Toxoplasma gondii Infection Potentiates Cognitive Impairments of Alzheimer's Disease in the BALB/c Mice

Journal of Parasitology

Volumn 102, Issue 6, 2016, Pages 629-635

  Mahmoudvand, Hossein ^a   Sheibani, Vahid ^b   Shojaee, Saeideh ^c   Mirbadie, Seyed Reza ^d   Keshavarz, Hossein ^c   Esmaeelpour, Khadijeh ^b   Keyhani, Ali Reza ^e   Ziaali, Naser ^f  

^a LORESTAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d SHAHROUD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^f KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MESSENGER RNA; TUMOR NECROSIS FACTOR; AMYLOID BETA PROTEIN; CYTOKINE;

BRAIN; COGNITION; DISEASE INCIDENCE; IMMUNE RESPONSE; MICROORGANISM; NERVOUS SYSTEM DISORDER; RODENT;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE COURSE; HIPPOCAMPUS; IMMUNOCOMPETENT CELL; LEARNING DISORDER; MALE; MEMORY; MORRIS WATER MAZE TEST; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROANATOMY; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SPATIAL LEARNING; TOXOPLASMOSIS; ANIMAL; ANIMAL TOXOPLASMOSIS; BRAIN; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GENETICS; MAZE TEST; METABOLISM; PARASITOLOGY; PATHOLOGY; RANDOMIZATION; SPATIAL MEMORY; SWIMMING;

ANIMALIA; MUS; TOXOPLASMA; TOXOPLASMA GONDII;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CYTOKINES; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED BALB C; NITRIC OXIDE SYNTHASE TYPE II; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPATIAL LEARNING; SPATIAL MEMORY; SWIMMING; TOXOPLASMOSIS, ANIMAL;

EID: 85010022808     PISSN: 00223395     EISSN: 19372345     Source Type: Journal    
DOI: 10.1645/16-28     Document Type: Article

References (34)

