Prenatal activation of maternal TLR3 receptors by viral-mimetic poly(I:C) modifies GluN2B expression in embryos and sonic hedgehog in offspring in the absence of kynurenine pathway activation

References

• Brown AS. Prenatal infection as a risk factor in schizophrenia. Schizophren Bull 2006;32:200–202
   PubMed Web of Science ®Google Scholar
• Ellman LM, Susser ES. The promise of epidemiologic studies: neuroimmune mechanisms in the etiologies of brain disorders. Neuron 2009;64:25–27
   Google Scholar
• Pearce BD. Modeling the role of infections in the etiology of mental illness. Clin Neurosci Res 2003;3:271–282
   Google Scholar
• Hornig M, Weissenbock H, Horscroft N, Lipkin WI. An infection-based model of neurodevelopmental damage. Proc Nat Acad Sci USA 1999;96:12102–12107
   PubMed Web of Science ®Google Scholar
• Brown AS. The environment and susceptibility to schizophrenia. Progr Neurobiol 2011;93:23–58
   PubMed Web of Science ®Google Scholar
• Fatemi SH, Pearce DA, Brooks AI, Sidwell RW. Prenatal viral infection in mouse causes differential expression of genes in brains of mouse progeny: a potential animal model for schizophrenia and autism. Synapse 2005;57:91–99
   PubMed Web of Science ®Google Scholar
• Zuckerman L, Weiner I. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. Psychiat Res 2005;39:311–323
   Google Scholar
• Meyer U, Schwendener S, Feldon J, Yee BK. Prenatal and postnatal maternal contributions in the infection model of schizophrenia. Exp Brain Res 2006;173:243–257
   Google Scholar
• Brown A.S, Derkits E.J. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Amer J Psychiat 2010;167:261–280
   PubMed Web of Science ®Google Scholar
• Ornoy A, Tenenbaum A. Pregnancy outcome following infections by coxsackie, echo, measles, mumps, hepatitis, polio and encephalitis viruses. Reprod Toxicol 2006;21:446–457
   PubMed Web of Science ®Google Scholar
• Shlyokhov E, Segev S, Rubinstein E. Main viral diseases with in utero transmission of pathogen during pregnancy: epidemiology, pathological features and outcome. Acta Obst Gynecol Scand 1998;77:875–882
   Google Scholar
• Zhang S-Y, Herman M, Ciancanelli MJ, et al. TLR3 immunity to infection in mice and humans. Curr Opin Immunol 2013;25:19–33
   PubMed Web of Science ®Google Scholar
• Kimura M, Toth LA, Agostini H, et al. Comparison of acute-phase responses induced in rabbits by lipopolysaccharide and double-stranded-RNA. Amer J Physiol – Reg Integ Comp Physiol 1994;267:1596–1605
   PubMedGoogle Scholar
• Werling D, Hope JC, Howard CJ, Jungi TW. Differential production of cytokines, reactive oxygen species and nitrogen by bovine macrophages and dendritic cells stimulated with Toll-like receptor agonists. Immunology 2004;111:41–52
   PubMed Web of Science ®Google Scholar
• Stone TW, Darlington LG. Endogenous kynurenines as targets for drug discovery and development. Nat Revs Drug Disc 2002;1:609–620
   PubMed Web of Science ®Google Scholar
• Perkins MN, Stone TW. An iontophoretic investigation of the action of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res 1982;257:184–187
   Google Scholar
• Stone TW, Perkins MN. Quinolinic acid: a potent endogenous excitant at amino acid receptors in CNS. Eur J Pharmacol 1981;72:411–412
   PubMed Web of Science ®Google Scholar
• Rajan I, Cline HT. Glutamate receptor activity is required for normal development of tectal cells dendrites in vivo. J Neurosci 1998;18:7836–7846
   PubMed Web of Science ®Google Scholar
• Colonnese MT, Zhao JP, Constantine-Paton M. NMDA receptor currents suppress synapse formation on sprouting axons in vivo. J Neurosci 2005;25:1291–1303
   Google Scholar
