Prenatal inflammation and neurodevelopment in schizophrenia: A review of human studies

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 42, Issue , 2013, Pages 92-100

  Miller, Brian J ^a   Culpepper, Nickolas ^a   Rapaport, Mark H ^b   Buckley, Peter ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Infection; Inflammation; Neurodevelopment; Pregnancy; Schizophrenia

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); BRAIN DERIVED NEUROTROPHIC FACTOR; C REACTIVE PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PHOSPHODIESTERASE 4B; PHOSPHODIESTERASE IV; PROTEIN KINASE B; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; BRAIN DEVELOPMENT; BRAIN MORPHOLOGY; COGNITION; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; FETUS RISK; GENE EXPRESSION; GENE INTERACTION; GENETIC ASSOCIATION; GENOTYPE ENVIRONMENT INTERACTION; HIGH RISK INFANT; HUMAN; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; INTRAUTERINE INFECTION; MOLECULAR PATHOLOGY; MORPHOLOGY; NONHUMAN; PRENATAL EXPOSURE; PROGENY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RISK ASSESSMENT; SCHIZOPHRENIA;

BRAIN; ENCEPHALITIS; FEMALE; HUMANS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; SCHIZOPHRENIA;

EID: 84873526928     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2012.03.010     Document Type: Article

References (75)

