Inflammation in rat pups subjected to short hyperthermic seizures enhances brain long-term excitability

Epilepsy Research

Volumn 86, Issue 2-3, 2009, Pages 124-130

  Auvin, Stéphane ^a,b,c   Porta, Natacha ^b,c   Nehlig, Astrid ^d   Lecointe, Cécile ^a,b   Vallée, Louis ^b,c   Bordet, Régis ^b  

^a HÔPITAL ROBERT DEBRÉ   (France)

^b UNIV LILLE   (France)

^c LILLE UNIVERSITY HOSPITAL   (France)

^d INSERM   (France)

Author keywords

Epilepsy; Febrile seizure; Immature brain; Inflammation; Pentylenetetrazole; Rat

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; PENTETRAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; CORE TEMPERATURE; ESCHERICHIA COLI; FEBRILE CONVULSION; HEATING; HISTOPATHOLOGY; HYPERTHERMIA; INFLAMMATION; MALE; NERVE CELL EXCITABILITY; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SEIZURE THRESHOLD;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BODY TEMPERATURE; CELL COUNT; FEVER; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; RATS; RATS, WISTAR; SEIZURES, FEBRILE; STAINING AND LABELING;

EID: 70349484628     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2009.05.010     Document Type: Article

References (55)

1. Almeida M.C., Steiner A.A., Branco L.G., and Romanovsky A.A. Cold-seeking behavior as a thermoregulatory strategy in systemic inflammation. Eur. J. Neurosci. 23 (2006) 3359-3367
2. Auvin S., and Sankar R. Inflammation, epilepsy, and anti-inflammatory therapies. In: Pellock J.M., Bourgeois B., Dodson W., Nordli Jr. D.R., and Sankar R. (Eds). Pediatric Epilepsy: Diagnosis and Therapy. third ed. (2008), Demos Medical Publishing, New York
3. Auvin S., Shin D., Mazarati A., Nakagawa J., Miyamoto J., and Sankar R. Inflammation exacerbates seizure-induced injury in the immature brain. Epilepsia 48 Suppl. 5 (2007) 27-34
4. Auvin S., Shin D., Mazarati A., and Sankar R. The utility of testing pentylenetetrazol threshold. Epilepsia 47 (2006) 662-663
5. Avishai-Eliner S., Brunson K.L., Sandman C.A., and Baram TZ. Stressed-out, or in (utero)?. Trends Neurosci 25 (2002) 518-524
6. Baram T.Z. Animals Models for febrile seizures. In: Baram T.Z., and Shinnar S. (Eds). Febrile Seizures (2002), Academic Press, San Diego 189-214
7. Ben-Ari Y. Seizures beget seizures: the quest for GABA as a key player. Crit. Rev. Neurobiol. 18 (2006) 135-144
8. Bender R.A., Dube C., Gonzalez-Vega R., Mina E.W., and Baram T.Z. Mossy fiber plasticity and enhanced hippocampal excitability, without hippocampal cell loss or altered neurogenesis, in an animal model of prolonged febrile seizures. Hippocampus 13 (2003) 399-412
9. Berg A.T. Are febrile seizures provoked by a rapid rise in temperature?. Am. J. Dis. Child. 147 (1993) 1101-1103
10. Berg A.T., and Shinnar S. Unprovoked seizures in children with febrile seizures: short-term outcome. Neurology 47 (1996) 562-568
11. Brewster A.L., Bernard J.A., Gall C.M., and Baram T.Z. Formation of heteromeric hyperpolarization-activated cyclic nucleotide-gated (HCN) channels in the hippocampus is regulated by developmental seizures. Neurobiol. Dis. 19 (2005) 200-207
12. Buono R.J., Ferraro T.N., O'Connor M.J., Sperling M.R., Ryan S.G., Scattergood T., Mulholland N., Gilmore J., Lohoff F.W., and Berrettini W.H. Lack of association between an interleukin 1 beta (IL-1beta) gene variation and refractory temporal lobe epilepsy. Epilepsia 42 (2001) 782-784
13. Cai Z., Pan Z.L., Pang Y., Evans O.B., and Rhodes P.G. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47 (2000) 64-72
14. Cendes F., Andermann F., Gloor P., Lopes-Cendes I., Andermann E., Melanson D., Jones-Gotman M., Robitaille Y., Evans A., and Peters T. Atrophy of mesial structures in patients with temporal lobe epilepsy: cause or consequence of repeated seizures?. Ann. Neurol. 34 (1993) 795-801