• Alvarez VA, Ridenour DA, Sabatini BL. Distinct structural and ionotropic roles of NMDA receptors in controlling spine and synapse stability. J Neurosci 2007;27:7365–7376
   PubMed Web of Science ®Google Scholar
• Ultanir SK, Kim J-E, Hall BJ, et al. Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Proc Nat Acad Sci USA 2007;104:19553–19558
   PubMed Web of Science ®Google Scholar
• Miura H, Shirokawa T, Isobe K, Ozaki N. Shifting the balance of brain tryptophan metabolism elicited by isolation housing and systemic administration of lipopolysaccharide in mice. Stress 2009;12:206–214
   PubMed Web of Science ®Google Scholar
• Gibney SM, McGuinness B, Prendergast C, et al. Poly I:C-induced activation of the immune response is accompanied by depression and anxiety-like behaviours, kynurenine pathway activation and reduced BDNF expression. Brain Behav Immun 2013;28:170–181
   PubMed Web of Science ®Google Scholar
• Gilmore JH, Jarskog LF, Vadlamudi S. Maternal poly I:C exposure during pregnancy regulates TNF alpha BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. J Neuroimmunol 2005;159:106–112
   PubMed Web of Science ®Google Scholar
• Zhang ZR, Trautmann K, Schluesener HJ. Microglia activation in rat spinal cord by systemic injection of TLR3 and TLR7/8 agonists. J Neuroimmunol 2005;164:154–160
   PubMed Web of Science ®Google Scholar
• 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. Molec Brain 2012;5:art 22
   Google Scholar
• Lewis DA, Melchitzky DS, Haycock JW. Expression and distribution of 2 isoforms of tyrosine-hydroxylase in macaque monkey brain. Brain Res 1994;656:1–13
   Google Scholar
• Sutoo D, Akiyama K, Yabe K. Comparison analysis of distributions of tyrosine hydroxylase, calmodulin and calcium/calmodulin-dependent protein kinase II in a triple stained slice of rat brain. Brain Res 2002;933:1–11
   Google Scholar
• Lynn RB, Hyde TM, Cooperman RR, Miselils RR. Distribution of bombesin-like immunoreactivity in the nucleus of the solitary tract and dorsal motor nucleus of the rat and human: colocalization with tyrosine hydroxylase. J Comp Neurol 1996;369:552–570
   Google Scholar
• Niu X, Bogdanovic N, Canlon B. The distribution and the modulation of tyrosine hydroxylase immunoreactivity in the lateral olivocochlear system of the guinea-pig. Neuroscience 2004;125:725–733
   Google Scholar
• Miner LH, Jedema HP, Moore FW, et al. Chronic stress increases the plasmalemmal distribution of the norepinephrine transporter and the coexpression of tyrosine hydroxylase in norepinephrine axons in the prefrontal cortex. J Neurosci 2006;26:1571–1578
   PubMed Web of Science ®Google Scholar
• Jacobsen KX, Hoistad M, Staines WA, Fuxe K. The distribution of dopamine D1 receptor and mu-opioid receptor 1 receptor immunoreactivities in the amygdala and interstitial nucleus of the posterior limb of the anterior commissure: relationships to tyrosine hydroxylase and opioid peptide terminal systems. Neuroscience 2006;141:2007–2018
   Google Scholar
• Leighton HJ, Waggoner WG. Measurement of tyrosine-hydroxylase activity in nerve-terminals of rat hippocampus, hypothalamus, and striatum using an improved assay for tyrosine-hydroxylase. Life Sci 1981;28:385–391
   Google Scholar
• Frotscher M, Leranth C. Catecholaminergic innervation of pyramidal and gabaergic nonpyramidal neurons in the rat hippocampus – double label immunostaining with antibodies against tyrosine-hydroxylase and glutamate-decarboxylase. Histochemistry 1988;88:313–319
   Google Scholar
• Saavedra JM, Brownste M, Palkovit M, et al. Tyrosine-hydroxylase and dopamine-beta-hydroxylase - distribution in individual rat hypothalamic nuclei. J Neurochem 1974;23:869–871
   Google Scholar
