Toxoplasma gondii and cognitive deficits in schizophrenia: An animal model perspective

Schizophrenia Bulletin

Volumn 38, Issue 6, 2012, Pages 1155-1161

  Kannan, Geetha ^a   Pletnikov, Mikhail V ^a,b  

^a Department of Psychiatry and Behavioral Sciences ^*  (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

environment interactions; gene ; immune system; infection; kynurenine; learning and memory; Toxoplasma

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENOTYPE ENVIRONMENT INTERACTION; IMMUNE SYSTEM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; BRAIN; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; HUMANS; MICE; RATS; SCHIZOPHRENIA; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; TOXOPLASMOSIS, CEREBRAL;

EID: 84869003435     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbs079     Document Type: Article

References (50)

1. Reichenberg A, Weiser M, Caspi A, et al. Premorbid intellectual functioning and risk of schizophrenia and spectrum disorders. J Clin Exp Neuropsychol. 2006;28:193-207.
2. Nuechterlein KH, Green MF, Kern RS, et al. The MATRICS consensus cognitive battery, part 1: test selection, reliability, and validity. Am J Psychiatry. 2008;165:203-213.
3. Keefe RS. Should cognitive impairment be included in the diagnostic criteria for schizophrenia? World Psychiatry. 2008;7:22-28.
4. Shirts BH, Prasad KM, Pogue-Geile MF, Dickerson F, Yolken RH, Nimgaonkar VL. Antibodies to cytomegalovirus and Herpes Simplex Virus 1 associated with cognitive function in schizophrenia. Schizophr Res. 2008;106:268-274.
5. Dollard SC, Grosse SD, Ross DS. New estimates of the prevalence of neurological and sensory sequelae and mortality associated with congenital cytomegalovirus infection. Rev Med Virol. 2007;17:355-363.
6. Webster JP. Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour. Microbes Infect. 2001;3:1037-1045.
7. Saeij JP, Boyle JP, Boothroyd JC. Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol. 2005;21:476-481.
8. Dubey JP, Lindsay DS, Speer CA. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev. 1998;11:267-299.
9. Yolken RH, Dickerson FB, Fuller TE. Toxoplasma and schizophrenia. Parasite Immunol. 2009;31:706-715.
10. Saxon SA, Knight W, Reynolds DW, Stagno S, Alford CA. Intellectual deficits in children born with subclinical congenital toxoplasmosis: a preliminary report. J Pediatr. 1973;82:792-797.
11. Jones JL, Lopez A, Wilson M, Schulkin J, Gibbs R. Congenital toxoplasmosis: a review. Obstet Gynecol Surv. 2001;56:296-305.
12. Brown AS, Vinogradov S, Kremen WS, et al. Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. Am J Psychiatry. 2009;166:683-690.
13. Piekarski G, Zippelius HM, Witting PA. Effects of a latent Toxoplasma infection on the learning ability in white laboratory rats and mice (author's transl). Z Parasitenkd. 1978;57(1):1-15.
14. Witting PA. Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Z Parasitenkd. 1979;61:29-51.
15. Kannan G, Moldovan K, Xiao JC, Yolken RH, Jones-Brando L, Pletnikov MV. Toxoplasma gondii strain-dependent effects on mouse behaviour. Folia Parasitol (Praha). 2010;57:151-155.
16. Hay J, Aitken PP, Graham DI. Toxoplasma infection and response to novelty in mice. Z Parasitenkd. 1984;70:575-588.
17. Webster JP, Brunton CF, MacDonald DW. Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology. 1994;109:37-43.
18. Hutchison WM, Aitken PP, Wells WP. Chronic Toxoplasma infections and familiarity-novelty discrimination in the mouse. Ann Trop Med Parasitol. 1980;74:145-150.
19. Hodkova H, Kodym P, Flegr J. Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism? Parasitology. 2007;134:1329-1337.
20. Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci U S A. 2007;104:6442-6447.
21. Gulinello M, Acquarone M, Kim JH, et al. Acquired infection with Toxoplasma gondii in adult mice results in sensorimotor deficits but normal cognitive behavior despite widespread brain pathology. Microbes Infect. 2010;12:528-537.
22. Xiao J, Kannan G, Jones-Brando L, et al. Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience. 2012;206:39-48.
23. Flegr J, Lenochova P, Hodny Z, Vondrova M. Fatal attraction phenomenon in humans: cat odour attractiveness increased for toxoplasma-infected men while decreased for infected women. PLoS Negl Trop Dis. 2011;5:e1389.
24. Wang T, Liu M, Gao XJ, Zhao ZJ, Chen XG, Lun ZR. Toxoplasma gondii: the effects of infection at different stages of pregnancy on the offspring of mice. Exp Parasitol. 2011;127:107-112.
