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

Molecular Brain

Volumn 5, Issue 1, 2012, Pages

  Forrest, Caroline M ^a   Khalil, Omari S ^a   Pisar, Mazura ^a   Smith, Robert A ^a   Darlington, Lynda Gail ^b   Stone, Trevor W ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b EPSOM GENERAL HOSPITAL   (United Kingdom)

Author keywords

Development; Eph receptors; Poly(I:C); Rho proteins; Synaptophysin; Synaptotagmin

Indexed keywords

BIOLOGICAL MARKER; CYCLINE; DOUBLE STRANDED RNA; DOUBLECORTIN; EPHRIN RECEPTOR A4; INTERLEUKIN 1BETA; IONOTROPIC RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUN1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUN2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUN2B; NERVE PROTEIN; POLYINOSINIC POLYCYTIDYLIC ACID; POSTSYNAPTIC DENSITY PROTEIN 95; RECEPTOR SUBTYPE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; SYNAPTOBREVIN 1; SYNAPTOPHYSIN; SYNAPTOTAGMIN; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR SOX2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; FEMALE; GESTATIONAL AGE; IMMUNOBLOTTING; IMMUNOSTIMULATION; MALE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION; VIRUS INFECTION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CYTOKINES; FEMALE; MALE; NEUROGENESIS; NEURONS; POLY I-C; PREGNANCY; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RHO GTP-BINDING PROTEINS; SYNAPSES; TOLL-LIKE RECEPTOR 3; VIRUSES;

ANIMALIA; RATTUS;

EID: 84861947641     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-5-22     Document Type: Article

References (69)