1. Abazyan B., Nomura J., Kannan G., Ishizuka K., Tamashiro K.L., Nucifora F., et al. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol Psychiatry 2010, 68:1172-1181.
2. Alvarez-de-la-Rosa M., Rebollo F.J., Codoceo R., Gonzalez Gonzalez A. Maternal serum interleukin 1, 2, 6, 8 and interleukin-2 receptor levels in preterm labor and delivery. Eur J Obstet Gynecol Reprod Biol 2000, 88:57-60.
3. Arion D., Travis U.T., Lewis D.A., Levitt P., Mirnics K. Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biol Psychiatry 2007, 62:711-721.
4. Bilbo S.D., Schwarz J.M. Early-life programming of later-life brain and behavior: a critical role for the immune system. Front Behav Neurosci 2009, 3:14.
5. Blackmore E.R., Moynihan J.A., Rubinow D.R., Pressman E.K., Gilchrist M., O'Connor T.G. Psychiatric symptoms and proinflammatory cytokines in pregnancy. Psychosom Med 2011, 73:656-663.
6. 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.
7. Borrell J., Vela J.M., Arévalo-Martin A., Molina-Holgado E., Guaza C. Prenatal immune challenge disrupts sensorimotor gating in adult rats. Implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 2002, 26:204-215.
8. Brown A., Derkits E. prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 2010, 167:261-280.
9. Brown A.S., Hooton J., Schaefer C.A., Zhang H., Petkova E., Babulas V., et al. Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. Am J Psychiatry 2004, 161:889-895.
10. Brown A.S., Vinogradov S., Kremen W.S., Poole J.H., Deicken R.F., Penner J.D., et al. Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. Am J Psychiatry 2009, 166:683-690.
11. Buka S.L., Tsuang M.T., Torrey E.F., Klebanoff M.A., Wagner R.L., Yolken R.H. Maternal cytokine levels during pregnancy and adult psychosis. Brain Behav Immun 2001, 15:411-420.
12. Cannon T.D., van Erp T.G., Rosso I.M., Huttunen M., Lönnqvist J., Pirkola T., et al. Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry 2002, 59:35-41.
13. Cassidy-Bushrow AE, Peters RM, Johnson DA, Templin TN. Association of depressive symptoms with inflammatory biomarkers among pregnant African-American women. J Reprod Immunol in press (Electronic publication ahead of print 2 March 2012).
14. Chen X., Wang X., Hossain S., O'Neill F.A., Walsh D., van den Oord E., et al. Interleukin 3 and schizophrenia: the impact of sex and family history. Mol Psychiatry 2007, 12:273-282.
15. Christian L.M., Franco A., Glaser R., Iams J.D. Depressive symptoms are associated with elevated serum proinflammatory cytokines among pregnant women. Brain Behav Immun 2009, 23:750-754.
16. Christian L.M., Franco A., Iams J.D., Sheridan J., Glaser R. Depressive symptoms predict exaggerated inflammatory responses to an in vivo immune challenge among pregnant women. Brain Behav Immun 2010, 24:49-53.
17. Clarke M., Tanskanen A., Huttunen M., Whittaker J., Cannon M. Evidence for an interaction between familial liability and prenatal exposure to infection in the causation of schizophrenia. Am J Psychiatry 2009, 166:1025-1030.
18. Conrad K.P., Miles T.M., Benyo D.F. Circulating levels of immunoreactive cytokines in women with preeclampsia. Am J Reprod Immunol 1998, 40:102-111.
19. Coussons-Read M.E., Okun M.L., Schmitt M.P., Giese S. Prenatal stress alters cytokine levels in a manner that may endanger human pregnancy. Psychosom Med 2005, 67:625-631.
20. Coussons-Read M.E., Okun M.L., Nettles C.D. Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 2007, 21:343-350.
21. Davis O.R., Breier A., Buchanan R.W., Holstein C. Obstetric complications in schizophrenia. Schizophr Res 1991, 4:255.
22. Deverman B.E., Patterson P.H. Cytokines and CNS development. Neuron 2009, 64:61-78.
23. Eaton W.W., Byrne M., Ewald H., Mors O., Chen C.Y., Agerbo E., et al. Association of schizophrenia and autoimmune diseases: linkage of Danish national registers. Am J Psychiatry 2006, 163:521-528.
24. Edwards T.L., Wang X., Chen Q., Wormly B., Riley B., O'Neill F.A., et al. Interaction between interleukin 3 and dystrobrevin-binding protein 1 in schizophrenia. Schizophr Res 2008, 106:208-217.
25. Ellman L.M., Yolken R.H., Buka S.L., Torrey E.F., Cannon T.D. Cognitive functioning prior to the onset of psychosis: the role of fetal exposure to serologically determined influenza infection. Biol Psychiatry 2009, 65:1040-1047.
26. Ellman L.M., Deicken R.F., Vinogradov S., Kremen W.S., Poole J.H., Kern D.M., et al. Structural brain alterations in schizophrenia following fetal exposure to the inflammatory cytokine interleukin-8. Schizophr Res 2010, 121:46-54.
