Physical exercise improves learning by modulating hippocampal mossy fiber sprouting and related gene expression in a developmental rat model of penicillin-induced recurrent epilepticus

Toxicology Letters

Volumn 191, Issue 1, 2009, Pages 26-32

  Ni, Hong ^a   Li, Chao ^a   Tao, Lu yuang ^a   Cen, Jian nong ^a  

^a CHILDREN S HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

CCK; GABA; Glutamate; Mossy fiber spouting; Physical exercise; Seizure

Indexed keywords

4 AMINOBUTYRIC ACID A ALPHA3; CHOLECYSTOKININ; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; OMEGA AMINO ACID; PENICILLIN G; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; EPILEPSY; GENE EXPRESSION; HIPPOCAMPUS; HISTOPATHOLOGY; LEARNING; MALE; MAZE TEST; NERVE SPROUTING; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; TREADMILL EXERCISE;

ANIMALS; CHOLECYSTOKININ; COLORING AGENTS; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; LEARNING; MALE; MAZE LEARNING; MOSSY FIBERS, HIPPOCAMPAL; NERVE REGENERATION; PENICILLINS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

RATTUS;

EID: 70350613336     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2009.07.028     Document Type: Article

References (40)

1. Arida R.M., Scorza F.A., de Lacerda A.F., G. da Silva S., and Cavalheiro E.A. Physical training in developing rats does not influence the kindling development in the adult life. Physiol. Behav. 90 4 (2007) 629-633
2. Arida R.M., Scorza F.A., Scorza C.A., and Cavalheiro E.A. Is physical activity beneficial for recovery in temporal lobe epilepsy? Evidences from animal studies. Neurosci. Biobehav. Rev. 33 3 (2009) 422-431
3. Brauer A.U., Savaskan N.E., and Plaschke M. Cholecystokinin expression after hippocampal deafferentiation: molecular evidence revealed by differential display-reverse transcription-polymerase chain reaction. Neuroscience 121 1 (2003) 111-121
4. Chen H.I., Lin L.C., and Yu L. Treadmill exercise enhances passive avoidance learning in rats: the role of down-regulated serotonin system in the limbic system. Neurobiol. Learn. Mem. 89 (2008) 489-496
5. Deshpande L.S., Lou J.K., Mian A., Blair R.E., Sombati S., Attkisson E., and DeLorenzo R.J. Time course and mechanism of hippocampal neuronal death in an in vitro model of status epilepticus: role of NMDA receptor activation and NMDA dependent calcium entry. Eur. J. Pharmacol. 583 1 (2008) 73-83
6. de Lanerolle N.C., Eid T., von Campe G., Kovacs I., Spencer D.D., and Brines M.L. Glutamate receptor subunits GluR1 and GluR2/3 distribution shows reorganization in the human epileptogenic hippocampus. Eur. J. Neurosci. 10 5 (1998) 1687-1703
7. Dulac O., Nabbout R., and Plouin P. Early seizures: causal events or predisposition to adult epilepsy?. Lancet Neurol. 6 7 (2007) 643-651
8. Hellier J.L., White A., Williams P.A., Edward Dudek F., and Staley K.J. NMDA receptor-mediated long-term alterations in epileptiform activity in experimental chronic epilepsy. Neurophamacology 56 2 (2009) 414-421
9. Eid T., Kovacs I., Spencer D.D., and De Lanerolle N.C. Novel expression of AMPA-receptor subunit GluR1 on mossy cells and CA3 pyramidal neurons in human epileptogenic hippocampus. Eur. J. Neurosci. 15 3 (2002) 517-527
10. Friedman L.K., Avallone J.M., and Magrys B. Maturational effects of single and multiple early-life seizures on AMPA receptors in prepubescent hippocampus. Dev. Neurosci. 29 6 (2007) 427-437
11. Gobbo O.L., and O'Mara S.M. Exercise, but not environmental enrichment, improves learning after kainic acid-induced hippocampal neurodegeneration in association with an increase in brain-derived neurotrophic factor. Behav. Brain Res. 159 1 (2005) 21-26
12. Griesbach G.S., Gómez-Pinilla F.D., and Hovda A. Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. J. Neurotrauma 24 7 (2007) 1161-1171
13. Grooms S.Y., Opitz T., Bennett M.V.L., and Zukin R.S. Status epilepticus decreases glutamate receptor 2 mRNA and protein expression in hippocampal pyramidal cells before neuronal death. Proc. Natl. Acad. Sci. U.S.A. 97 7 (2000) 3631-3636
14. Holmes G.L. Effects of seizures on brain development: lessons from the laboratory. Pediatr. Neurol. 33 1 (2005) 1-11
15. Holopainen I.E. Seizures in the developing brain: cellular and molecular mechanisms of neuronal damage, neurogenesis and cellular reorganization. Neurochem. Int. 52 6 (2008) 935-947
16. Johnson M.R., Wang K., Smith J.B., Heslin M.J., and Diasio R.B. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal. Biochem. 278 2 (2000) 175-184
17. Kamphuis W., De Rijk T.C., Talamini L.M., and Lopes da Silva F.H. Rat hippocampal kindling induces changes in the glutamate receptor mRNA expression patterns in dentate granule neurons. Eur. J. Neurosci. 6 7 (1994) 1119-1127
18. Kim D.Y., Kim S.H., Choi H.B., Min C., and Gwaq B.J. High abundance of GluR1 mRNA and reduced Q/R editing of GluR2 mRNA in individual NADPH-diaphorase neurons. Mol. Cell. Neurosci. 17 6 (2001) 1025-1033
