European Neuropsychopharmacology
Volume 19, Issue 9 , Pages 648-653 , September 2009

Prenatal viral infection of mice at E16 causes changes in gene expression in hippocampi of the offspring

  • S. Hossein Fatemi

      Affiliations

    • Department of Psychiatry, Division of Neuroscience Research, University of Minnesota School of Medicine, Minneapolis, USA
    • Department of Pharmacology, University of Minnesota School of Medicine, Minneapolis, USA
    • Department of Neuroscience, University of Minnesota School of Medicine, Minneapolis, USA
    • Corresponding Author InformationCorresponding author. Department of Psychiatry, Division of Neuroscience Research, University of Minnesota, Medical School, MMC 392, 420 Delaware St. S.E., Minneapolis, MN 55455, USA. Tel.: +1 612 626 3633; fax: +1 612 624 8935.
  • ,
  • Timothy D. Folsom

      Affiliations

    • Department of Psychiatry, Division of Neuroscience Research, University of Minnesota School of Medicine, Minneapolis, USA
  • ,
  • Teri J. Reutiman

      Affiliations

    • Department of Psychiatry, Division of Neuroscience Research, University of Minnesota School of Medicine, Minneapolis, USA
  • ,
  • Hao Huang

      Affiliations

    • Department of Radiology, Division of NMR, Johns Hopkins University School of Medicine, Baltimore, USA
  • ,
  • Kenichi Oishi

      Affiliations

    • Department of Radiology, Division of NMR, Johns Hopkins University School of Medicine, Baltimore, USA
  • ,
  • Susumu Mori

      Affiliations

    • Department of Radiology, Division of NMR, Johns Hopkins University School of Medicine, Baltimore, USA

Received 21 January 2009 ,Revised 4 March 2009 ,Accepted 24 March 2009.