27. Gaughran F., O'Neill E., Sham P., Daly R.J., Shanahan F. Soluble interleukin 2 receptor levels in families of people with schizophrenia. Schizophr Res 2002, 56:235-239.
28. Girard S., Tremblay L., Lepage M., Sébire G. IL-1 receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. J Immunol 2010, 184:3997-4005.
29. Gunawardana L., Zammit S., Lewis G., Gunnell D., Hollis C., Wolke D., et al. Examining the association between maternal analgesic use during pregnancy and risk of psychotic symptoms during adolescence. Schizophr Res 2011, 126:220-225.
30. Hänninen K., Katila H., Saarela M., Rontu R., Mattila K.M., Fan M., et al. Interleukin-1 beta gene polymorphism and its interactions with neuregulin-1 gene polymorphism are associated with schizophrenia. Eur Arch Psychiatry Clin Neurosci 2008, 258:10-15.
31. Hsu P.C., Nwulia E., Sawa A. Using bioinformatic tools. Am J Psychiatry 2009, 166:854.
32. Imamura Y., Nakane Y., Ohta Y., Kondo H. Lifetime prevalence of schizophrenia among individuals prenatally exposed to atomic bomb radiation in Nagasaki City. Acta Psychiatr Scand 1999, 100:344-349.
33. International Schizophrenia Consortium, Purcell S.M., Wray N.R., Stone J.L., Visscher P.M., O'Donovan M.C., et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 2009, 460:748-752.
34. Jia P., Wang L., Meltzer H.Y., Zhao Z. Common variants conferring risk of schizophrenia: a pathway analysis of GWAS data. Schizophr Res 2010, 122:38-42.
35. Jones P.B., Ranatakallio P., Hartikainen A.L., Isohanni M., Sipila P. Schizophrenia as a long-term outcome of pregnancy, delivery and perinatal complications: a 28-year follow-up of the 1966 north Finland general population birth cohort. Am J Psychiatry 1998, 155:335-364.
36. Kampman O., Anttila S., Illi A., Mattila K.M., Rontu R., Leinonen E., et al. Interaction of tumor necrosis alpha-G308A and epidermal growth factor gene polymorphisms in early-onset schizophrenia. Eur Arch Psychiatry Clin Neurosci 2005, 255:279-283.
37. Khashan A.S., Abel K.M., McNamee R., Pedersen M.G., Webb R.T., Baker P.N., et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 2008, 65:146-152.
38. Kirch D.G. Infection and autoimmunity as etiologic factors in schizophrenia: a review and reappraisal. Schizophr Bull 1993, 19:355-370.
39. Koenig J.I., Kirkpatrick B., Lee P. Glucocorticoid hormones and early brain development in schizophrenia. Neuropsychopharmacology 2002, 27:309-318.
40. Laskowska M., Laskowska K., Leszczyńska-Gorzelak B., Oleszczuk J. Comparative analysis of the maternal and umbilical interleukin-8 levels in normal pregnancies and in pregnancies complicated by preeclampsia with intrauterine normal growth and intrauterine growth retardation. J Matern Fetal Neonatal Med 2007, 20:527-532.
41. Malaspina D., Corcoran C., Kleinhaus K.R., Perrin M.C., Fennig S., Nahon D., et al. Acute maternal stress in pregnancy and schizophrenia in offspring: a cohort prospective study. BMC Psychiatry 2008, 8:71.
42. Marballi K., Quinones M.P., Jimenez F., Escamilla M.A., Raventós H., Soto-Bernardini M.C., et al. In vivo and in vitro genetic evidence of involvement of neuregulin 1 in immune system dysregulation. J Mol Med 2010, 88:1133-1141.
43. Mattes E., McCarthy S., Gong G., van Eekelen J., Dunstan J., Foster J., et al. Maternal mood scores in mid-pregnancy are related to aspects of neonatal immune function. Brain Behav Immun 2009, 23:380-388.
44. Messias E.L., Chen C.Y., Eaton W.W. Epidemiology of schizophrenia: review of findings and myths. Psychiatr Clin North Am 2007, 30:323-338.
45. Meyer U., Murray P., Urwyler A., Yee B., Schedlowski M., Feldon J. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol Psychiatry 2008, 13:208-221.
46. Meyer U., Feldon J., Yee B.K. A review of the fetal brain cytokine imbalance hypothesis of schizophrenia. Schizophr Bull 2009, 35:959-972.
47. Miller B., Messias E., Miettunen J., Alaräisänen A., Jarvelin M.-R., Koponen H., et al. Meta-analysis of paternal age and schizophrenia risk. in male versus female offspring. Schizophr Bull 2011, 37:1039-1047.
48. Moilanen K., Jokelainen J., Jones P.B., Hartikainen A.L., Järvelin M.R., Isohanni M. Deviant intrauterine growth and risk of schizophrenia: a 34-year follow-up of the Northern Finland 1966 Birth Cohort. Schizophr Res 2010, 124:223-230.
49. Monji A., Kato T., Kanba S. Cytokines and schizophrenia: microglia hypothesis of schizophrenia. Psychiatry Clin Neurosci 2009, 63:257-265.
