Maternal immune activation increases seizure susceptibility in juvenile rat offspring

Epilepsy and Behavior

Volumn 47, Issue , 2015, Pages 93-97

  Yin, Ping ^a,b   Zhang, Xin Ting ^a,b   Li, Jun ^a,b   Yu, Lin ^c   Wang, Ji Wen ^a,b   Lei, Ge Fei ^a,b   Sun, Ruo Peng ^a,b   Li, Bao Min ^a,b  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Astrogliosis; Elevated plus maze; Lipopolysaccharide; Maternal immune activation; Seizure; Y maze

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; KAINIC ACID; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN DAMAGE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DISEASE PREDISPOSITION; ELEVATED PLUS MAZE TEST; FEMALE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFECTION; INTRAUTERINE INFECTION; JUVENILE ANIMAL; LEARNING DISORDER; MALE; MATERNAL DISEASE; NONHUMAN; PRENATAL EXPOSURE; PROGENY; RAT; SEIZURE; SPATIAL LEARNING; ANIMAL; ANXIETY; BRAIN INJURIES; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; EPILEPSY; HIPPOCAMPUS; IMMUNOLOGY; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ANXIETY; BRAIN INJURIES; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; EPILEPSY; FEMALE; HIPPOCAMPUS; KAINIC ACID; LIPOPOLYSACCHARIDES; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES;

EID: 84937627923     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2015.04.018     Document Type: Article

References (39)