References 

  1. Arndt TL, Stodgell CJ, Rodier PM. The teratology of autism. Int. J. Dev. Neurosci. 2005;23(2–3):189–199
  2. Arnold SE, Trojanowski JQ. Recent advanced in defining the neuropathology of schizophrenia. Acta Neuropath. 1996;92:217–231
  3. Aylward EH, Minshew NJ, Goldstein G, Honeycutt NA, Augustine AM, Yates KO, et al. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology. 1999;53:2145–2150
  4. Bauman ML, Kemper TL. Neuroanatomic observations of the brain in autism. In:  Bauman ML,  Kemper TL editor. The Neurobiology of Autism. Baltimore, MD: Johns Hopkins University Press; 1994;p. 19–145
  5. Brown AS. Prenatal infection as a risk factor for schizophrenia. Schizophr. Bull. 2006;32:200–202
  6. Brown AS, Begg MD, Gravenstein S, Schaefer CA, Wyatt RJ, Bresnahan M, et al. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry. 2004;61:774–780
  7. Chambers JS, Perrone-Bizzozero NI. Altered myelination of the hippocampal formation in subjects with schizophrenia and bipolar disorder. Neurochem. Res. 2004;29:2293–2302
  8. Connor SE, Ng V, McDonald C, Schulze K, Morgan K, Dazzan P, et al. A study of hippocampal shape anomaly in schizophrenia and in families multiply affected by schizophrenia or bipolar disorder. Neuroradiology. 2004;46:523–534
  9. In:  Fatemi SH editors. Neuropsychiatric Disorders and Infection. London: Taylor & Francis; 2005;
  10. Fatemi SH. Schizophrenia. In:  Fatemi SH,  Clayton P editor. The Medical Basis of Psychiatry. Third Edition. New York: Humana Press; 2008;p. 85–108
  11. Fatemi SH, Sidwell R, Akhter P, Sedgewick J, Thuras P, Bailey K, et al. Human influenza viral infection in utero increases nNOS expression in hippocampi of neonatal mice. Synapse. 1998;29:84–88
  12. Fatemi SH, Sidwell R, Kist D, Akhter P, Meltzer HY, Bailey K, et al. Differential expression of synaptosome-associated protein 25 kDa [SNAP-25] in hippocampi of neonatal mice following exposure to human influenza virus in utero. Brain Res. 1998;800:1–9
  13. Fatemi SH, Emamian ES, Kist D, Sidwell RW, Nakajima K, Akhter P, et al. Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol. Psychiatry. 1999;4(2):145–154
  14. Fatemi SH, Cuadra AE, El-Fakahany EE, Sidwell RW, Thuras P. Prenatal viral infection causes alterations in nNOS expression in developing brains. Neuroreport. 2000;11:1493–1496
  15. Fatemi SH, Emamian ES, Sidwell RW, Kist DA, Stary JM, Earle JA, et al. Human influenza viral infection in utero alters glial fibrillary acidic protein immunoreactivity in the developing brains of neonatal mice. Mol. Psychiatry. 2002;7:633–640
  16. Fatemi SH, Earle J, Kanodia R, Kist D, Patterson P, Shi L, et al. Prenatal viral infection causes macrocephaly and pyramidal cell atrophy in the developing mice. Cell. Mol. Neurobiol. 2002;22:25–33
  17. Fatemi SH, Araghi-Niknam M, Laurence JA, Stary JM, Sidwell RW, Lee S. Glial fibrillary acidic protein and glutamic acid decarboxylase 65 and 67 kDa proteins are increased in brains of neonatal BALB/c mice following viral infection in utero. Schizophr. Res. 2004;69:121–123
  18. 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
  19. Fatemi SH, Reutiman TJ, Folsom TD, Huang H, Oishi K, Mori S, et al. Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders. Schizophr. Res. 2008;99:56–70
  20. Fatemi SH, Folsom TD, Reutiman TJ, Lee S. Expression of astrocytic markers aquaporin 4 and connexin 43 is altered in brains of subjects with autism. Synapse. 2008;62:501–507
  21. Fatemi SH, Folsom TD, Reutiman TJ, Sidwell RW. Viral regulation of aquaporin 4, connexin 43, microcephalin and nucleolin. Schizophr. Res. 2008;98:163–177
  22. Feldcamp LA, Souza RP, Romano-Silva M, Kennedy JL, Wong AH. Reduced prefrontal cortex DARPP-32 mRNA in completed suicide victims with schizophrenia. Schizophr. Res. 2008;103:192–200
  23. Gong X, Jia M, Ruan Y, Shuang M, Liu J, Wu S, et al. Association between the FOXP2 gene and autistic disorder in Chinese population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2004;127:113–116
  24. Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2001;98:4746–4751
  25. Hamid EH, Hyde TM, Egan MF, Wolf SS, Herman MM, Nemeroff CB, et al. Neurotensin receptor binding abnormalities in the entorhinal cortex in schizophrenia and affective disorders. Biol. Psychiatry. 2002;51:795–800
  26. Harrison PJ, Owen MJ. Genes for schizophrenia? Recent findings and their pathophysiological implications. Lancet. 2003;361:417–419