25. Webster JP. The effect of Toxoplasma gondii on animal behavior: playing cat and mouse. Schizophr Bull. 2007;33:752-756.
26. Liesenfeld O, Nguyen TA, Pharke C, Suzuki Y. Importance of gender and sex hormones in regulation of susceptibility of the small intestine to peroral infection with Toxoplasma gondii tissue cysts. J Parasitol. 2001;87:1491-1493.
27. Roberts CW, Cruickshank SM, Alexander J. Sex-determined resistance to Toxoplasma gondii is associated with temporal differences in cytokine production. Infect Immun. 1995;63:2549-2555.
28. Zenner L, Foulet A, Caudrelier Y, et al. Infection with Toxoplasma gondii RH and Prugniaud strains in mice, rats and nude rats: kinetics of infection in blood and tissues related to pathology in acute and chronic infection. Pathol Res Pract. 1999;195:475-485.
29. McAfoose J, Baune BT. Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev. 2009;33:355-366.
30. Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA. A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS One. 2009;4:e4801.
31. Prandovszky E, Gaskell E, Martin H, Dubey JP, Webster JP, McConkey GA. The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS One. 2011;6:e23866.
32. Stibbs HH. Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Ann Trop Med Parasitol. 1985;79:153-157.
33. Goodwin DG, Hrubec TC, Klein BG, et al. Congenital infection of mice with Toxoplasma gondii induces minimal change in behavior and no change in neurotransmitter concentrations. J Parasitol. 2012;98:706-712.
34. Moghaddam B, Javitt D. From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology. 2011;37:4-15.
35. Schwarcz R, Hunter CA. Toxoplasma gondii and schizophrenia: linkage through astrocyte-derived kynurenic acid? Schizophr Bull. 2007;33:652-653.
36. Potter MC, Elmer GI, Bergeron R, et al. Reduction of endogenous kynurenic acid formation enhances extracellular glutamate, hippocampal plasticity, and cognitive behavior. Neuropsychopharmacology. 2010;35:1734-1742.
37. Huerta PT, Kowal C, DeGiorgio LA, Volpe BT, Diamond B. Immunity and behavior: antibodies alter emotion. Proc Natl Acad Sci U S A. 2006;103:678-683.
38. Birner P, Gatterbauer B, Drobna D, Bernheimer H. Molecular mimicry in infectious encephalitis and neuritis: binding of antibodies against infectious agents on Western blots of human nervous tissue. J Infect. 2000;41:32-38.
39. Kosugi I, Kawasaki H, Tsuchida T, Tsutsui Y. Cytomegalovirus infection inhibits the expression of N-methyl-D-aspartate receptors in the developing mouse hippocampus and primary neuronal cultures. Acta Neuropathol. 2005;109:475-482.
40. Glynn MW, Elmer BM, Garay PA, et al. MHCI negatively regulates synapse density during the establishment of cortical connections. Nat Neurosci. 2011;14:442-451.
41. Luder CG, Lang C, Giraldo-Velasquez M, Algner M, Gerdes J, Gross U. Toxoplasma gondii inhibits MHC class II expression in neural antigen-presenting cells by down-regulating the class II transactivator CIITA. J Neuroimmunol. 2003;134:12-24.
42. Kipnis J, Cohen H, Cardon M, Ziv Y, Schwartz M. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc Natl Acad Sci U S A. 2004;101:8180-8185.
43. Moritz S, Kuelz AK, Jacobsen D, Kloss M, Fricke S. Severity of subjective cognitive impairment in patients with obsessive-compulsive disorder and depression. J Anxiety Disord. 2006;20:427-443.
44. Manove E, Levy B. Cognitive impairment in bipolar disorder: an overview. Postgrad Med. 2010;122:7-16.
45. Chadman KK, Yang M, Crawley JN. Criteria for validating mouse models of psychiatric diseases. Am J Med Genet B Neuropsychiatr Genet. 2009;150B(1):1-11.
46. Millar JK, Wilson-Annan JC, Anderson S, et al. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet. 2000;9:1415-1423.
47. Brandon NJ, Sawa A. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci. 2011;12:707-722.
48. Abazyan B, Nomura J, Kannan G, et al. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology. Biol Psychiatry. 2011;68:1172-1181.
49. Carter CJ. Schizophrenia susceptibility genes directly implicated in the life cycles of pathogens: cytomegalovirus, influenza, herpes simplex, rubella, and Toxoplasma gondii. Schizophr Bull. 2009;35:1163-1182.
50. Webster JP, Lamberton PH, Donnelly CA, Torrey EF. Parasites as causative agents of human affective disorders? The impact of anti-psychotic, mood-stabilizer and anti-parasite medication on Toxoplasma gondii's ability to alter host behaviour. Proc Biol Sci. 2006;273:1023-1030.