Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring

Journal of Neuroscience

Volumn 23, Issue 1, 2003, Pages 297-302

  Shi, Limin ^a   Fatemi, S Hossein ^b   Sidwell, Robert W ^c   Patterson, Paul H ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UTAH STATE UNIVERSITY   (United States)

Author keywords

Acoustic startle; Autism; Chlorpromazine; Clozapine; Ketamine; Mental retardation; Novel object; Open field; Poly(I:C); Prepulse inhibition; Schizophrenia

Indexed keywords

CHLORPROMAZINE; CLOZAPINE; DOUBLE STRANDED RNA; KETAMINE; POLYINOSINIC POLYCYTIDYLIC ACID;

ACUTE DRUG ADMINISTRATION; ADOLESCENT; ANIMAL BEHAVIOR; ARTICLE; AUTISM; BEHAVIOR DISORDER; BREEDING; CONTROLLED STUDY; DRUG RESPONSE; EXPLORATORY BEHAVIOR; FEMALE; FETUS; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VIRUS; MATERNAL DISEASE; MOUSE; NONHUMAN; PHARMACOLOGY; PREGNANCY; PREPULSE INHIBITION; PRIORITY JOURNAL; PROGENY; SCHIZOPHRENIA; SOCIAL INTERACTION;

EID: 0037218688     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-01-00297.2003     Document Type: Article

References (42)