1. Buss C., Davis E.P., Muftuler L.T., Head K., Sandman C.A. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 2010, 35:141-153.
2. Harvey L., Boksa P. Prenatal and postnatal animal models of immune activation: relevance to a range of neurodevelopmental disorders. Dev Neurobiol 2012, 72:1335-1348.
3. Escobar M., Crouzin N., Cavalier M., Quentin J., Roussel J., Lante F., et al. Early, time-dependent disturbances of hippocampal synaptic transmission and plasticity after in utero immune challenge. Biol Psychiatry 2011, 70:992-999.
4. Meyer U. Developmental neuroinflammation and schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2013, 42:20-34.
5. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat Rev Neurol 2011, 7:31-40.
6. Riazi K., Galic M.A., Pittman Q.J. Contributions of peripheral inflammation to seizure susceptibility: cytokines and brain excitability. Epilepsy Res 2010, 89:34-42.
7. Galic M.A., Riazi K., Heida J.G., Mouihate A., Fournier N.M., Spencer S.J., et al. Postnatal inflammation increases seizure susceptibility in adult rats. J Neurosci 2008, 28:6904-6913.
8. Wu C.S., Pedersen L.H., Miller J.E., Sun Y., Streja E., Uldall P., et al. Risk of cerebral palsy and childhood epilepsy related to infections before or during pregnancy. PLoS One 2013, 8:e57552.
9. Norgaard M., Ehrenstein V., Nielsen R.B., Bakketeig L.S., Sorensen H.T. Maternal use of antibiotics, hospitalisation for infection during pregnancy, and risk of childhood epilepsy: a population-based cohort study. PLoS One 2012, 7:e30850.
10. Glass H.C., Pham T.N., Danielsen B., Towner D., Glidden D., Wu Y.W. Antenatal and intrapartum risk factors for seizures in term newborns: a population-based study, California 1998-2002. J Pediatr 2009, 154:24-28.
11. Yin P., Liu J., Li Z., Wang Y.Y., Qiao N.N., Huang S.Y., et al. Prenatal immune challenge in rats increases susceptibility to seizure-induced brain injury in adulthood. Brain Res 2013, 1519:78-86.
12. Sofroniew M.V. Multiple roles for astrocytes as effectors of cytokines and inflammatory mediators. Neuroscientist 2014, 20:160-172.
13. Furman J.L., Sama D.M., Gant J.C., Beckett T.L., Murphy M.P., Bachstetter A.D., et al. Targeting astrocytes ameliorates neurologic changes in a mouse model of Alzheimer's disease. J Neurosci 2012, 32:16129-16140.
14. Seifert G., Steinhauser C. Neuron-astrocyte signaling and epilepsy. Exp Neurol 2013, 244:4-10.
15. Clasadonte J., Dong J., Hines D.J., Haydon P.G. Astrocyte control of synaptic NMDA receptors contributes to the progressive development of temporal lobe epilepsy. Proc Natl Acad Sci U S A 2013, 110:17540-17545.
16. Crunelli V., Carmignoto G., Steinhäuser C. Novel astrocyte targets: new avenues for the therapeutic treatment of epilepsy. Neuroscientist. 2015, 21:62-83.
17. Fedele D.E., Gouder N., Guttinger M., Gabernet L., Scheurer L., Rulicke T., et al. Astrogliosis in epilepsy leads to overexpression of adenosine kinase, resulting in seizure aggravation. Brain 2005, 128:2383-2395.
18. Losi G., Cammarota M., Carmignoto G. The role of astroglia in the epileptic brain. Front Pharmacol 2012, 3:132.
19. Wetherington J., Serrano G., Dingledine R. Astrocytes in the epileptic brain. Neuron 2008, 58:168-178.
20. Rousset C.I., Chalon S., Cantagrel S., Bodard S., Andres C., Gressens P., et al. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 2006, 59:428-433.
21. Fatemi S.H., Emamian E.S., Sidwell R.W., Kist D.A., Stary J.M., Earle J.A., et al. Human influenza viral infection in utero alters glial fibrillary acidic protein immunoreactivity in the developing brains of neonatal mice. Mol Psychiatry 2002, 7:633-640.
22. Samuelsson A.M., Jennische E., Hansson H.A., 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.
23. Ghiani C.A., Mattan N.S., Nobuta H., Malvar J.S., Boles J., Ross M.G., et al. Early effects of lipopolysaccharide-induced inflammation on foetal brain development in rat. ASN Neuro 2011 Nov 17, 3(4). 10.1042/AN20110027.
24. Somera-Molina K.C., Nair S., Van Eldik L.J., Watterson D.M., Wainwright M.S. Enhanced microglial activation and proinflammatory cytokine upregulation are linked to increased susceptibility to seizures and neurologic injury in a 'two-hit' seizure model. Brain Res 2009, 1282:162-172.
25. Devinsky O., Vezzani A., Najjar S., De Lanerolle N.C., Rogawski M.A. Glia and epilepsy: excitability and inflammation. Trends Neurosci 2013, 36:174-184.
26. Aronica E., Ravizza T., Zurolo E., Vezzani A. Astrocyte immune responses in epilepsy. Glia 2012, 60:1258-1268.
27. Chung J.I., Kim A.Y., Lee S.H., Baik E.J. Seizure susceptibility in immature brain due to lack of COX-2-induced PGF2alpha. Exp Neurol 2013, 249:95-103.
28. Richetto J., Calabrese F., Riva M.A., Meyer U. Prenatal immune activation induces maturation-dependent alterations in the prefrontal GABAergic transcriptome. Schizophr Bull 2014, 40:351-361.
29. Li Y.K., Wang F., Wang W., Luo Y., Wu P.F., Xiao J.L., et al. Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: involvement of downregulation of glutamate transporter-1 expression. Neuropsychopharmacology 2012, 37:1867-1878.
30. Kashon M.L., Ross G.W., O'Callaghan J.P., Miller D.B., Petrovitch H., Burchfiel C.M., et al. Associations of cortical astrogliosis with cognitive performance and dementia status. J Alzheimers Dis 2004, 6:595-604. [discussion 673-81].
31. Verkhratsky A., Parpura V. Recent advances in (patho)physiology of astroglia. Acta Pharmacol Sin 2010, 31:1044-1054.
32. Han C., Lu Y., Wei Y., Wu B., Liu Y., He R. D-ribosylation induces cognitive impairment through RAGE-dependent astrocytic inflammation. Cell Death Dis 2014, 5:e1117.
33. Zhao Q., Peng C., Wu X., Chen Y., Wang C., You Z. Maternal sleep deprivation inhibits hippocampal neurogenesis associated with inflammatory response in young offspring rats. Neurobiol Dis 2014, 68:57-65.
34. Diz-Chaves Y., Astiz M., Bellini M.J., Garcia-Segura L.M. Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain Behav Immun 2013, 28:196-206.
35. Paris J.J., Brunton P.J., Russell J.A., Frye C.A. Immune stress in late pregnant rats decreases length of gestation and fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring. Stress 2011, 14:652-664.
36. Lante F., Meunier J., Guiramand J., De Jesus Ferreira M.C., Cambonie G., Aimar R., et al. Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation. Hippocampus 2008, 18:602-609.
37. Enayati M., Solati J., Hosseini M.H., Shahi H.R., Saki G., Salari A.A. Maternal infection during late pregnancy increases anxiety- and depression-like behaviors with increasing age in male offspring. Brain Res Bull 2012, 87:295-302.
38. Wischhof L., Irrsack E., Osorio C., Koch M. Prenatal LPS-exposure-a neurodevelopmental rat model of schizophrenia-differentially affects cognitive functions, myelination and parvalbumin expression in male and female offspring. Prog Neuropsychopharmacol Biol Psychiatry 2015, 57:17-30.
39. Dada T., Rosenzweig J.M., Al Shammary M., Firdaus W., Al Rebh S., Borbiev T., et al. Mouse model of intrauterine inflammation: sex-specific differences in long-term neurologic and immune sequelae. Brain Behav Immun 2014, 38:142-150.