  27. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Lange N, Bakardjiev A, et al. Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain. 2003;126:1182–1192
  28. Hurst JA, Baraitser M, Auger E, Graham F, Norel SV. An extended family with a dominantly inherited speech disorder. Dev. Med. Child Neurol. 1990;32:352–355
  29. Kakinuma H, Ozaki M, Sato H, Takahashi H. Variation in GABA-A subunit gene copy number in an autistic patient with mosaic 4p duplication (p12p16). Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008;147B:973–975
  30. Laurence JA, Fatemi SH. Glial fibrillary acidic protein is elevated in superior frontal, parietal and cerebellar cortices of autistic subjects. Cerebellum. 2005;4:206–210
  31. Lehman DM, Harrison JM. Flash visual evoked potentials in the hypomyelinated mutant mouse shiverer. Doc. Ophthalmol. 2002;104:83–95
  32. Le-Niculescu H, Balaraman Y, Patel S, Tan J, Sidhu K, Jerome RE, et al. Towards understanding the schizophrenia code: an expanded convergent functional genomics approach. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2007;144B:129–158
  33. Lewis CM, Levinson DF, Wise LH, DeLisi LE, Straub RE, Hovatta I, et al. Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: schizophrenia. Am. J. Hum. Genet. 2003;73:34–48
  34. Libbey JE, Sweeten TL, McMahon WM, Fujinami RS. Autistic disorder and viral infections. J. Neurovirology. 2005;11:1–10
  35. Marui T, Funatogawa I, Koishi S, Yamamoto K, Matsumoto H, Hashimoto O, et al. Association of the neuronal cell adhesion molecule (NRCAM) gene variants with autism. Int. J. Neuropsychopharmacol. 2008;30:1–10
  36. Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, et al. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 2006;26:4752–4762
  37. Meyer U, Yee BK, Feldon J. The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse?. Neuroscientist. 2007;13:241–256
  38. Mori S, Ito R, Zhang J, Kaufmann WE, van Zijl PC, Solaiyappan M, et al. Diffusion tensor imaging of the developing mouse brain. Magn. Reson. Med. 2001;46:18–23
  39. Papadopoulos MC, Manley GT, Krishna S, Verkman AS. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 2004;18:1291–1293
  40. Rodier PM. Chronology of neuron development animal studies and their clinical implications. Dev. Med. Child Neurol. 1980;22:525–545
  41. Sanjuan J, Tolosa A, Gonzalez JC, Aguilar EJ, Perez-Tur J, Najera C, et al. Association between FOXP2 polymorphisms and schizophrenia with auditory hallucinations. Psychiatr. Genet. 2006;16:67–72
  42. Shi L, Fatemi SH, Sidwell RW, Patterson PH. A mouse model of mental illness: maternal influenza infection causes behavioral and pharmacological abnormalities in the offspring. J. Neurosci. 2003;23:297–302
  43. So HC, Chen RY, Chen EY, Cheung EF, Li T, Sham PC. An association study of RGS4 polymorphisms with clinical phenotypes of schizophrenia in a Chinese population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008;147B:77–85
  44. Sparks BF, Friedman SD, Shaw DW, Aylward EH, Echelard D, Artru AA, et al. Brain structural abnormalities in young children with autism spectrum disorder. Neurology. 2002;59:184–192
  45. Steffek AE, McCullumsmith RE, Haroutunian V, Meador-Woodruff JH. Cortical expression of glial fibrillary acidic protein and glutamine synthetase is decreased in schizophrenia. Schizophr. Res. 2008;103:71–82
  46. Sultana R, Yu CE, Yu J, Munson J, Chen D, Hua W, et al. Identification of a novel gene on chromosome 7q11.2 interrupted by a translocation breakpoint in a pair of autistic twins. Genomics. 2002;80:129–134
  47. Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, et al. Schizophrenia after prenatal famine. Arch. Gen. Psychiatry. 1997;53:25–31
  48. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, et al. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet. 2003;362:798–805
  49. Verkman AS, Binder DK, Bloch O, Auguste K, Papadopoulos MC. Three distinct roles of aquaporin-4 in brain function revealed by knockout mice. Biochim. Biophys. Acta. 2006;1758:1085–1093
  50. Weiss AP, Dewitt I, Goff D, Ditman T, Heckers S. Anterior and posterior hippocampal volumes in schizophrenia. Schizophr. Res. 2005;73:103–112
  51. Wu Z, Irizarry R, Gentleman R, Murillo F, Spencer F. A model based background adjustment for oligonucleotide expression arrays. In: Technical Report. Johns Hopkins University, Department of Biostatistics Working Papers, Baltimore, MD. 2004;

PII: S0924-977X(09)00091-1

doi: 10.1016/j.euroneuro.2009.03.004

European Neuropsychopharmacology
Volume 19, Issue 9 , Pages 648-653 , September 2009