15. Chang Y.C., Huang A.M., Kuo Y.M., Wang S.T., Chang Y.Y., and Huang C.C. Febrile seizures impair memory and cAMP response-element binding protein activation. Ann. Neurol. 54 (2003) 706-718
16. Chugani H.T., and Phelps M.E. Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 231 (1986) 840-843
17. Chugani H.T., Phelps M.E., and Mazziotta J.C. Positron emission tomography study of human brain functional development. Ann. Neurol. 22 (1987) 487-497
18. Dubé C., Chen K., Eghbal-Ahmadi M., Brunson K., Soltesz I., and Baram T.Z. Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long term. Ann. Neurol. 47 (2000) 336-344
19. Dubé C., Richichi C., Bender R.A., Chung G., Litt B., and Baram T.Z. Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis. Brain 129 (2006) 911-922
20. Dubé C., Vezzani A., Behrens M., Bartfai T., and Baram T.Z. Interleukin-1beta contributes to the generation of experimental febrile seizures. Ann. Neurol. 57 (2005) 152-155
21. Dube C.M., Brewster A.L., Richichi C., Zha Q., and Baram T.Z. Fever, febrile seizures and epilepsy. Trends Neurosci. 30 (2007) 490-496
22. Florez-Duquet M., Peloso E., and Satinoff E. Fever and behavioral thermoregulation in young and old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 (2001) R1457-R1461
23. French J.A., Williamson P.D., Thadani V.M., Darcey T.M., Mattson R.H., Spencer S.S., and Spencer D.D. Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann. Neurol. 34 (1993) 774-780
24. Galic M.A., Riazi K., Heida J.G., Mouihate A., Fournier N.M., Spencer S.J., Kalynchuk L.E., Teskey G.C., and Pittman Q.J. Postnatal inflammation increases seizure susceptibility in adult rats. J. Neurosci. 28 (2008) 6904-6913
25. Haas K.Z., Sperber E.F., Opanashuk L.A., Stanton P.K., and Moshe S.L. Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling. Hippocampus 11 (2001) 615-625
26. Heida J.G., Boisse L., and Pittman Q.J. Lipopolysaccharide-induced febrile convulsions in the rat: short-term sequelae. Epilepsia 45 (2004) 1317-1329
27. Heida J.G., and Pittman Q.J. Causal links between brain cytokines and experimental febrile convulsions in the rat. Epilepsia 46 (2005) 1906-1913
28. Heida J.G., Teskey G.C., and Pittman Q.J. Febrile convulsions induced by the combination of lipopolysaccharide and low-dose kainic acid enhance seizure susceptibility, not epileptogenesis, in rats. Epilepsia 46 (2005) 1898-1905
29. Heils A., Haug K., Kunz W.S., Fernandez G., Horvath S., Rebstock J., Propping P., and Elger C.E. Interleukin-1beta gene polymorphism and susceptibility to temporal lobe epilepsy with hippocampal sclerosis. Ann. Neurol. 48 (2000) 948-950
30. Jansky L., Vybiral S., Pospisilova D., Roth J., Dornand J., Zeisberger E., and Kaminkova J. Production of systemic and hypothalamic cytokines during the early phase of endotoxin fever. Neuroendocrinology 62 (1995) 55-61
31. Kanemoto K., Kawasaki J., Miyamoto T., Obayashi H., and Nishimura M. Interleukin (IL)1beta, IL-1alpha, and IL-1 receptor antagonist gene polymorphisms in patients with temporal lobe epilepsy. Ann. Neurol. 47 (2000) 571-574
32. Kanemoto K., Kawasaki J., Yuasa S., Kumaki T., Tomohiro O., Kaji R., and Nishimura M. Increased frequency of interleukin-1beta-511T allele in patients with temporal lobe epilepsy, hippocampal sclerosis, and prolonged febrile convulsion. Epilepsia 44 (2003) 796-799
33. Kauffman M.A., Moron D.G., Consalvo D., Bello R., and Kochen S. Association study between interleukin 1 beta gene and epileptic disorders: a HuGe review and meta-analysis. Genet. Med. 10 (2008) 83-88
34. Lee S.C., Liu W., Dickson D.W., Brosnan C.F., and Berman J.W. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J. Immunol. 150 (1993) 2659-2667
