Studies on the effects prenatal immune activation on postnatal behavior: Models of developmental origins of schizophrenia

Neuromethods

Volumn 109, Issue , 2016, Pages 263-278

  Ratnayake, Udani ^a   Hill, Rachel Anne ^a  

^a NONE

Author keywords

Animal model; Behavior; Poly I:C; Prenatal immune activation; Schizophrenia; Symptoms

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYTOKINE; ENDOTOXIN; INTERLEUKIN 6; POLYINOSINIC POLYCYTIDYLIC ACID;

ATTENTION DISTURBANCE; COGNITIVE DEFECT; EXPERIMENTAL HYPERACTIVITY; HUMAN; INFLUENZA VIRUS; INTRAUTERINE INFECTION; LATENT INHIBITION; LEARNING DISORDER; MEMORY DISORDER; NEGATIVE SYNDROME; NONHUMAN; PRENATAL EXPOSURE; PREPULSE INHIBITION; PRIORITY JOURNAL; PRODROMAL SYMPTOM; PSYCHOSIS; RODENT MODEL; SCHIZOPHRENIA; SENSORY GATING; SOCIAL BEHAVIOR;

EID: 84946762229     PISSN: 08932336     EISSN: 19406045     Source Type: Book Series    
DOI: 10.1007/978-1-4939-3014-2_13     Document Type: Chapter

References (90)