1. Prenatal infection as a risk factor in schizophrenia. Brown AS, Schizophren Bull 2006 32 200 202 10.1093/schbul/sbj052
2. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Brown AS, Begg MD, Gravenstein S, Schaefer CA, Wyatt RJ, Bresnahan M, Babulas VP, Susser ES, Arch gen Psychiat 2004 61 774 780 10.1001/archpsyc.61.8.774 15289276 (Pubitemid 39031117)
3. Modeling the role of infections in the etiology of mental illness. Pearce BD, Clin Neurosci Res 2003 3 271 282 10.1016/S1566-2772(03)00098-7 (Pubitemid 37461292)
4. An infection-based model of neurodevelopmental damage. Hornig M, Weissenbock H, Horscroft N, Lipkin WI, Proc Nat Acad Sci USA 1999 96 12102 12107 10.1073/pnas.96.21.12102 10518583 (Pubitemid 29502865)
5. The environment and susceptibility to schizophrenia. Brown AS, Progr Neurobiol 2011 93 23 58 10.1016/j.pneurobio.2010.09.003
6. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y, Tonegawa S, Knopfel T, Erzurumlu RS, Itohara S, Nature 2000 406 726 731 10.1038/35021059 10963597
7. Prenatal viral infection in mouse causes differential expression of genes in brains of mouse progeny: A potential animal model for schizophrenia and autism. Fatemi SH, Pearce DA, Brooks AI, Sidwell RW, Synapse 2005 57 91 99 10.1002/syn.20162 15906383 (Pubitemid 40911524)
8. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. Zuckerman L, Weiner I, Psychiat Res 2005 39 311 323 10.1016/j.jpsychires.2004.08.008 (Pubitemid 40255916)
9. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Meyer U, Feldon J, Prog Neurobiol 2010 90 285 326 10.1016/j.pneurobio.2009.10. 018 19857543
10. In vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Meyer U, Feldon J, Fatemi SH, Neurosci Biobehav Revs 2009 33 1061 1079 10.1016/j.neubiorev. 2009.05.001
11. Regulation of Toll-like receptor-induced chemokine production in murine dendritic cells by mitogen-activated protein kinases. Mitchell D, Olive C, Molec Immunol 2010 47 2065 2073 10.1016/j.molimm.2010.04.004
12. Maternal poly I:C exposure during pregnancy regulates TNF-, BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. Gilmore JH, Jarskog LF, Vadlamudi S, J Neuroimmunol 2005 159 106 112 10.1016/j.jneuroim.2004.10.008 15652408 (Pubitemid 40126182)
13. The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Cunningham C, Campion S, Teeling J, Felton L, Perry VH, Brain Behav Immun 2007 21 490 502 10.1016/j.bbi.2006.12.007 17321719 (Pubitemid 46528682)
14. The viral mimetic, polyinosinic:polycytidylic acid, induces a fever in rats via an interleukin-1-dependent mechanism. Fortier M-E, Kent S, Ashdown H, Poole S, Boska P, Luheshi GN, Am J Physiol Regul Integr Comp Physiol 2004 287 759 R766 10.1152/ajpregu.00293.2004 15205185 (Pubitemid 39280460)
15. Age exacerbates sickness behavior following exposure to a viral mimetic. McLinden KA, Kranjac D, Deodati LE, Kahn M, Chumley MJ, Boehm GW, Physiol Behav 2012 105 1219 1225 10.1016/j.physbeh.2011.04.024 21549726
16. Activation of Rho GTPases by synaptic transmission in the hippocampus. OKane EM, Stone TW, Morris BJ, J Neurochem 2003 87 1309 1312 10.1046/j.1471-4159.2003.02102.x 14622110 (Pubitemid 37485086)
17. A role for RhoB in synaptic plasticity and the regulation of neuronal morphology. McNair K, Spike R, Guilding C, Prendergast GC, Stone TW, Cobb SR, Morris BJ, J Neurosci 2010 30 3508 3517 10.1523/JNEUROSCI.5386-09.2010 20203211
18. Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Favaro R, Valotta M, Ferri ALM, Latorre E, Mariani J, Giachino C, Lancini C, Tosetti V, Ottolenghi S, Taylor V, Nicolis SK, Nature Neurosci 2009 12 1248 1262 10.1038/nn.2397 19734891
19. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Ferri ALM, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP, Sala M, DeBiasi S, Nicolis SK, Development 2004 131 3805 3819 10.1242/dev.01204 15240551 (Pubitemid 39199387)
20. Maternal infection and fever during late gestation are associated with altered synaptic transmission in the hippocampus of juvenile offspring rats. Lowe GC, Luheshi GN, Williams S, Amer J Physiol 2008 295 1563 R1571 10.1152/ajprenal.90302.2008
21. Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Ito HT, Smith SEP, Hsiao E, Patterson PH, Brain Behav Immun 2010 24 930 941 10.1016/j.bbi.2010.03.004 20227486
22. Effects of congenital HCMV infection on synaptic plasticity in dentate gyrus (DG) of rat hippocampus. Wu D, Yang L, Xu XX, Zhang GC, Bu XS, Ruan D, Tang JL, Brain Res 2011 1389 27 34 21396925
23. Influenza A virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Beraki S, Aronsson F, Karlsson H, Ogren SO, Kristensson K, Molec Psychiat 2005 10 299 308 10.1038/sj.mp.4001545 15241434 (Pubitemid 40432683)
24. Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Wolff AR, Bilkey DK, Behav Brain Res 2008 190 156 159 10.1016/j.bbr.2008.02.021 18367260
25. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Bitanihirwe BKY, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U, Neuropsychopharmacology 2010 35 2462 2478 10.1038/npp.2010.129 20736993
