Maternal infection during late pregnancy increases anxiety- and depression-like behaviors with increasing age in male offspring

Aikey, 2002, Testosterone rapidly reduces anxiety in male house mice (Mus musculus), Horm. Behav., 42, 448, 10.1006/hbeh.2002.1838 Allan, 2003, Inflammation in central nervous system injury, Philos. Trans. R. Soc. Lond. B: Biol. Sci., 358, 1669, 10.1098/rstb.2003.1358 Alonso, 1991, Effects of maternal stress during pregnancy on forced swimming test behavior of the offspring, Physiol. Behav., 50, 511, 10.1016/0031-9384(91)90538-Y Alonso, 2000, Behavioral despair in mice after prenatal stress, J. Physiol. Biochem., 56, 77, 10.1007/BF03179902 Anisman, 2008, Experiential and genetic contributions to depressive- and anxiety-like disorders: clinical and experimental studies, Neurosci. Biobehav. Rev., 32, 1185, 10.1016/j.neubiorev.2008.03.001 Antonow-Schlorke, 2003, Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain, J. Physiol., 547, 117, 10.1113/jphysiol.2002.025700 Asiaei, 2011, Prenatal exposure to lps leads to long-lasting physiological consequences in male offspring, Dev. Psychobiol., 10.1002/dev.20568 Baharnoori, 2010, Neonatal behavioral changes in rats with gestational exposure to lipopolysaccharide: a prenatal infection model for developmental neuropsychiatric disorders, Schizophr. Bull., 10.1093/schbul/sbq098 Baker, 2009, Effects of gestational stress: 2. Evaluation of male and female adult offspring, Brain Res., 1302, 194, 10.1016/j.brainres.2009.09.023 Bell, 2002, Effects of intrauterine inflammation on developing rat brain, J. Neurosci. Res., 70, 570, 10.1002/jnr.10423 Bergman, 2010, Maternal prenatal cortisol and infant cognitive development: moderation by infant–mother attachment, Biol. Psychiatry, 67, 1026, 10.1016/j.biopsych.2010.01.002 Beuke, 2003, Anxiety and depression: why and how to measure their separate effects, Clin. Psychol. Rev., 23, 831, 10.1016/S0272-7358(03)00074-6 Bewernick, 2010, Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression, Biol. Psychiatry, 67, 110, 10.1016/j.biopsych.2009.09.013 Boksa, 2010, Effects of prenatal infection on brain development and behavior: a review of findings from animal models, Brain Behav. Immun., 24, 881, 10.1016/j.bbi.2010.03.005 Bourin, 2009, Augmentation effect of combination therapy of aripiprazole and antidepressants on forced swimming test in mice, Psychopharmacology (Berl.), 206, 97, 10.1007/s00213-009-1583-7 Boyd, 1990, Phobia: prevalence and risk factors, Soc. Psychiatry Psychiatr. Epidemiol., 25, 314, 10.1007/BF00782887 Chaouloff, 2007, Acute stress facilitates hippocampal CA1 metabotropic glutamate receptor-dependent long-term depression, J. Neurosci., 27, 7130, 10.1523/JNEUROSCI.1150-07.2007 Cratty, 1995, Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces, Brain Res., 675, 297, 10.1016/0006-8993(95)00087-7 Dahlgren, 2006, Interleukin-6 in the maternal circulation reaches the rat fetus in mid-gestation, Pediatr. Res., 60, 147, 10.1203/01.pdr.0000230026.74139.18 Degroot, 2001, Pharmacol. Biochem. Behav., 69, 391, 10.1016/S0091-3057(01)00541-X Estanislau, 2005, Prenatal stress produces more behavioral alterations than maternal separation in the elevated plus-maze and in the elevated T-maze, Behav. Brain Res., 163, 70, 10.1016/j.bbr.2005.04.003 Field, 2010, Prenatal depression effects and interventions: a review, Infant Behav. Dev., 33, 409, 10.1016/j.infbeh.2010.04.005 Fonseca, 2002, Effects of prenatal stress on stress-induced changes in behavior and macrophage activity of mice, Physiol. Behav., 77, 205, 10.1016/S0031-9384(02)00812-0 Fride, 1988, Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity, Life Sci., 42, 1059, 10.1016/0024-3205(88)90561-9 Frye, 2004, Testosterone's metabolism in the hippocampus may mediate its anti-anxiety effects in male rats, Pharmacol. Biochem. Behav., 78, 473, 10.1016/j.pbb.2004.04.019 Frye, 2003, Effect of prenatal stress and gonadal hormone condition on depressive behaviors of female