Lothman E.W., Vezzani A., Sperk G. Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience. 69:1995;831-845.
42. Sheng J.G., Boop F.A., Mrak R.E., Griffin W.S. Increased neuronal beta-amyloid precursor protein expression in human temporal lobe epilepsy association with interleukin-1 alpha immunoreactivity . J. Neurochem. 63:1994;1872-1879.
43. Sherriff F.E., Bridges L.R., Sivaloganathan S. Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol. 87:1994;55-62.
44. Shibley H., Smith B.N. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res. 49:2002;109-120.
45. Stone J.R., Walker S.A., Povlishock J.T. The visualization of a new class of traumatically injured axons through the use of a modified method of microwave antigen retrieval. Acta Neuropathol. 97:1999;335-345.
46. Suzuki F., Junier M.P., Guilhem D., Sorensen J.C., Onteniente B. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor. Neuroscience. 64:1995;665-674.
47. Turski W.A., Cavalheiro E.A., Bortolotto Z.A., Mello L.M., Schwarz M., Turski L. Seizures produced by pilocarpine in mice a behavioral, electroencephalographic and morphological analysis . Brain Res. 321:1984;237-253.
48. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., Turski L. Limbic seizures produced by pilocarpine in rats behavioral, electroencephalographic and neuropathological study . Behav. Brain Res. 9:1983;315-335.
49. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F., De Simoni M.G. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application functional evidence for enhancement of electrographic seizures . J. Neurosci. 19:1999;5054-5065.
50. Vezzani A., Michalkiewicz M., Michalkiewicz T., Moneta D., Ravizza T., Richichi C., Aliprandi M., Mule F., Pirona L., Gobbi M., Schwarzer C., Sperk G. Seizure susceptibility and epileptogenesis are decreased in transgenic rats overexpressing neuropeptide Y. Neuroscience. 110:2002;237-243.
51. Vezzani A., Sperk G., Colmers W.F. Neuropeptide Y emerging evidence for a functional role in seizure modulation . Trends Neurosci. 22:1999;25-30.
52. Yang G., Kitagawa K., Matsushita K., Mabuchi T., Yagita Y., Yanagihara T., Matsumoto M. C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains selective neuronal death in the murine transient forebrain ischemia . Brain Res. 752:1997;209-218.
53. Zhang X., Cui S.S., Wallace A.E., Hannesson D.K., Schmued L.C., Saucier D.M., Honer W.G., Corcoran M.E. Relations between brain pathology and temporal lobe epilepsy. J. Neurosci. 22:2002;6052-6061.