1. Tandon R et al (2008) Schizophrenia, “Just the Facts”: what we know in 2008 part 1: overview. Schizophr Res 100(1-3):4-19
2. Williams JG et al (2006) The epidemiology of autistic spectrum disorders: is the prevalence rising. Arch Dis Child 91:8-15
3. Cannon TD (1998) Neurodevelopmental influences in the genesis and epigenesis of schizophrenia: an overview. Appl Prev Psychol 7:47-62
4. Cannon M, Murray RM (1998) Neonatal origins of schizophrenia. Arch Dis Child 78 (1):1-3
5. Brown AS et al (2001) Prenatal rubella, pre-morbid abnormalities, and adult schizophrenia. Biol Psychiatry 49(6):473-486
6. Brown AS et al (2000) Nonaffective psychosis after prenatal exposure to rubella. Am J Psychiatry 157(3):438-443
7. Mednick SA et al (1988) Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 45(2):189-192
8. O’Callaghan E et al (1991) Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic. Lancet 337(8752):1248-1250
9. Brown AS et al (2000) Maternal exposure to respiratory infections and adult schizophrenia spectrum disorders: a prospective birth cohort study. Schizophr Bull 26(2):287-295
10. Machon RA et al (2002) Adult schizotypal personality characteristics and prenatal influenza in a Finnish birth cohort. Schizophr Res 54(1-2):7-16
11. Limosin F et al (2003) Prenatal exposure to influenza as a risk factor for adult schizophrenia. Acta Psychiatr Scand 107(5):331-335
12. Brown AS et al (2004) Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 61(8):774-780
13. Kendell RE, Kemp IW (1989) Maternal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 46(10):878-882
14. Buka SLS et al (2001) Maternal infections and subsequent psychosis among offspring. Arch Gen Psychiatry 58(11):1032-1037
15. Brown AS et al (2005) Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. Am J Psychiatry 162 (4):767-773
16. Mortensen PB et al (2007) Toxoplasma gondii as a risk factor for early-onset schizophrenia: analysis of filter paper blood samples obtained at birth. Biol Psychiatry 61(5):688-693
17. Suvisaari J et al (1999) Association between prenatal exposure to poliovirus infection and adult schizophrenia. Am J Psychiatry 156 (7):1100-1102
18. Fuller Torrey E et al (1988) Schizophrenic births and viral diseases in two states. Schizophr Res 1(1):73-77
19. Babulas V et al (2006) Prenatal exposure to maternal genital and reproductive infections and adult schizophrenia. Am J Psychiatry 163 (5):927-929
20. Watanabe Y et al (2010) Cytokine hypothesis of schizophrenia pathogenesis: evidence from human studies and animal models. Psychiatry Clin Neurosci 64(3):217-230
21. Fatemi SH et al (1999) Defective corticogen-esis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol Psychiatry 4 (2):145-154
22. Fatemi SH et al (2002) Prenatal viral infection leads to pyramidal cell atrophy and macroce-phaly in adulthood: implications for genesis of autism and schizophrenia. Cell Mol Neurobiol 22(1):25-33
23. Fatemi SH et al (2002) Human influenza viral infection in utero alters glial fibrillary acidic protein immunoreactivity in the developing brains of neonatal mice. Mol Psychiatry 7 (6):633-640
24. Bayer TA et al (1999) Evidence for activation of microglia in patients with psychiatric illnesses. Neurosci Lett 271(2):126-128
25. Shi L et al (2003) Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 23 (1):297-302
26. Shi L et al (2005) Maternal influenza infection is likely to alter fetal brain development indirectly: the virus is not detected in the fetus. Int J Dev Neurosci 23(2-3):299-305
27. Fatemi SH et al (2012) The viral theory of schizophrenia revisited: abnormal placental gene expression and structural changes with lack of evidence for H1N1 viral presence in placentae of infected mice or brains of exposed offspring. Neuropharmacology 62 (3):1290-1298
28. Golan HM et al (2005) Specific neurodevelop-mental damage in mice offspring following maternal inflammation during pregnancy. Neuropharmacology 48(6):903-917
29. Urakubo A et al (2001) Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr Res 47(1):27-36
30. Fidel PL Jr et al (1994) Systemic and local cytokine profiles in endotoxin-induced preterm parturition in mice. Am J Obstet Gynecol 170 (5):1467-1475
31. Ashdown Hetal (2006) The role of cytokines in mediating effects ofprenatal infection on the fetus: implications for schizophrenia. Mol Psychiatry 11(1):47-55
32. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17(1):1-14
33. Romero E et al (2007) Neurobehavioral and immunological consequences of prenatal immune activation in rats. Influence of antipsy-chotics. Neuropsychopharmacology 32 (8):1791-1804
34. Borrell J et al (2002) Prenatal immune challenge disrupts sensorimotor gating in adult rats: implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 26 (2):204
35. Hao LY et al (2010) Prenatal exposure to lipo-polysaccharide results in cognitive deficits in age-increasing offspring rats. Neuroscience 166(31):763-770
36. Graciarena M et al (2010) Prenatal inflammation impairs adult neurogenesis and memory related behavior through persistent hippocampal TGFbeta1 downregulation. Brain Behav Immun 24(8):1301-1309
37. Bakos J et al (2004) Prenatal immune challenge affects growth, behavior, and brain dopamine in offspring. Ann N Y Acad Sci 1018:281-287 (Stress: Current Neuroendocrine and Genetic Approaches)
38. Quinn TA et al (2014) Adrenal steroidogenesis following prenatal dexamethasone exposure in the spiny mouse. J Endocrinol 221:347
39. Samuelsson A-M et al (2006) Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABAA dysregulation and impaired spatial learning. Am J Physiol Regul Integr Comp Physiol 290(5):R1345-R1356
40. Smith SEP et al (2007) Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 27(40): 10695-10702
41. Hsiao EY, Patterson PH (2011) Activation of the maternal immune system induces endocrine changes in the placenta via IL-6. Brain Behav Immun 25(4):604-615
42. Fortier ME et al (2004) The viral mimic, poly-inosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism. Am J Physiol Regul Integr Comp Physiol 287 (4):R759-R766
43. Alexopoulou L et al (2001) Recognition of double-stranded RNA and activation of NF-[kappa]B by Toll-like receptor 3. Nature 413 (6857):732(7)
44. Meyer U et al (2005) Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci Biobehav Rev 29(6):913-947
45. Cunningham C et al (2007) 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 21(4):490-502
46. Gandhi R et al (2007) Influence of poly I:C on sickness behaviors, plasma cytokines, corticosterone and central monoamine activity: moderation by social stressors. Brain Behav Immun 21(4):477-489