1. BLENNOW, K., M. J. DE LEON, AND H. ZETTERBERG. 2006. Alzheimers disease. Lancet 368: 387-403.
2. DALIMI, A., AND A. ABDOLI. 2012. Latent toxoplasmosis and human. Iranian Journal of Parasitology 2: 1-17.
3. DANIELS, B. P., S. R. SESTITO, AND S. T. ROUSE. 2015. An expanded task battery in the Morris water maze reveals effects of Toxoplasma gondii infection on learning and memory in rats. Parasitology International 64: 5-12.
4. DUBEY, J. P. 2004. Toxoplasmosis-A waterborne zoonosis. Veterinary Parasitology 126: 57-72.
5. DUNN, A. J. 2006. Effects of cytokines and infections on brain neurochemistry. Clinical Neuroscience Research 6: 52-68.
6. ESMAEILI-MAHANI, S., Z. EBRAHIMI, T. NORAIE, V. SHEIBANI, AND Z. HAJIALIZADEH. 2013. Exercise-induced morphine insensitivity is accompanied with a decrease in specific G-protein subunits gene expression in rats. Pharmacology, Biochemistry and Behavior 105: 128-133.
7. FEKADU, A., T. SHIBRE, AND A. J. CLEARE. 2010. Toxoplasmosis as a cause for behavior disorders-Overview of evidence and mechanisms. Folia Parasitology (Praha) 57: 105-113.
8. FERRI, C. P., R. SOUSA, E. ALBANESE, W. S. RIBEIRO, AND M. HONYASHIKI. 2009. World Alzheimer Report 2009-Executive summary. In Alzheimers Disease International, M. Prince and J. Jackson (eds.). Alzheimers Disease International, London, U.K., 1-22.
9. GATKOWSKA, J., M. WIECZOREK, B. DZIADEK, K. DZITKO, AND H. DLUGONSKA. 2013. Sex-dependent neurotransmitter level changes in brains of Toxoplasma gondii infected mice. Experimental Parasitology 133: 1-7.
10. GHORBANI, M., A. HAFIZI, M. T. SHEGERFCAR, M. REZAIAN, A.NADIM, M. ANWAR, AND A. AFSHAR. 1983. Animal toxoplasmosis in Iran. Journal of Tropical Medicine and Hygiene 86: 73-76.
11. GRIFFIN, W. S., J. G. SHENG, M. C. ROYSTON, S. M. GENTLEMAN, J. E. MCKENZIE, D. I. GRAHAM, G. W. ROBERTS, AND R. E. MRAK. 1998. Glial-neuronal interactions in Alzheimers disease: The potential role of a cytokine cycle in disease progression. Brain Pathology 8: 65-72.
12. GRIFFIN, W. S. T. 2000. IL-1 and the cytokine cycle in Alzheimers disease. Journal of Neurochemistry 74: S52-56.
13. HA, T. Y., K. A. CHANG, J. A. KIM, H. S. KIM, AND S. KIM. 2010. S100a9 knockdown decreases the memory impairment and the neuropathology in Tg2576, AD animal model. PLoS One 5: e8840.
14. HAROON, F., U. HANDEL, F. ANGENSTEIN, J. GOLDSCHMIDT, P. KREUTZMANN, AND H. LISON. 2012. Toxoplasma gondii actively inhibits neuronal function in chronically infected mice. PLoS One 7: e35516.
15. HENEKA, M. T., M. K. OBANION, D. TERWEL, AND M. P. KUMMER. 2010. Neuroinflammatory processes in Alzheimers disease. Journal of Neural Transmission 117: 919-947.
16. HILL, D., AND J. P. DUBEY. 2002. Toxoplasma gondii: Transmission, diagnosis and prevention. Clinical Microbiology and Infection 8: 634-640.
17. JUNG, B. K., K. H. PYO, K. Y. SHIN, Y. S.HWANG, H. LIM, S. J. LEE, J.H. MOON, S. H. LEE, AND Y. H. SUH. 2012. Toxoplasma gondii infection in the brain inhibits neuronal degeneration and learning and memory impairments in a murine model of Alzheimers disease. PLoS One 7: e33312.
18. LIESENFELD, O., I. PARVANOVA, J. ZERRAHN, S. J. HAN, F. HEINRICH, M. MUNOZ, F. KAISER, T. AEBISCHER, AND T. BUCH. 2011. The IFNgamma-inducible GTPase, Irga6, protects mice against Toxoplasma gondii but not against Plasmodium berghei and some other intracellular pathogens. PLoS One 6: e20568.
19. LIU, J., Y. MA, S. TIAN, L. ZHANG, M. ZHAO, Y. ZHANG, AND D. XU. 2014. T cells promote the regeneration of neural precursor cells in the hippocampus of Alzheimers disease mice. Neural Regeneration Research 9: 1541-1547.
20. MAHMOUDVAND, H., E. SAEDI DEZAKI, S. SOLEIMANI, M. R. BANESHI, F. KHEIRANDISH, B. EZATPOUR, AND N. ZIA-ALI. 2015a. Seroprevalence and risk factors of Toxoplasma gondii infection among healthy blood donors in southeast of Iran. Parasite Immunology 37: 362-367.
21. MAHMOUDVAND, H., N. ZIAALI, NI. AGHAEI, V. SHEIBANI, S. SHOJAEE, H. KESHAVARZ, AND M. SHABANI. 2015b. The possible association between Toxoplasma gondii infection and risk of anxiety and cognitive disorders in BALB/c mice. Pathogen and Global Health 109: 369-376.
22. MAHMOUDVAND, H., N. ZIAALI, H. GHAZVINI, S. SHOJAEE, H. KESHAVARZ, K. ESMAEILPOUR, AND V. SHEIBANI. 2016. Toxoplasma gondii infection promotes neuroinflammation through cytokine networks and induced hyperalgesia in BALB/c mice. Inflammation 39: 405-412.
23. MCCUSKER, R. H., AND K. W. KELLEY. 2013. Immune-neural connections: How the immune systems response to infectious agents influences behavior. Journal of Experimental Biology 216: 84-98.
24. MUNOZ, M., O. LIESENFELD, AND M. M. HEIMESAAT. 2011. Immunology of Toxoplasma gondii. Immunological Reviews 240: 269-285.
25. NOVOTNÁ, M., J. HANUSOVA, J. KLOSE, M. PREISS, J. HAVLICEK, K. ROUBALOVÁ, AND J. FLEGR. 2015. Probable neuroimmunological link between Toxoplasma and cytomegalovirus infections and personality changes in the human host. BMC Infectious Diseases 5: e54.
26. PRANDOVSZKY, E., E. GASKELL, H. MARTIN, J. P. DUBEY, J. P. WEBSTER, AND G. A. MCCONKEY. 2011. The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS One 6: e23866.
27. QUERFURTH, H.W., AND F. M. LAFERLA. 2010. Alzheimers disease. New England Journal of Medicine 362: 329-344.
28. SAADATI, H., S. ESMAEILI-MAHANI, K. ESMAEILPOUR, M. NAZERI, S. MAZHARI, AND V. SHEIBANI. 2015. Exercise improves learning and memory impairments in sleep deprived female rats. Physiology and Behavior 138: 285-291.
29. SAITO, K., S. P. MARKEY, AND M. P. HEYES. 1991. Chronic effects of gamma-interferon on quinolinic acid and indoleamine-2, 3-dioxygenase in brain of C57BL6 mice. Brain Research 546: 151-154.
30. TORREY, E. F., J. J. BARTKO, AND R. H. YOLKEN. 2012. Toxoplasma gondii and other risk factors for schizophrenia: An update. Schizophrenia Bulletin 38: 642-647.
31. WEBSTER, J. P. 2007. The effect of Toxoplasma gondii on animal behavior: Playing cat and mouse. Schizophrenia Bulletin 33: 752-756.
32. WORTH, A. R., A. J. LYMBERY, AND R. C. A. THOMPSON. 2013. Adaptive host manipulation by Toxoplasm gondii: Fact or fiction? Trends in Parasitology 29: 150-155.
33. YILMAZ, K. O., M. OZLEM, Y. MEHMET, A. ORHAN CEM, Y. SULEYMAN. 2011. Could Toxoplasma gondii have any role in Alzheimer disease? Alzheimer Disease and Associated Disorders 25: 1-3.
34. ZHOU, Y. H., X. B. WANG, S. F. JIANG, Y. L. XU, J. P. TAO, X. P. ZHANG, Y. ZHANG, AND Q. GAO. 2011. Impairment of learning and memory ability in mice with latent infection of Toxoplasma gondii. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 29: 333-338.