• Brooks E, Waters E, Farrington L, Canal MM. Differential hypothalamic tyrosine hydroxylase distribution and activation by light in adult mice reared under different light conditions during the suckling period. Brain Struct Funct 2011;216:357–370
   Google Scholar
• Alex KD, Yavanian GJ, McFarlane HG, et al. Modulation of dopamine release by striatal 5-HT2C receptors. Synapse 2005;55:242–251
   PubMed Web of Science ®Google Scholar
• Egerton A, Ahmad R, Hirani E, Grasby PM. Modulation of striatal dopamine release by 5-HT(2A) and 5-HT(2C) receptor antagonists: (11)C raclopride PET studies in the rat. Psychopharmacology 2008;200:487–496
   PubMed Web of Science ®Google Scholar
• Jiang ZF, Mak TW, Sen G, Li XX. Toll-like receptor 3-mediated activation of NF-kappa B and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing INF-beta. Proc Nat Acad Sci USA 2004;101:3533–3538
   PubMed Web of Science ®Google Scholar
• Handa P, Tupper JC, Jordan KC, Harlan JM. FLIP (Flice-like inhibitory protein) suppresses cytoplasmic double-stranded-RNA-induced apoptosis and NF-kappa B and IRF3-mediated signaling. Cell Commun Signaling 2011;9:art 16
   Google Scholar
• Zhao W, Qi J, Wang L, et al. LY294002 inhibits TLR3/4-mediated IFN-beta production via inhibition of IRF3 activation with a PI3K-independent mechanism. FEBS Lett 2012;586:705–710
   Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Meyer U, Feldon J. Prenatal exposure to infection: a primary mechanism for abnormal dopaminergic development in schizophrenia. Psychopharmacology 2009;206:587–602
   PubMedGoogle Scholar
• Beraki S, Aronsson F, Karlsson H, et al. Influenza A virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Molec Psychiat 2005;10:299–308
   PubMed Web of Science ®Google Scholar
• Wolff AR, Bilkey DK. Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav Brain Res 2008;190:156–159
   Google Scholar
• Ratnayake U, Quinn TA, Castillo-Melendez M, et al. Behaviour and hippocampus-specific changes in spiny mouse neonates after treatment of the mother with the viral-mimetic Poly I:C at mid-pregnancy. Brain Behav Immun 2012;26:1288–1299
   Google Scholar
• Connor CM, Dincer A, Straubhaar J, et al. Maternal immune activation alters behavior in adult offspring, with subtle changes in the cortical transcriptome and epigenome. Schizophrenia Res 2012;140:175–184
   Google Scholar
• Kranjac D, McLinden KA, Koster KM, et al. Peripheral administration of poly I:C disrupts contextual fear memory consolidation and BDNF expression in mice. Behav Brain Res 2012;228:452–457
   Google Scholar
• Dobbing J, Sands J. Comparative aspects of the brain growth spurt. Early Human Devel 1979;311:79–83
   Google Scholar
• Konat GW, Borysiewicz E, Fil D, James I. Peripheral challenge with double-stranded RNA elicits global up-regulation of cytokine gene expression in the brain. J Neurosci Res 2009;87:1381–1388
   Google Scholar
• Fil D, Borysiewicz E, Konat GW. A broad upregulation of cerebral chemokine genes by peripherally-generated inflammatory mediators. Metab Brain Dis 2011;26:49–59
   Google Scholar
• Field R, Campion S, Warren C, et al. Systemic challenge with the TLR3 agonist polyI:C induces amplified IFN-alpha/beta and IL-1 beta responses in the diseased brain and exacerbates chronic neurodegeneration. Brain Behav Immun 2010;24:996–1007
   PubMed Web of Science ®Google Scholar
• McLinden KA, Kranjac D, Deodati LE, et al. Age exacerbates sickness behavior following exposure to a viral mimetic. Physiol Behav 2012;105:1219–1225
   Google Scholar
• Cunningham C, Campion S, Teeling J, et al. The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Brain Behav Immun 2007;21:490–502
   PubMed Web of Science ®Google Scholar