19. Kjoller C., and Diemer N.H. GluR2 protein synthesis and metabolism in rat hippocampus following transient and ischemic tolerance induction. Neurochem. Int. 37 1 (2000) 7-15
20. Maranqoz C., and Baqirici F. Effects of l-arginine on penicillin-induced epileptiform activity in rats. Jpn. J. Pharmacol. 86 3 (2001) 297-301
21. Mathern G.W., Pretorius J.K., Mendoza D., Lozada A., and Kornblum H.I. Hippocampal AMPA and NMDA mRNA levels correlate with aberrant fascia dentate mossy fiber sprouting in the pilocarpine model of spontaneous limbic epilepsy. J. Neurosci. Res. 54 6 (1998) 734-753
22. Mathern G.W., Pretorius J.K., Leite J.P., Kornblum H.I., Mendoza D., Lozada A., and Bertram III E.H. Hippocampal AMPA and NMDA mRNA levels and subunit immunoreactivity in human temporal lobe epilepsy patients and a rodent model of chronic mesial limbic epilepsy. Epilepsy Res. 32 1-2 (1998) 154-171
23. + conductance in hippocampal interneurons. J. Neurosci. 17 13 (1997) 4994-5003
24. Ni H., Jiang Y.W., Bo T., Wang J.M., and Wu X.R. C-Fos, N-methyl-d-aspartate receptor 2C, GABA-A-1 immono-reactivity, seizure latency and neuronal injury following single or recurrent neonatal seizures in hippocampus of Wistar rat. Neurosci. Lett. 380 1-2 (2005) 149-154
25. Ni H., Jiang Y.W., Bo T., Wang J.M., Pan H., and Wu X.R. Long-term effects ofneonatal seizures on subsequent NMDA-1 and GABA-A-α1 receptor expression in hippocampus of the Wistar rat. Neurosci. Lett. 368 3 (2004) 254-257
26. Ni H., Jiang Y.W., Tao L.Y., Jin M.F., and Wu X.R. ZnT-1, ZnT-3, CaMKII, PRG-1 expressions in hippocampus following neonatal seizure-induced cognitive deficit in rats. Toxicol. Lett. 184 3 (2009) 145-150
27. Ni H., Jiang Y.W., Tao L.Y., Cen J.N., and Wu X.R. Effects of penicillin-induced developmental epilepticus on hippocampal regenerative sprouting, related gene expression and cognitive deficits in rats. Toxicol. Lett. 188 2 (2009) 161-166
28. Ni H., Jiang Y.W., Jiang W.M., Wang Z.D., and Wu X.R. Effects of physical exercise on the developmental expression of hippocampal zinc transporter 1 and glutamate receptor subunit 2, and on cognitive function in a rat model of recurrent neonatal seizure. Neural. Regen. Res. 4 1 (2009) 20-25
29. Reiss J.I., Dishman R.K., Boyd H.E., Robinson J.K., and Holmes P.V. Chronic activity wheel running reduces the severity of kainic acid-induced seizures in the rat: possible role of galanin. Brain Res. 1266 (2009) 54-63
30. Sanchez R.M., Koh S., Rio C., Wang C., Lamperti E.D., Sharma D., Corfas G., and Jensen F.E. Decreased glutamate receptor 2 expression and enhanced epileptogenesis in immature rat hippocampus after perinatal hypoxia-induced seizures. J. Neurosci. 21 20 (2001) 8154-8163
31. Sankar R., and Rho J.M. Do seizures affect the developing brain? Lessons from the laboratory. J. Child Neurol. 22 Suppl. 5 (2007) 21S-29S
32. Sartori C.R., Pelaqio F.C., Teixeira S.A., Valentinuzzi V.S., Nascimento A.L., Roqerio F., Muscara M.N., Ferrari E.A., and Lanqone F. Effects of voluntary running on spatial memory and mature brain-derived neurotrophic factor expression in mice hippocampus after status epilepticus. Behav. Brain Res. 203 2 (2009) 165-172
33. Setkowicz Z., and Mazur A. Physical training decreases susceptibility to subsequent pilocarpine-induced seizures in the rat. Epilepsy Res. 71 2-3 (2006) 142-148
34. Silva de Lacerda A.F., Janjoppi L., Scorza F.A., Lima E., Amado D., Cavalheiro E.A., and Arida R.M. Physical exercise program reverts the effects of pinealectomy on the amygdale kindling development. Brain Res. Bull. 74 4 (2007) 216-220
35. Sogawa Y., Monokoshi M., Silveira D.C., Cha B.H., Cilio M.R., McCabe B.K., Liu X., Hu Y., and Holmes G.L. Timing of cognitive deficits following neonatal seizures: relationship to histological changes in the hippocampus. Brain Res. Dev. Brain Res. 131 1-2 (2001) 73-83
36. Sutula T.P., and Dudek F.E. Unmasking recurrent excitation generated by mossy fiber sprouting in the epileptic dentate gyrus: an emergent property of a complex system. Prog. Brain Res. 163 (2007) 541-563
37. Tauck D.L., and Nadler J.V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5 4 (1985) 1016-1022
38. Tirassa P., Costa N., and Aloe L. CCK-8 prevents the development of kindling and regulates the GABA and NPY expression in the hippocampus of pentylenetetrazole (PTZ)-treated adult rats. Neuropharmacology 48 5 (2005) 732-742
39. Winter B., Breitenstein C., Mooren F.C., Voelker K., Fobker M., Lechtermann A., Krueger K., Fromme A., Korsukewitz C., Floel A., and Knecht S. High impact running improves learning. Neurobiol. Learn. Mem. 87 4 (2007) 597-609
40. Ying Z., Roy R.R., and Edgerton V.R. Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp. Neurol. 193 2 (2005) 411-419