26. Comparative aspects of the brain growth spurt. Dobbing J, Sands J, Early Human Devel 1979 311 79 83 (Pubitemid 9141710)
27. Peripheral challenge with dsRNA elicits global up-regulation of cytokine gene expression in the brain. Konat GW, Borysiewicz E, Fil D, James I, J Neurosci Res 2009 87 1381 1388 10.1002/jnr.21958 19115408
28. Levels of mRNAs encoding synaptic vesicle and synaptic plasma membrane proteins in the temporal cortex of elderly schizophrenic patients. Sokolov BP, Tcherepanov AA, Haroutunian V, Davis KL, Biol Psychiat 2000 48 184 196 10.1016/S0006-3223(00)00875-1 10924661 (Pubitemid 30618990)
29. Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development. Halim ND, Weickert CS, McClintock BW, Hyde TM, Weinberger DR, Kleinman JE, Lipska BK, Molec Psychiat 2003 8 797 810 10.1038/sj.mp.4001319 12931207 (Pubitemid 37100713)
30. Analysis of gene expression in two large schizophrenia cohorts identifies multiple changes associated with nerve terminal function. Maycox PR, Kelly F, Taylor A, Bates S, Reid J, Logendra R, Barnes MR, Larminie C, Jones N, Lennon M, Davies C, Hagan JJ, Scorer CA, Angelinetta C, Akbar T, Hirsch S, Mortimer AM, Barnes TRE, de Belleroche J, Molec Psychiat 2009 14 1083 1094 10.1038/mp.2009.18 19255580
31. Prenatal stress alters presynaptic marker proteins in the hippocampus of rat pups. Afadlal S, Polaboon N, Surakul P, Govitrapong P, Jutapakdeegul N, Neurosci Lett 2010 470 24 27 10.1016/j.neulet.2009.12.046 20035832
32. Modulation of neuronal migration by NMDA receptors. Komuro H, Rakic P, Science 1993 260 95 97 10.1126/science.8096653 8096653 (Pubitemid 23122752)
33. NMDA receptor currents suppress synapse formation on sprouting axons in vivo. Colonnese MT, Zhao JP, Constantine-Paton M, J Neurosci 2005 25 1291 1303 10.1523/JNEUROSCI.4063-04.2005 15689567 (Pubitemid 40268972)
34. Glutamate receptor activity is required for normal development of tectal cells dendrites in vivo. Rajan I, Cline HT, J Neurosci 1998 18 7836 7846 9742152 (Pubitemid 28441023)
35. Distinct structural and ionotropic roles of NMDA receptors in controlling spine and synapse stability. Alvarez VA, Ridenour DA, Sabatini BL, J Neurosci 2007 27 7365 7376 10.1523/JNEUROSCI.0956-07.2007 17626197 (Pubitemid 47066561)
36. Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Ultanir SK, Kim J-E, Hall BJ, Deerinck T, Ellisman M, Ghosh A, Proc Nat Acad Sci USA 2007 104 19553 19558 10.1073/pnas.0704031104 18048342
37. Role of NMDA receptors in adult primate cortical somatosensory plasticity. Myers WA, Churchill JD, Muja N, Garraghty P, J Comp Neurol 2000 418 373 382 10.1002/(SICI)1096-9861(20000320)418:4<373::AID-CNE1>3.0.CO;2-F 10713567 (Pubitemid 30127682)
38. Suppression of cortical NMDA receptor function prevents development of orientation selectivity in the primary visual cortex. Ramoa AS, Mower AF, Liao D, Jafri SIA, J Neurosci 2001 21 4299 4309 11404415 (Pubitemid 32538555)
39. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW, Science 1999 283 70 74 10.1126/science.283.5398.70 9872743 (Pubitemid 29044848)
40. Long-term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism. Harris LW, Sharp T, Gartlon J, Jones DNC, Harrison PJ, Europ J Neurosci 2003 18 1706 1710 10.1046/j.1460-9568.2003.02902.x (Pubitemid 37215123)
41. Neonatal exposure to MK-801, an N-methyl-D-aspartate receptor antagonist, enhances methamphetamine-induced locomotion and disrupts sensorimotor gating in pre- and postpubertal rats. Uehara T, Sumiyoshi T, Seo T, Matsuoka T, Itoh H, Suzuki M, Kurachi M, Brain Res 2010 1352 223 230 20633540
42. Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Cochran SM, Kennedy M, Mckerchar CE, Steward LJ, Pratt JA, Morris BJ, Neuropsychopharmacology 2003 28 265 275 10.1038/sj.npp.1300031 12589379
43. Neonatal inflammation produces selective behavioural deficits and alters NMDA receptor subunit mRNA in the adult rat brain. Harre EM, Galic MA, Mouihate A, Noorbakhsh F, Pittman QJ, Europ J Neurosci 2008 27 644 653 10.1111/j.1460-9568.2008.06031.x (Pubitemid 351239289)
44. Altered apoptotic responses in neurons lacking RhoB GTPase. Barberan S, McNair K, Iqbal K, Smith NC, Prendergast GC, Stone TW, Cobb SR, Morris BJ, Europ J Neurosci 2011 34 1737 1746 10.1111/j.1460-9568.2011.07891.x
45. Differential effects of Rho GTPases on axonal and dendritic development in hippocampal neurons. Ahnert-Hilger G, Holtje M, Grosse G, Pickert G, Mucke C, Nixdorf-Bergweiler B, Boquet P, Hofmann F, Just I, J Neurochem 2004 90 9 18 10.1111/j.1471-4159.2004.02475.x 15198662 (Pubitemid 38879157)
46. Rho GTPases and their regulators in neuronal functions and development. Koh CG, Neurosignals 2006 15 228 237 10.1159/000101527 17409776
47. Eph/ephrin signaling in morphogenesis, neural development and plasticity. Klein R, Curr Opin Cell Biol 2004 16 580 589 10.1016/j.ceb.2004.07.002 15363810 (Pubitemid 39201244)
