Maternal immune activation promotes hippocampal kindling epileptogenesis in mice

Annals of Neurology

Volumn 74, Issue 1, 2013, Pages 11-19

  Pineda, Eduardo ^a   Shin, Don ^a   You, Su Jeong ^a,b   Auvin, Stéphane ^c   Sankar, Raman ^a   Mazarati, Andréy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Inje University College of Medicine   (South Korea)

^c HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE ANTIBODY; INTERLEUKIN 1BETA; INTERLEUKIN 6; POLYINOSINIC POLYCYTIDYLIC ACID; RECOMBINANT CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; C57BL 6 MOUSE; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; EXCITABILITY; FEMALE; HIPPOCAMPUS; KINDLING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGENY; RISK FACTOR; SEIZURE SUSCEPTIBILITY;

ANIMALS; ANTIBODIES; BODY TEMPERATURE; EPILEPSY; FEMALE; HIPPOCAMPUS; INTERFERON INDUCERS; INTERLEUKIN-1BETA; INTERLEUKIN-6; KINDLING, NEUROLOGIC; MALE; MICE; MICE, INBRED C57BL; POLY I-C; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SOCIAL BEHAVIOR;

EID: 84883272562     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23898     Document Type: Article

References (46)

1. Ravizza T, Gagliardi B, Noe F, et al. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 2008; 29: 142-160.
2. Vezzani A, French J, Bartfai T, Baram TZ,. The role of inflammation in epilepsy. Nat Rev Neurol 2011; 7: 31-40.
3. Bien CG, Urbach H, Schramm J, et al. Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy. Neurology 2007; 69: 1236-1244.
4. Solbrig MV, Adrian R, Baratta J, et al. Kappa opioid control of seizures produced by a virus in an animal model. Brain 2006; 129: 642-654.
5. Stuck ED, Christensen RN, Huie JR, et al. Tumor necrosis factor alpha mediates GABA(A) receptor trafficking to the plasma membrane of spinal cord neurons in vivo. Neural Plast 2012; 2012: 261345.
6. Viviani B, Bartesaghi S, Gardoni F, et al. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 2003; 23: 8692-8700.
7. Buehler MR,. A proposed mechanism for autism: an aberrant neuroimmune response manifested as a psychiatric disorder. Med Hypotheses 2011; 76: 863-870.
8. Jonakait GM,. The effects of maternal inflammation on neuronal development: possible mechanisms. Int J Dev Neurosci 2007; 25: 415-425.
9. Ponzio NM, Servatius R, Beck K, et al. Cytokine levels during pregnancy influence immunological profiles and neurobehavioral patterns of the offspring. Ann N Y Acad Sci 2007; 1107: 118-128.
10. Boksa P,. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 2010; 24: 881-897.
11. Garay PA, Hsiao EY, Patterson PH, McAllister AK,. Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development. Brain Behav Immun 2013; 31: 54-68.
12. Brown AS, Susser ES,. In utero infection and adult schizophrenia. Ment Retard Dev Disabil Res Rev 2002; 8: 51-57.
13. Patterson PH,. Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav Brain Res 2009; 204: 313-321.
14. Aderem A, Ulevitch RJ,. Toll-like receptors in the induction of the innate immune response. Nature 2000; 406: 782-787.
15. Fortier ME, Kent S, Ashdown H, et al. The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism. Am J Physiol Regul Integr Comp Physiol 2004; 287: R759-R766.
16. Patterson PH,. Maternal infection and immune involvement in autism. Trends Mol Med 2011; 17: 389-394.
17. Malkova NV, Yu CZ, Hsiao EY, et al. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun 2012; 26: 607-616.
18. Smith SE, Li J, Garbett K, et al. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 2007; 27: 10695-10702.
19. Fatemi SH, Reutiman TJ, Folsom TD, et al. Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders. Schizophr Res 2008; 99: 56-70.
20. Vezzani A, Moneta D, Richichi C, et al. Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 2002; 43 (suppl 5): 30-35.
21. Crawley JN,. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 2007; 17: 448-459.
22. Nadler JJ, Moy SS, Dold G, et al. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 2004; 3: 303-314.