• Qin L, Crews FT. Chronic ethanol increases systemic TLR3 agonist-induced neuroinflammation and neurodegeneration. J Neuroinflamm 2012;9:art 130
   Google Scholar
• Zhang ZR, Trautmann K, Schluesener HJ. Microglia activation in rat spinal cord by systemic injection of TLR3 and TLR7/8 agonists. J Neuroimmunol 2005;164:154–160
   PubMed Web of Science ®Google Scholar
• Juckel G, Manitz MP, Bruene M, et al. Microglial activation in a neuroinflammational animal model of schizophrenia -- a pilot study. Schizophrenia Res 2011;131:96–100
   Google Scholar
• Abazyan B, Nomura J, Kannan G, et al. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol Psychiat 2010;68:1172–1181
   PubMed Web of Science ®Google Scholar
• Arrode-Brusés G, Brusés JL. Maternal immune activation by poly(I:C) induces expression of cytokines IL-1β and IL-13, chemokine MCP-1 and colony stimulating factor VEGF in fetal mouse brain. J Neuroinflamm 2012;9:art 83
   Google Scholar
• Fischer S, Gerriets T, Wessels C, et al. Extracellular RNA mediates endothelial-cell permeability via vascular endothelial growth factor. Blood 2007;110:2457–2465
   PubMed Web of Science ®Google Scholar
• Petrovic V, Piquette-Miller M. Impact of polyinosinic/polycytidylic acid on placental and hepatobiliary drug transporters in pregnant rats. Drug Metab Disposition 2010;38:1760–1766
   PubMed Web of Science ®Google Scholar
• Abdallah MW, Larsen N, Grove J, et al. Amniotic fluid chemokines and autism spectrum disorders: an exploratory study utilizing a Danish historic birth cohort. Brain Behav Immun 2012;26:170–176
   Google Scholar
• Patterson PH. Maternal infection and immune involvement in autism. Trends Mol Med 2011;17:389–394
   PubMed Web of Science ®Google Scholar
• Suh H-S, Zhao M-L, Rivieccio M, et al. Astrocyte indoleamine 2,3-dioxygenase is induced by the TLR3 ligand Poly(I:C): mechanism of induction and role in antiviral response. J Virol 2007;81:9838–9850
   PubMed Web of Science ®Google Scholar
• Wang B, Koga K, Osuga Y, et al. Toll-Like receptor-3 ligation-induced indoleamine 2,3-dioxygenase expression in human trophoblasts. Endocrinology 2011;152:4984–4992
   PubMed Web of Science ®Google Scholar
• Deleidi M, Hallett PJ, Koprich JB, et al. The toll-like receptor-3 agonist polyinosinic:polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J Neurosci 2010;30:16091–16101
   PubMed Web of Science ®Google Scholar
• Barlow BK, Cory-Slechta DA, Richfield EK, Thiruchelvam M. The gestational environment and Parkinson's disease: evidence for neurodevelopmental origins of a neurodegenerative disorder. Reprod Toxicol 2007;23:457–470
   PubMed Web of Science ®Google Scholar
• Zuckerman L, Rehavi M, Nachman R, Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 2003;28:1778–1789
   PubMed Web of Science ®Google Scholar
• Ozawa K, Hashimoto K, Kishimoto T, et al. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neuro-developmental animal model of schizophrenia. Biol Psychiat 2006;59:546–554
   PubMed Web of Science ®Google Scholar
• Vuillermot S, Weber L, Feldon J, Meyer U. A longitudinal examination of the neurodevelopmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia. J Neurosci 2010;30:1270–1287
   Google Scholar
• Meyer U, Engler A, Weber L, et al. Preliminary evidence for a modulation of fetal dopaminergic development by maternal immune activation during pregnancy. Neuroscience 2008;154:701–709
   Google Scholar
• Ozansoy M, Basak AN. The central theme of parkinson's disease: alpha-synuclein. Molec Neurobiol 2013;47:460–465
   PubMed Web of Science ®Google Scholar
• Guerrero E, Vasudevaraju P, Hegde ML, et al. Recent advances in alpha-synuclein functions, advanced glycation, and toxicity: implications for Parkinson's disease. Molec Neurobiol 2013;47:525–536