48. Functions of ephrin/Eph interactions in the development of the nervous system: Emphasis on the hippocampal system. Martinez A, Soriano E, Brain Res Revs 2005 49 211 226 10.1016/j.brainresrev.2005.02.001 (Pubitemid 41160391)
49. The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Henderson JT, Georgiou J, Jia ZP, Robertson J, Elowe S, Roder JC, Pawson T, Neuron 2001 32 1041 1056 10.1016/S0896-6273(01)00553-0 11754836 (Pubitemid 34075395)
50. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Takasu MA, Dalva MB, Zigmond R, Greenberg ME, Science 2002 295 491 494 10.1126/science.1065983 11799243 (Pubitemid 34101638)
51. Knockdown of Oct-4 or Sox-2 attenuates neurogenesis of mouse embryonic stem cells. Chen S, Choo ABH, Nai-Dy W, Heng-Phon T, Oh SKW, Stem Cells Dev 2007 16 413 420 10.1089/scd.2006.0099 17610371 (Pubitemid 47016226)
52. Immunohistological markers for proliferative events, gliogenesis and neurogenesis within the adult hippocampus. Von Bohlen, Halbach O, Cell Tiss Res 2011 345 1 19 10.1007/s00441-011-1196-4
53. Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Brazel CY, Limke TL, Osborne JK, Miura T, Cai JL, Pevny L, Rao MS, Aging Cell 2005 4 197 207 10.1111/j.1474-9726.2005.00158.x 16026334 (Pubitemid 41602741)
54. SOX2 expression levels distinguish between neural progenitor populations of the developing dorsal telencephalon. Hutton SR, Pevny LH, Devel Biol 2011 352 40 47 10.1016/j.ydbio.2011.01.015
55. Consequence of the loss of Sox2 in the developing brain of the mouse. Miyagi S, Masui S, Niwa H, Saito T, Shimazaki T, Okano H, Nishimoto M, Muramatsu M, Iwama A, Okuda A, FEBS Lett 2008 582 2811 2815 10.1016/j.febslet.2008.07.011 18638478
56. Akt Increases Sox2 Expression in Adult Hippocampal Neural Progenitor Cells, but Increased Sox2 Does Not Promote Proliferation. Peltier J, Conway A, Keung AJ, Schaffer DV, Stem Cells Devel 2011 20 1153 1161 10.1089/scd.2010.0130
57. The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Ashdown H, Dumont Y, Ng M, Poole S, Boksa P, Luheshi GN, Molec Psychiat 2006 11 47 55 10.1038/sj.mp.4001748 16189509 (Pubitemid 43251087)
58. The impact of IL-1 modulation on the development of lipopolysaccharide- induced cognitive dysfunction. Terrando N, Fidalgo AR, Vizcaychipi M, Cibelli M, Ma D, Monaco Claudia, Feldmann M, Maze M, Critical Care 2010 14 88 10.1186/cc9019 20470406
59. Microglial activation and TNF alpha production mediate altered CNS excitability following peripheral inflammation. Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA, Pittman QJ, Proc Nat Acad Sci USA 2008 105 17151 17156 10.1073/pnas.0806682105 18955701
60. Contributions of peripheral inflammation to seizure susceptibility: Cytokines and brain excitability. Riazi K, Galic MA, Pittman QJ, Epilepsy Res 2010 89 34 42 10.1016/j.eplepsyres.2009.09.004 19804959
61. Altered expression of pro-inflammatory and developmental genes in the fetal brain in a mouse model of maternal infection. Liverman CS, Kaftan HA, Cui L, Hersperger SG, Taboada E, Klein RM, Berman NEJ, Neurosci Lett 2006 399 220 225 10.1016/j.neulet.2006.01.064 16497437
62. Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain. Gayle DA, Beloosesky R, Desai M, Amidi F, Nunez SE, Ross MG, Amer J Physiol - Regul Integ Comp Physiol 2004 286 1024 R1029 10.1152/ajpregu.00664.2003 16211675 (Pubitemid 38661389)
63. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Cai ZW, Pan ZL, Pang Y, Evans OB, Rhodes PG, Pediat Res 2000 47 64 72 10.1203/00006450-200001000-00013 10625084 (Pubitemid 30038893)
64. IL-1 receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. Girard S, Tremblay L, Lepage M, Sebire G, J Immunol 2010 184 3997 4005 10.4049/jimmunol.0903349 20181892
65. Cytokines and the nervous-system.2. Actions and mechanisms of action. Rothwell NJ, Hopkins SJ, Trends Neurosci 1995 18 130 136 10.1016/0166-2236(95) 93890-A 7754524
66. Interleukin-6 in the maternal circulation reaches the rat fetus in mid-gestation. Dahlgren J, Samuelsson AM, Jansson T, Holmang Agneta, Pediat Res 2006 60 147 151 10.1203/01.pdr.0000230026.74139.18 16864694 (Pubitemid 44297583)
67. Cytokine immunoreactivity in cortical and subcortical neurons in periventricular leukomalacia: are cytokines implicated in neuronal dysfunction in cerebral palsy? Kadhim H, Tabarki B, De Prez C, Sebire G, Acta Neuropathol. 2003 105 209 216 12557006 (Pubitemid 36798811)
68. Maternal immune activation by LPS selectively alters specific gene expression profiles of interneuron migration and oxidative stress in the fetus without triggering a fetal immune response. Oskvig DB, Elkahloun AG, Johnson KR, Phillips TM, Herkenham M, Brain Behav Immun 2012 26 623 634 10.1016/j.bbi.2012.01.015 22310921
69. Extracellular RNA mediates endothelial-cell permeability via vascular endothelial growth factor. Fischer S, Gerriets T, Wessels C, Walberer M, Kostin S, Stolz E, Zheleva Kirila, Hocke A, Hippenstiel S, Preissner KT, Blood 2007 110 2457 2465 10.1182/blood-2006-08-040691 17576819 (Pubitemid 47523167)