23. Jamain S, Radyushkin K, Hammerschmidt K, et al. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci U S A 2008; 105: 1710-1715.
24. Lothman EW, Williamson JM,. Closely spaced recurrent hippocampal seizures elicit two types of heightened epileptogenesis: a rapidly developing, transient kindling and a slowly developing, enduring kindling. Brain Res 1994; 649: 71-84.
25. Parent JM, von dem Bussche N, Lowenstein DH,. Prolonged seizures recruit caudal subventricular zone glial progenitors into the injured hippocampus. Hippocampus 2006; 16: 321-328.
26. Mazarati A, Shin D, Auvin S, et al. Kindling epileptogenesis in immature rats leads to persistent depressive behavior. Epilepsy Behav 2007; 10: 377-383.
27. Arrode-Bruses G, Bruses JL,. Maternal immune activation by poly(I:C) induces expression of cytokines IL-1beta and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain. J Neuroinflammation 2012; 9: 83.
28. Garbett KA, Hsiao EY, Kalman S, et al. Effects of maternal immune activation on gene expression patterns in the fetal brain. Transl Psychiatry 2012; 2: e98.
29. Hsiao EY, McBride SW, Chow J, et al. Modeling an autism risk factor in mice leads to permanent immune dysregulation. Proc Natl Acad Sci U S A 2012; 109: 12776-12781.
30. Forrest CM, Khalil OS, Pisar M, et al. Prenatal activation of Toll-like receptors-3 by administration of the viral mimetic poly(I:C) changes synaptic proteins, N-methyl-D-aspartate receptors and neurogenesis markers in offspring. Mol Brain 2012; 5: 22.
31. Roumier A, Pascual O, Bechade C, et al. Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function. PLoS One 2008; 3: e2595.
32. Samuelsson AM, Jennische E, Hansson HA, Holmang A,. Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1345-R1356.
33. Vezzani A, Moneta D, Conti M, et al. Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc Natl Acad Sci U S A 2000; 97: 11534-11539.
34. Maroso M, Balosso S, Ravizza T, et al. Interleukin-1beta biosynthesis inhibition reduces acute seizures and drug resistant chronic epileptic activity in mice. Neurotherapeutics 2011; 8: 304-315.
35. Galic MA, Riazi K, Henderson AK, et al. Viral-like brain inflammation during development causes increased seizure susceptibility in adult rats. Neurobiol Dis 2009; 36: 343-351.
36. Lehtimaki KA, Keranen T, Palmio J, et al. Increased plasma levels of cytokines after seizures in localization-related epilepsy. Acta Neurol Scand 2007; 116: 226-230.
37. Li G, Bauer S, Nowak M, et al. Cytokines and epilepsy. Seizure 2011; 20: 249-256.
38. Lehtimaki KA, Peltola J, Koskikallio E, et al. Expression of cytokines and cytokine receptors in the rat brain after kainic acid-induced seizures. Brain Res Mol Brain Res 2003; 110: 253-260.
39. Rosell DR, Nacher J, Akama KT, McEwen BS,. Spatiotemporal distribution of gp130 cytokines and their receptors after status epilepticus: comparison with neuronal degeneration and microglial activation. Neuroscience 2003; 122: 329-348.
40. Atladottir HO, Thorsen P, Ostergaard L, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord 2010; 40: 1423-1430.
41. Atladottir HO, Henriksen TB, Schendel DE, Parner ET,. Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics 2012; 130: e1447-e1454.
42. Yoon BH, Jun JK, Romero R, et al. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997; 177: 19-26.
43. Booth R, Wallace GL, Happe F,. Connectivity and the corpus callosum in autism spectrum conditions: insights from comparison of autism and callosal agenesis. Prog Brain Res 2011; 189: 303-317.
44. Clarke DF, Roberts W, Daraksan M, et al. The prevalence of autistic spectrum disorder in children surveyed in a tertiary care epilepsy clinic. Epilepsia 2005; 46: 1970-1977.
45. Steffenburg S, Gillberg C, Steffenburg U,. Psychiatric disorders in children and adolescents with mental retardation and active epilepsy. Arch Neurol 1996; 53: 904-912.
46. Tuchman R, Rapin I,. Epilepsy in autism. Lancet Neurol 2002; 1: 352-358.