and male rats, Horm. Behav., 44, 319, 10.1016/S0018-506X(03)00159-4 Genn, 2003, Age-associated sex differences in response to food deprivation in two animal tests of anxiety, Neurosci. Biobehav. Rev., 27, 155, 10.1016/S0149-7634(03)00017-4 Glover, 2009, Association between maternal and amniotic fluid cortisol is moderated by maternal anxiety, Psychoneuroendocrinology, 34, 430, 10.1016/j.psyneuen.2008.10.005 Glover, 2010, Prenatal stress and the programming of the HPA axis, Neurosci. Biobehav. Rev., 35, 17, 10.1016/j.neubiorev.2009.11.008 Golan, 2005, Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy, Neuropharmacology, 48, 903, 10.1016/j.neuropharm.2004.12.023 Granger, 2003, Salivary testosterone diurnal variation and psychopathology in adolescent males and females: individual differences and developmental effects, Dev. Psychopathol., 15, 431, 10.1017/S0954579403000233 Guzzetti, 2008, Strain differences in paroxetine-induced reduction of immobility time in the forced swimming test in mice: role of serotonin, Eur. J. Pharmacol., 594, 117, 10.1016/j.ejphar.2008.07.031 Harris, 2011, Glucocorticoids, prenatal stress and the programming of disease, Horm. Behav., 59, 279, 10.1016/j.yhbeh.2010.06.007 Hava, 2006, Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy, Dev. Psychobiol., 48, 162, 10.1002/dev.20116 Hsiao, 2011, Activation of the maternal immune system induces endocrine changes in the placenta via IL-6, Brain Behav. Immun., 25, 604, 10.1016/j.bbi.2010.12.017 Huang, 2001, Repeated prenatal corticosteroid administration delays myelination of the corpus callosum in fetal sheep, Int. J. Dev. Neurosci., 19, 415, 10.1016/S0736-5748(01)00026-0 Imhof, 1993, Influence of gender and age on performance of rats in the elevated plus maze apparatus, Behav. Brain Res., 56, 177, 10.1016/0166-4328(93)90036-P Kapoor, 2008, Fetal programming of hypothalamic–pituitary–adrenal (HPA) axis function and behavior by synthetic glucocorticoids, Brain Res. Rev., 57, 586, 10.1016/j.brainresrev.2007.06.013 Kendler, 2007, The sources of co-morbidity between major depression and generalized anxiety disorder in a Swedish national twin sample, Psychol. Med., 37, 453, 10.1017/S0033291706009135 Khairova, 2009, A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder, Int. J. Neuropsychopharmacol., 12, 561, 10.1017/S1461145709009924 Levitt, 1996, Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat, Neuroendocrinology, 64, 412, 10.1159/000127146 Lister, 1987, The use of a plus-maze to measure anxiety in the mouse, Psychopharmacology, 92, 180, 10.1007/BF00177912 Mairesse, 2007, Maternal stress alters endocrine function of the feto-placental unit in rats, Am. J. Physiol. Endocrinol. Metab., 292, E1526, 10.1152/ajpendo.00574.2006 Matthews, 2001, Antenatal glucocorticoids and the developing brain: mechanisms of action, Semin. Neonatol., 6, 309, 10.1053/siny.2001.0066 McAfoose, 2009, Evidence for a cytokine model of cognitive function, Neurosci. Biobehav. Rev., 33, 355, 10.1016/j.neubiorev.2008.10.005 Meyer, 2005, Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia, Neurosci. Biobehav. Rev., 29, 913, 10.1016/j.neubiorev.2004.10.012 Meyer, 2008, Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice, Brain Behav. Immun., 22, 469, 10.1016/j.bbi.2007.09.012 Mitra, 2008, Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy, Proc. Natl. Acad. Sci. U.S.A., 105, 5573, 10.1073/pnas.0705615105 Monk, 2008, Amygdala nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression, Am. J. Psychiatry, 165, 90, 10.1176/appi.ajp.2007.06111917 Muneoka, 1997, Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring, Am. J. Physiol., 273, R1669 Murmu, 2006, Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy, Eur. J. Neurosci., 24, 1477, 10.1111/j.1460-9568.2006.05024.x Myatt, 2010, Review Reactive oxygen and nitrogen species and functional adaptation of the placenta, Placenta, 31, S66, 10.1016/j.placenta.2009.12.021 Owen, 2005, Maternal adversity, glucocorticoids