1. Boin F, Zanardini R, Pioli R, Altamura CA, Maes M, Germarelli M (2001) Association between-G308A tumor necrosis factor alpha gene polymorphism and schizophrenia. Mol Psychiat 6:79-82.
2. Brown AS, Schaefer CA, Wyatt RJ, Goetz R, Begg MD, Gorman JM, Susser ES (2000) Maternal exposure to respiratory infections and adult schizophrenia spectrum disorders: A prospective birth cohort study. Schizophrenia Bull 26:287-295.
3. Burger RA, Warren RP (1998) Possible immunogenetic basis for autism. Ment Retard Dev Disabil Res Rev 4:137-141.
4. Cella M, Salio M, Sakakibara Y, Langen H, Julkunen I, Lanzavecchia A (1999) Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 189:821-829.
5. Ciaranello AL, Ciaranello RD (1995) The neurobiology of infantile autism. Annu Rev Neurosci 18:101-128.
6. Cotter D, Takei N, Farrell M, Sham P, Quinn P, Larkin C, Oxford J, Murray R, O'Callaghan E (1995) Does prenatal exposure to influenza in mice induce pyramidal cell disarray in the dorsal hippocampus? Schizophrenia Res 16:233-241.
7. Ellison G (1995) The N-methyl-D-aspartate antagonists phencyclidine, ketamine, dizocilpine as both behavioral and anatomical models of the dementias. Brain Res Rev 20:250-267.
8. Fatemi SH, Sidwell RW, Akhter P, Sedgewick J, Thuras P, Bailey K, Kist D (1998a) Human influenza viral infection in utero increases nNOS expression in hippocampi of neonatal mice. Synapse 29:84-88.
9. Fatemi SH, Sidwell RW, Kist D, Akhter P, Meltzer HY, Bailey K, Thuras P, Sedgewick J (1998b) 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 800:1-9.
10. Fatemi SH, Emamian ES, Kist D, Sidwell RW, Nakajima K, Akhter P, Shie A, Sheikh S, Bailey K (1999) Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol Psychiat 4:145-154.
11. Fatemi SH, Cuadra AE, El-Fakahany EE, Sidwell RW, Thuras P (2000) Prenatal viral infection causes alterations in nNOS expression in developing mouse brains. NeuroReport 11:1493-1496.
12. Fatemi SH, Earle J, Kamodia R, Kist D, Emamian ES, Patterson PH, Shi L, Sidwell R (2002) Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: Implications for genesis of autism and schizophrenia. Cell Mol Neurobiol 22:25-33.
13. File SE (1985) Models of anxiety. Br J Clin Prac 38:15-20.
14. Geyer MA, Braff DL, Swerdlow NR (1999) Startle-response measures of information processes in animals: Relevance to schizophrenia. In: Animal Models of Human Emotion and Cognition (Haug M, Whalen, RE, eds), pp 103-116. Washington, DC: American Psychiatric Association.
15. Gust ID, Hampson AW, Lavachy D (2001) Planning for the next pandemic of influenza. Rev Med Virol 11:59-70.
16. Hornig M, Lipkin WI (2001) Infectious and immune factors in the pathogenesis of neurodevelopmental disorders: Epidemiology, hypotheses and animal models. Ment Retard Dev Disabil Res Rev 7:200-210.
17. Impagnatiello F, Guidotti AR, Pesold C, Dwivedi Y, Caruncho H, Pisu MG, Uzunov DP, Smallheiser NR, Davis JM, Pandey GN, Pappas GD, Tueting P, Sharma RP, Costa E (1998) A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc Natl Acad Sci USA 95:15718-15723.
18. Irving WL, James DK, Stephenson T, Laing P, Jameson C, Oxford JS, Chakraverty P, Brown DWG, Boon ACM, Zambon MC (2000) Influenza virus infection in the second and third trimesters of pregnancy: A clinical and seroepidemiological study. Br J Obstet Gynecol 107:1282-1289.
19. Jyonouchi H, Sun SN, Le H (2001) Proinflammatory and regulatory cytokine production associated with innate and adaptive immune responses in children with autism spectrum disorders and developmental regression. J Neuroimmunol 120:170-179.
20. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59:107-128.
21. Malhotra AK, Pinals DA, Adler CM, Elman I, Clifton A, Pickar D, Breier A (1997) Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 17:141-150.
22. Marenco S, Weinberger DR (2000) The neurodevelopmental hypothesis of schizophrenia: Following a trail of evidence from cradle to grave. Dev Psychopathol 12:501-527.
23. McAlonan GM, Daly E, Kumari V, Critchley HD, van Amelsvoort T, Suckling J, Simmons A, Sigmundsson T, Greenwood K, Russell A, Schmitz N, Happe F, Howlin P, Murphy DG (2002) Brain anatomy and sensorimotor gating in Asperger's syndrome. Brian 125:1594-1606.
24. Mednick SA, Machon RA, Huttunen MO, Bonett D (1988) Adult schizophrenia following prenatal exposure to influenza epidemic. Arch Gen Psychiat 45:189-192.
25. Muller N, Riedel M, Ackenheil M, Schwarz MJ (1999) The role of immune function in schizophrenia: An overview. Eur Arch Psychiat Clin Neurosci 249 [Suppl 4]:62-68.
26. Nawa H, Takahashi M, Patterson P (2000) Cytokine and growth factor involvement in schizophrenia: Support for the developmental model. Mol Psychiat 5:594-603.
27. Patterson PH (2002) Maternal infection: Window on neuroimmune inter-actions in fetal brain development and mental illness. Curr Opin Neurobiol 12:115-118.
28. Pearce BD (2001) Schizophrenia and viral infection during neurodevelopment: A focus on mechanisms. Mol Psychiat 6:634-646.
29. Purcell AE, Jeon OH, Zimmerman AW, Pevsner J (2001) Postmortem brain abnormalities of the glutamate neurotransmitter system in autism. Neurology 57:1618-1628.
30. Rothermundt M, Arolt V, Bayer TA (2001) Review of immunological and immunopathological findings in schizophrenia. Brain Behav Immunol 15:319-339.
31. Shahab SZ, Glezen WP (1994) Influenza virus. In: Viral Diseases in Pregnancy (Gonik B, ed), pp 215-223. New York: Springer.
32. Sidwell RW, Huffman JH, Call EW, Alaghamandan H, Cook PD, Robins RK (1986) Effect of selenazofurin on influenza A and B virus infections of mice. Antiviral Res 6:343-353.
33. Stuart-Harris CH, Schild GC, Oxford JA (1985) Influenza: The Viruses and the Disease, 2nd Ed. Littleton, MA: Publishing Sciences Group.
34. Swerdlow NR, Geyer MA (1998) Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophrenia Bull 24:285-301.
35. Swerdlow NR, Bakshi V, Waikar M, Taaid N, Geyer MA (1998) Seroquel, clozapine and chlorpromazine restore sensorimotor gating in ketaminetreated rats. Psychopharmacology 140:75-80.
36. Torrey EF, Yolken RH (2000) Familial and genetic mechanisms in schizophrenia. Brain Res Rev 31:113-117.
37. Tumpey TM, Lu X, Morken T, Zaki SR, Katz JM (2000) Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (HSN1) virus isolated from humans. J Virol 74:6105-6116.
38. Van Reeth KV (2000) Cytokines in the pathogenesis of influenza. Vet Microbiol 74:109-116.
39. Verdijk RM, Mutis T, Esendam B, Kamp J, Melief DJM, Brand A, Goulmy E (1999) Polyriboinosinic polyribocytidylic acid (Poly(I:C)) induces stable maturation of functionally active human dendritic cells. J Immunol 163:57-61.
40. Weiss SM, Lightower S, Stanhope KJ, Kennett GA, Dourish CT (2000) Measurement of anxiety in transgenic mice. Rev Neurosci 11:59-74.
41. Williams K, MacKenzie JS (1977) Influenza infections during pregnancy in the mouse. J Hygiene 79:249-257.
42. Wright P, Murray RM (1993) Schizophrenia: Prenatal influenza and autoimmunity. Ann Med 25:497-502.