   PubMed Web of Science ®Google Scholar
• Huels S, Hoegen T, Vassallo N, et al. AMPA-receptor-mediated excitatory synaptic transmission is enhanced by iron-induced alpha-synuclein oligomers. J Neurochem 2011;117:868–878
   Google Scholar
• Yasuda T, Mochizuki H. The regulatory role of alpha-synuclein and parkin in neuronal cell apoptosis; possible implications for the pathogenesis of Parkinson's disease. Apoptosis 2010;15:1312–1321
   PubMed Web of Science ®Google Scholar
• Chinta SJ, Mallajosyula K, Rane A, Andersen JK. Mitochondrial alpha-synuclein accumulation impairs complex I function in dopaminergic neurons and results in increased mitophagy in vivo. Neurosci Lett 2010;486:235–239
   PubMed Web of Science ®Google Scholar
• Watson JB, Hatami A, David H, et al. Alterations in corticostriatal synaptic plasticity in mice overexpressing human alpha-synuclein. Neuroscience 2009;159:501–513
   PubMed Web of Science ®Google Scholar
• Nemani VM, Lu W, Berge V, et al. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 2010;65:66–79
   PubMed Web of Science ®Google Scholar
• Alvarez-Erviti L, Couch Y, Richardson J, et al. Alpha-synuclein release by neurons activates the inflammatory response in a microglial cell line. Neurosci Res 2011;69:337–342
   PubMed Web of Science ®Google Scholar
• Musgrove REJ, King AE, Dickson TC. Neuroprotective upregulation of endogenous alpha-synuclein precedes ubiquitination in cultured dopaminergic neurons. Neurotox Res 2011;19:592–602
   Google Scholar
• Mosharov EV, Larsen KE, Kanter E, et al. Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron 2009;62:218–229
   PubMed Web of Science ®Google Scholar
• Li YH, Gao N, Ye YW, et al. alpha-Synuclein functions as a negative regulator for expression of tyrosine hydroxylase. Acta Neurol Belg 2011;111:130–135
   Google Scholar
• Zhou Z, Kim J, Insolera R, et al. RhoGTPase regulation of α-synuclein and VMAT2: implications for pathogenesis of Parkinson's disease. Molec Cell Neurosci 2011;48:29–37
   Google Scholar
• Tang M, Villaescusa JC, Luo SX, et al. Interactions of wnt/beta-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J Neurosci 2010;30:9280–9291
   Google Scholar
• Gonzalez-Reyes LE, Verbitsky M, Blesa J, et al. Sonic hedgehog maintains cellular and neurochemical homeostasis in the adult nigrostriatal circuit. Neuron 2012;75:306–319
   Google Scholar
• Palma V, Lim DA, Dahmane N, et al. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005;132:335–344
   PubMed Web of Science ®Google Scholar
• Banerjee SB, Rajendran R, Dias BG, et al. Recruitment of the Sonic hedgehog signalling cascade in electroconvulsive seizure-mediated regulation of adult rat hippocampal neurogenesis. Eur J Neurosci 2005;22:1570–1580
   PubMed Web of Science ®Google Scholar
• Prajerova I, Honsa P, Chvatal A, Anderova M. Distinct effects of sonic hedgehog and wnt-7a on differentiation of neonatal neural stem/progenitor cells in vitro. Neuroscience 2010;171:693–711
   PubMedGoogle Scholar
• Traiffort E, Angot E, Ruat M. Sonic hedgehog in the mammalian brain. J Neurochem 2010;113:576–590
   Google Scholar
• Charytoniuk D, Porcel B, Gomez JR, et al. Sonic hedgehog signalling in the developing and adult brain. J Physiol (Paris) 2002;96:9–16
   Google Scholar
• Brandon NJ, Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nature Rev Neurosci 2001;12:707–722
   Google Scholar
• Singh KK, De Rienzo G, Drane L, et al. Common DISC1 polymorphisms disrupt wnt/gsk3 beta signaling and brain development. Neuron 2011;72:545–558
   PubMed Web of Science ®Google Scholar
• Kim JY, Liu CY, Zhang F, et al. Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 2012;148:1051–1064
   PubMed Web of Science ®Google Scholar