47. Gilmore JH et al (2005) Maternal poly I:C exposure during pregnancy regulates TNF [alpha], BDNF, and NGF expression in neonatal brain and the maternal-fetal unit ofthe rat. J Neuroimmunol 159(1-2):106-112
48. Meyer U et al (2006) Immunological stress at the maternal-foetal interface: a link between neurodevelopment and adult psychopathology. Brain Behav Immun 20(4):378-388
49. Meyer U et al (2006) The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 26(18): 4752-4762
50. Song X et al (2011) The nuclear factor-kappaB inhibitor pyrrolidine dithiocarbamate reduces polyinosinic-polycytidilic acid-induced immune response in pregnant rats and the behavioral defects of their adult offspring. Behav Brain Funct 7(1):50
51. Arrode-Bruses G, Bruses JL (2012) 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 9:83
52. Arsenault D et al (2014) The different effects of LPS and poly I:C prenatal immune challenges on the behavior, development and inflammatory responses in pregnant mice and their offspring. Brain Behav Immun 38:77-90
53. Zuckerman L, Weiner I (2005) Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J Psychiatr Res 39:311-323
54. Zuckerman L et al (2003) 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 neu-rodevelopmental model of schizophrenia. Neuropsychopharmacology 28 (10):1778-1789
55. De Miranda J et al (2010) Induction of Toll-like receptor 3-mediated immunity during gestation inhibits cortical neurogenesis and causes behavioral disturbances. MBio 1(4): e00176410
56. Meyer U et al (2010) Chronic clozapine treatment improves prenatal infection-induced working memory deficits without influencing adult hippocampal neurogenesis. Psychopharmacology (Berl) 208(4):531-543
57. Shi L et al (2009) Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav Immun 23 (1):116-123
58. Ratnayake U et al (2012) 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 26(8):1288-1299
59. Giovanoli S et al (2013) Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 339(6123):1095-1099
60. Winter C et al (2009) Prenatal immune activation leads to multiple changes in basal neurotransmitter levels in the adult brain: implications for brain disorders of neurodeve-lopmental origin such as schizophrenia. Int J Neuropsychopharmacol 12(04):513-524
61. Vuillermot S et al (2010) A longitudinal examination of the neurodevelopmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia. J Neurosci 30 (4):1270-1287
62. Meyer U et al (2008) Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 33(2):441-456
63. Ozawa KK et al (2006) Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol Psychiatry 59 (6):546-554
64. Nyffeler M et al (2006) Maternal immune activation during pregnancy increases limbic GABAA receptor immunoreactivity in the adult offspring: implications for schizophrenia. Neuroscience 143(1):51-62
65. Meyer U et al (2008) Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 22 (4):469-486
66. Li Q et al (2009) Prenatal immune challenge is an environmental risk factor for brain and behavior change relevant to schizophrenia: evidence from MRI in a mouse model. PLoS One 4(7):e6354
67. Piontkewitz Y et al (2011) Abnormal trajectories of neurodevelopment and behavior following in utero insult in the rat. Biol Psychiatry 70(9):842-851
68. Wilson CA, Koenig JI (2014) Social interaction and social withdrawal in rodents as readouts for investigating the negative symptoms of schizophrenia. Eur Neuropsychopharmacol 24 (5):759-773
69. Ratnayake U et al (2014) Prenatal exposure to the viral mimetic Poly I:C alters fetal brain cytokine expression, and postnatal behaviour. Dev Neurosci 36:83
70. Bauman MD et al (2014) Activation of the maternal immune system during pregnancy alters behavioral development of rhesus monkey offspring. Biol Psychiatry 75(4):332-341
71. Schwartzer JJ et al (2013) Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice. Transl Psychiatr 3:e240
72. Nuechterlein KH et al (2004) Identification of separable cognitive factors in schizophrenia. Schizophr Res 72(1):29-39
73. Ito HT et al (2010) Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav Immun 24(6):930-941
74. Savanthrapadian S et al (2013) Enhanced hippocampal neuronal excitability and LTP persistence associated with reduced behavioral flexibility in the maternal immune activation model of schizophrenia. Hippocampus 23 (12):1395-1409
75. Zhang Y et al (2012) Prenatal exposure to a viral mimetic alters behavioural flexibility in male, but not female, rats. Neuropharmacology 62(3):1299-1307
76. Han M et al (2012) Gender differences in cognitive function of patients with chronic schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 39(2):358-363
77. Wolff AR et al (2011) Behavioural deficits associated with maternal immune activation in the rat model of schizophrenia. Behav Brain Res 225(1):382-387
78. Howland JG et al (2012) Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy. Neuroscience 201:184-198
79. Abazyan B et al (2010) Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol Psychiatry 68(12):1172-1181
80. Feldon J, Weiner I (1992) From an animal model of an attentional deficit towards new insights into the pathophysiology of schizophrenia. J Psychiatr Res 26(4):345-366
81. Weiner I (2003) The “two-headed” latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment. Psychopharmacology (Berl) 169(3-4):257-297
82. Zuckerman L, Weiner I (2003) Post-pubertal emergence of disrupted latent inhibition following prenatal immune activation. Psychopharmacology (Berl) 169(3/4):308
83. Ellinwood EH Jr et al (1973) Evolving behavior in the clinical and experimental amphetamine (model) psychosis. Am J Psychiatry 130 (10):1088-1093
84. Snyder SH (1973) Amphetamine psychosis: a “model” schizophrenia mediated by catecholamines. Am J Psychiatry 130(1):61-67
85. van den Buuse M et al (2005) Importance of animal models in schizophrenia research. Aust N Z J Psychiatry 39(7):550-557
86. Makinodan M et al (2008) Maternal immune activation in mice delays myelination and axonal development in the hippocampus of the offspring. J Neurosci Res 86(10):2190-2200
87. Wolff AR, Bilkey DK (2008) Immune activation during mid-gestation disrupts sensorimotor gating in rat offspring. Behav Brain Res 190 (1):156-159
88. Deslauriers J et al (2014) Preventive effect of alpha-lipoic acid on prepulse inhibition deficits in a juvenile two-hit model of schizophrenia. Neuroscience 272:261
89. Stridh L et al (2013) Toll-like receptor-3 activation increases the vulnerability of the neonatal brain to hypoxia-ischemia. J Neurosci 33 (29):12041-12051
90. Romero E et al (2010) Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia. Mol Psychiatry 15(4):372-383