50. Myhrman A., Rantakallio P., Isohanni M., Jones P., Partanen U. Unwantedness of a pregnancy and schizophrenia in the child. Br J Psychiatry 1996, 169:637-640.
51. Nagai T., Ibi D., Yamada K. Animal model for schizophrenia that reflects gene-environment interactions. Biol Pharm Bull 2011, 34:1364-1368.
52. Nawa H., Takei N. Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci Res 2006, 56:2-13.
53. Nunes S.O., Matsuo T., Kaminami M.S., Watanabe M.A., Reiche E.M., Itano E.N. An autoimmune or an inflammatory process in patients with schizophrenia, schizoaffective disorder, and in their biological relatives. Schizophr Res 2006, 84:180-182.
54. Okazaki K., Nishida A., Kato M., Kozawa K., Uga N., Kimura H. Elevation of cytokine concentrations in asphyxiated neonates. Biol Neonate 2006, 89:183-189.
55. Papiol S., Molina V., Desco M., Rosa A., Reig S., Gispert J.D., et al. Ventricular enlargement in schizophrenia is associated with a genetic polymorphism at the interleukin-1 receptor antagonist gene. Neuroimage 2005, 27:1002-1006.
56. Patterson P. Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav Brain Res 2009, 204:313-321.
57. Paul-Samojedny M., Kowalczyk M., Suchanek R., Owczarek A., Fila-Danilow A., Szczygiel A., et al. Functional polymorphism in the interleukin-6 and interleukin-10 genes in patients with paranoid schizophrenia-a case-control study. J Mol Neurosci 2010, 42:112-119.
58. Richardson A.C., Carpenter M.W. Inflammatory mediators in gestational diabetes mellitus. Obstet Gynecol Clin North Am 2007, 34:213-224.
59. Roiz-Santiáñez R., Crespo-Facorro B., Pérez-Iglesias R., Pelayo-Terán J.M., Carrasco-Marín E., Mata I., et al. Interleukin-1 receptor antagonist genotype and brain morphometry in first-episode non-affective psychosis. Psychiatry Res 2008, 162:167-171.
60. Romero E., Ali C., Mlina-Holgado E., Castellano B., Guaza C., Borrell J. Neurobehavioral and immunological consequences of prenatal immune activation in rats. Influence of antipsychotics. Neuropsychopharmacology 2007, 32:1791-1804.
61. Romero E., Guaza C., Castellano B., Borrell J. Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia. Mol Psychiatry 2010, 15:372-383.
62. Saetre P., Emilsson L., Axelsson E., Kreuger J., Linkholm E., Jazin E. Inflammation-related genes up-regulated in schizophrenia brains. BMC Psychiatry 2007, 7:46.
63. Samuelsson A.M., Jennische E., Hansson H.A., Holmäng 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.
64. Sävman K., Blennow M., Gustafson K., Tarkowski E., Hagberg H. Cytokine response in cerebrospinal fluid after birth asphyxia. Pediatr Res 1998, 43:746-751.
65. Schlotz W., Phillips D.I. Fetal origins of mental health: evidence and mechanisms. Brain Behav Immun 2009, 23:905-916.
66. Shi J., Levinson D.F., Duan J., Sanders A.R., Zheng Y., Pe'er I., et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 2009, 460:753-757.
67. Smith S., Li J., Garbett K., Mirnics K., Patterson P. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 2007, 27:10695-10702.
68. Song C., Merali Z., Anisman H. Variations of nucleus accumbens dopamine and serotonin following systemic interleukin-1, interleukin-2 or interleukin-6 treatment. Neuroscience 1999, 88:823-836.
69. Sørensen H.J., Mortensen E.L., Reinisch J.M., Mednick S.A. Association between prenatal exposure to analgesics and risk of schizophrenia. Br J Psychiatry 2004, 185:366-371.
70. Stefannson H., Ophoff R.A., Steinberg S., Andreassen O.A., Cichon S., Rujescu D., et al. Common variants conferring risk of schizophrenia. Nature 2009, 460:744-747.
71. Susser E.S., Lin S.P. Schizophrenia after prenatal exposure to the Dutch Huger Winter of 1944-1945. Arch Gen Psychiatry 1992, 49:983-988.
72. von Minckwitz G., Grischke E.M., Schwab S., Hettinger S., Loibl S., Aulmann M., et al. Predictive value of serum interleukin-6 and -8 levels in preterm labor or rupture of the membranes. Acta Obstet Gynecol Scand 2000, 79:667-672.
73. Zalcman S., Green-Johnson J.M., Murray L., Nance D.M., Dyck D., Anisman H., et al. Cytokine-specific central monoamine alterations induced by interleukin-1, -2 and -6. Brain Res 1994, 643:40-49.
74. Zalcman S., Savina I., Wise R.A. Interleukin-6 increases sensitivity to the locomotor-stimulating effects of amphetamine in rats. Brain Res 1999, 847:276-283.
75. Zammit S., Odd D., Horwood J., Thompson A., Thomas K., Menezes P., et al. Investigating whether adverse prenatal and perinatal events are associated with non-clinical psychotic symptoms at age 12 years in the ALSPAC birth cohort. Psychol Med 2009, 39:1457-1467.