• Ishizuka K, Kamiya A, Oh EC, et al. DISC1-dependent switch from progenitor proliferation to migration in the developing cortex. Nature 2011;473:92–107
   PubMedGoogle Scholar
• Namba T, Ming GL, Song H, et al. NMDA receptor regulates migration of newly generated neurons in the adult hippocampus via Disrupted-in-schizophrenia 1 (DISC1). J Neurochem 2011;118:34–44
   Google Scholar
• Ramsey AJ, Milemkovic M, Oliveira AF, et al. Impaired NMDA receptor transmission alters striatal synapses and DISC1 protein in an age-dependent manner. J Neurosci 2011;108:5795–5800
   Google Scholar
• Brigman JL, Feyder M, Saksida LM, et al. Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learning Memory 2008;15:50–54
   Google Scholar
• Bannerman DM, Niewoehner B, Lyon L, et al. NMDA receptor subunit NR2A is required for rapidly acquired spatial working memory but not incremental spatial reference memory. J Neurosci 2008;28:3623–3630
   Google Scholar
• Lemay-Clermont J, Robitaille C, Auberson YP, et al. Blockade of NMDA Receptors 2A subunit in the dorsal striatum impairs the learning of a complex motor skill. Behav Neurosci 2011;125:714–723
   Google Scholar
• Huemmeke M, Eysel UT, Mittmann T. Lesion-induced enhancement of LTP in rat visual cortex is mediated by NMDA receptors containing the NR2B subunit. J Physiol (Lond) 2004;559:875–882
   Google Scholar
• White TL, Youngentob SL. The effect of NMDA-NR2B receptor subunit over-expression on olfactory memory task performance in the mouse. Brain Res 2004;1021:1–7
   PubMedGoogle Scholar
• Rammes G, Starker LK, Haseneder R, et al. Isoflurane anaesthesia reversibly improves cognitive function and long-term potentiation (LTP) via an up-regulation in NMDA receptor 2B subunit expression. Neuropharmacology 2009;56:626–636
   Google Scholar
• Barria A, Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 2005;48:289–301
   PubMed Web of Science ®Google Scholar
• Vasuta C, Caunt C, James R, et al. Effects of exercise on NMDA receptor subunit contributions to bidirectional synaptic plasticity in the mouse dentate gyrus. Hippocampus 2007;17:1201–1208
   Google Scholar
• Hu N-W, Klyubin I, Anwyl R, Rowan MJ. GluN2B subunit-containing NMDA receptor antagonists prevent A beta-mediated synaptic plasticity disruption in vivo. Proc Nat Acad Sci USA 2009;106:20504–20509
   PubMed Web of Science ®Google Scholar
• Mehlen P, Guenebeaud C. Netrin-1 and its dependence receptors as original targets for cancer therapy. Curr Opin Oncol 2010;22:46–54
   PubMed Web of Science ®Google Scholar
• Hong KS, Hinck L, Nishiyama M, et al. A ligand-gated association between cytoplasmic domains of Unc5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999;97:927–941
   PubMed Web of Science ®Google Scholar
• Osborne PB, Halliday GM, Cooper HM, Keast JR. Localization of immunoreactivity for deleted in colorectal cancer (DCC), the receptor for the guidance factor netrin-1, in ventral tier dopamine projection pathways in adult rodents. Neuroscience 2005;131:671–681
   Google Scholar
• Flores C. Role of netrin-1 in the organization and function of the mesocorticolimbic dopamine system. J Psychiat Neurosci 2011;36:296–310
   Google Scholar
• Yetnikoff L, Labelle-Dumais C, Flores C. Regulation of netrin-1 receptors by amphetamine in the adult brain. Neuroscience 2007;150:764–773
   Google Scholar
• Bitanihirwe BKY, Woo T-UW. Oxidative stress in schizophrenia: an integrated approach. Neurosci Biobehav Revs 2011;35:878–893
   PubMed Web of Science ®Google Scholar
• Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 2003;53:S26–S36
   PubMed Web of Science ®Google Scholar
• Henchcliffe C, Beal MF. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nature Clin Pract Neurol 2008;4:600–609