35. Long N.C., Otterness I., Kunkel S.L., Vander A.J., and Kluger M.J. Roles of interleukin 1 beta and tumor necrosis factor in lipopolysaccharide fever in rats. Am. J. Physiol. 259 (1990) R724-R728
36. Loscher W., Honack D., Fassbender C.P., and Nolting B. The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. III. Pentylenetetrazole seizure models. Epilepsy Res. 8 (1991) 171-189
37. Millichap J.G., and Millichap J.J. Role of viral infections in the etiology of febrile seizures. Pediatr. Neurol. 35 (2006) 165-172
38. Nakayama J., and Arinami T. Molecular genetics of febrile seizures. Epilepsy Res. 70 Suppl. 1 (2006) S190-S198
39. Nehlig A. Respective roles of glucose and ketone bodies as substrates for cerebral energy metabolism in the suckling rat. Dev. Neurosci. 18 (1996) 426-433
40. Nehlig A., de Vasconcelos A.P., and Boyet S. Quantitative autoradiographic measurement of local cerebral glucose utilization in freely moving rats during postnatal development. J. Neurosci. 8 (1988) 2321-2333
41. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1982), Academic, Sydney
42. Pineau N., Charriaut-Marlangue C., Motte J., and Nehlig A. Pentylenetetrazol seizures induce cell suffering but not death in the immature rat brain. Brain Res. Dev. Brain Res. 112 (1999) 139-144
43. Pollack G.M., and Shen D.D. A timed intravenous pentylenetetrazol infusion seizure model for quantitating the anticonvulsant effect of valproic acid in the rat. J. Pharmacol. Methods 13 (1985) 135-146
44. Ravizza T., Noe F., Zardoni D., Vaghi V., Sifringer M., and Vezzani A. Interleukin Converting Enzyme inhibition impairs kindling epileptogenesis in rats by blocking astrocytic IL-1beta production. Neurobiol. Dis. 31 (2008) 327-333
45. Ravizza T., Rizzi M., Perego C., Richichi C., Veliskova J., Moshe S.L., De Simoni M.G., and Vezzani A. Inflammatory response and glia activation in developing rat hippocampus after status epilepticus. Epilepsia 46 Suppl. 5 (2005) 113-117
46. Rizzi M., Perego C., Aliprandi M., Richichi C., Ravizza T., Colella D., Veliskova J., Moshe S.L., De Simoni M.G., and Vezzani A. Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development. Neurobiol. Dis. 14 (2003) 494-503
47. Romanovsky A.A., Shido O., Sakurada S., Sugimoto N., and Nagasaka T. Endotoxin shock: thermoregulatory mechanisms. Am. J. Physiol. 270 (1996) R693-R703
48. Sankar R., Shin D.H., Liu H., Mazarati A., Pereira d.V., and Wasterlain C.G. Patterns of status epilepticus-induced neuronal injury during development and long-term consequences. J. Neurosci. 18 (1998) 8382-8393
49. Sankar R., Shin D.H., and Wasterlain C.G. Serum neuron-specific enolase is a marker for neuronal damage following status epilepticus in the rat. Epilepsy Res. 28 (1997) 129-136
50. Schmued L.C., Albertson C., and Slikker Jr. W. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751 (1997) 37-46
51. Sullivan P.G., Dube C., Dorenbos K., Steward O., and Baram T.Z. Mitochondrial uncoupling protein-2 protects the immature brain from excitotoxic neuronal death. Ann. Neurol. 53 (2003) 711-717
52. Toth Z., Yan X.X., Haftoglou S., Ribak C.E., and Baram T.Z. Seizure-induced neuronal injury: vulnerability to febrile seizures in an immature rat model. J. Neurosci. 18 (1998) 4285-4294
53. Turrin N.P., Gayle D., Ilyin S.E., Flynn M.C., Langhans W., Schwartz G.J., and Plata-Salaman C.R. Pro-inflammatory and anti-inflammatory cytokine mRNA induction in the periphery and brain following intraperitoneal administration of bacterial lipopolysaccharide. Brain Res. Bull. 54 (2001) 443-453
54. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F., and 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
55. Vezzani A., and Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46 (2005) 1724-1743