and programming of neuroendocrine function and behaviour, Neurosci. Biobehav. Rev., 29, 209, 10.1016/j.neubiorev.2004.10.004 Pellow, 1986, Anxiolytic and anxiogenic drug effects in a novel test of anxiety: are exploratory models of anxiety in rodents valid?, Methods Find. Exp. Clin. Pharmacol., 8, 557 Pellow, 1985, Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat, J. Neurosci. Methods, 14, 149, 10.1016/0165-0270(85)90031-7 Pellow, 1986, Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat, Pharmacol. Biochem. Behav., 24, 525, 10.1016/0091-3057(86)90552-6 Porsolt, 1978, Behavioural despair in rats: a new model sensitive to antidepressant treatments, Eur. J. Pharmacol., 47, 379, 10.1016/0014-2999(78)90118-8 Porsolt, 1977, Behavioral despair in mice: a primary screening test for antidepressants, Arch. Int. Pharmacodyn. Ther., 229, 327 Rodgers, 1995, Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety, Pharmacol. Biochem. Behav., 52, 297, 10.1016/0091-3057(95)00138-M Rua, 1995, Effects of maternal adrenalectomy and glucocorticoid administration on the development of rat hippocampus, J. Hirnforsch., 36, 473 Salari, 2010, Intra-peritoneal injection of salmonella typhimurium LPS affects anxiety behaviors and serum corticosterone level in pregnant mice and its male offspring, Int. J. Psychiat. Clin., 14, 35 Salaria, 2006, Microarray analysis of cultured human brain aggregates following cortisol exposure: implications for cellular functions relevant to mood disorders, Neurobiol. Dis., 23, 630, 10.1016/j.nbd.2006.05.003 Samuelsson, 2004, Prenatal exposure to interleukin-6 results in hypertension and increased hypothalamic–pituitary–adrenal axis activity in adult rats, Endocrinology, 145, 4897, 10.1210/en.2004-0742 Sanson, 1999, Long-lasting inhibitory avoidance acquisition in rats submitted to the elevated T-maze model of anxiety, Behav. Brain Res., 101, 59, 10.1016/S0166-4328(98)00140-5 Schulz, 2007, Despair induced by extinction trials in the water maze: relationship with measures of anxiety in aged and adult rats, Neurobiol. Learn. Mem., 87, 309, 10.1016/j.nlm.2006.09.006 Sloviter, 1993, Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system, J. Comp. Neurol., 330, 337, 10.1002/cne.903300305 Smith, 2007, Maternal immune activation alters fetal brain development through interleukin-6, J. Neurosci., 27, 10695, 10.1523/JNEUROSCI.2178-07.2007 Solati, 2010, Dorsal hippocampal opioidergic system modulates anxiety-like behaviors in adult male Wistar rats, Psychiatry Clin. Neurosci., 64, 634, 10.1111/j.1440-1819.2010.02143.x Uno, 1994, Neurotoxicity of glucocorticoids in the primate brain, Horm. Behav., 28, 336, 10.1006/hbeh.1994.1030 Urakubo, 2001, Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain, Schizophr. Res., 47, 27, 10.1016/S0920-9964(00)00032-3 Vallee, 1997, Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion, J. Neurosci., 17, 2626, 10.1523/JNEUROSCI.17-07-02626.1997 Ward, 1984, The prenatal stress syndrome: current status, Psychoneuroendocrinology, 9, 3, 10.1016/0306-4530(84)90016-7 Ward, 1984, Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers, Endocrinology, 114, 1635, 10.1210/endo-114-5-1635 Welberg, 2000, Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring, Eur. J. Neurosci., 12, 1047, 10.1046/j.1460-9568.2000.00958.x Welberg, 2001, Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour, Neuroscience, 104, 71, 10.1016/S0306-4522(01)00065-3 Welberg, 2005, Chronic maternal stress inhibits the capacity to up-regulate placental 11-hydroxysteroid dehydrogenase type 2 activity, J. Endocrinol., 186, R7, 10.1677/joe.1.06374 Williamson, 2005, A genetic epidemiologic perspective on comorbidity of depression and anxiety, Child Adolesc. Psychiatr. Clin. N. Am., 14, 707, 10.1016/j.chc.2005.05.007 Zhao, 1998, Involvement of cytokines in normal CNS development and neurological diseases: recent progress and perspectives, J. Neurosci. Res., 52, 7, 10.1002/(SICI)1097-4547(19980401)52:1<7::AID-JNR2>3.0.CO;2-I