   PubMedGoogle Scholar
• Miller RL, James-Kracke M, Sun GY, Sun AY. Oxidative and inflammatory pathways in Parkinson's Disease. Neurochem Res 2009;34:55–65
   PubMed Web of Science ®Google Scholar
• Lundberg AM, Drexler SK, Monaco C, et al. Key differences in TLR3/poly I: C signaling and cytokine induction by human primary cells: a phenomenon absent from murine cell systems. Blood 2007;110:3245–3252
   PubMed Web of Science ®Google Scholar
• Gesuete R, Packard AEB, Vartanian KB, et al. Poly-ICLC preconditioning protects the blood-brain barrier against ischemic injury in vitro through type I interferon signaling. J Neurochem 2012;123:75–85
   Google Scholar
• Palma JP, Kwon D, Clipstone NA, Kim BS. Infection with Theiler's murine encephalomyelitis virus directly induces proinflammatory cytokines in primary astrocytes via NF-kappa B activation: potential role for the initiation of demyelinating disease. J Virol 2003;77:6322–6331
   Google Scholar
• Maire M, Parent R, Morand A-L, et al. Characterization of the double-stranded RNA responses in human liver progenitor cells. Biochem Biophys Res Commun 2008;368:556–562
   Google Scholar
• Goriely S, Molle C, Nguyen M, et al. Interferon regulatory factor 3 is involved in Toll-like receptor 4 (TLR4)- and TLR3-induced IL-12p35 gene activation. Blood 2006;107:1078–1084
   Google Scholar
• Lauterbach H, Bathke B, Gilles S, et al. Mouse CD8 alpha(+) DCs and human BDCA3(+) DCs are major producers of IFN-lambda in response to poly IC. J Exp Med 2010;207:2703–2717
   PubMed Web of Science ®Google Scholar
• Sweeney SE, Corr M, Kimbler TB. Role of interferon regulatory factor 7 in serum-transfer arthritis regulation of interferon-beta production. Arthritis Rheumat 2012;64:1046–1056
   Google Scholar
• Inoue K, Tsukiyama-Kohara K, Matsuda C, et al. Impairment of interferon regulatory factor-3 activation by hepatitis C virus core protein basic amino acid region 1. Biochem Biophys Res Commun 2012;428:494–499
   Google Scholar
• Hammaker D, Boyle DL, Firestein GS. Synoviocyte innate immune responses: TANK-binding kinase-1 as a potential therapeutic target in rheumatoid arthritis. Rheumatology 2012;51:610–618
   Google Scholar
• Meyer U, Feldon J. To poly(I:C) or not to poly(I:C): advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacology 2012;62:1308–1321
   PubMed Web of Science ®Google Scholar
• Kimura K, Matsuzaki Y, Nishikawa Y, et al. Characterization of retinoic acid-inducible gene-I (RIG-I) expression corresponding to viral infection and UVB in human keratinocytes. J Dermatol Sci 2012;66:64–70
   Google Scholar
• Sweeney SE, Kimbler TB, Firestein GS. Synoviocyte innate immune responses: II. Pivotal role of IFN regulatory factor 3. J Immunol 2010;184:7162–7168
   PubMed Web of Science ®Google Scholar
• Ozes ON, Taylor MW. Reversal of interferon-gamma-resistant phenotype by poly(i-c) - possible involvement of isgf2 (irf1) in interferon-gamma-mediated induction of the IDO gene. J Interferon Res 1994;14:25–32
   Google Scholar
• Ali S, Kukolj G. Interferon regulatory factor 3-independent double-stranded RNA-induced inhibition of hepatitis C virus replicons in human embryonic kidney 293 cells. J Virol 2005;79:3174–3178
   Google Scholar
• Vu AT, Chen X, Xie Y, et al. Extracellular double-stranded RNA induces TSLP via an endosomal acidification- and NF-kappa B-dependent pathway in human keratinocytes. J Invest Dermatol 2011;131:2205–2212
   PubMed Web of Science ®Google Scholar
• Joung SM, Park Z-Y, Rani S, et al. Akt contributes to activation of the TRIF-dependent signaling pathways of TLRs by interacting with TANK-binding kinase 1. J Immunol 2011;186:499–507
   Google Scholar