Chronic infection of Toxoplasma gondii downregulates miR-132 expression in multiple brain regions in a sex-dependent manner

Parasitology

Volumn 760, Issue , 2014, Pages 623-632

  Li, Ye ^a,b   Kannan, Geetha ^a   Pletnikov, Mikhail V ^a   Yolken, Robert H ^a   Xiao, Jianchun ^a  

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

^b WUHAN UNIVERSITY   (China)

Author keywords

BDNF; Bradyzoite density; Hippocampus; Host sex; MiR 132; Toxoplasma gondii

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MICRORNA 132; DNA; RNA; RNA 5S; MICRORNA; MIRN132 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRADYZOITE; BRAIN CORTEX; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; DOWN REGULATION; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; HYPOTHALAMUS; IN VIVO STUDY; INFECTION SENSITIVITY; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; PARASITE LOAD; POLYMERASE CHAIN REACTION; TOXOPLASMA GONDII; TOXOPLASMOSIS; TROPISM; BRAIN TISSUE; CHRONIC DISEASE; DISEASE PREDISPOSITION; INFECTION; PRIORITY JOURNAL; SEX DIFFERENCE; ANIMAL; ANIMAL TOXOPLASMOSIS; BAGG ALBINO MOUSE; BRAIN; CEREBRAL TOXOPLASMOSIS; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PARASITOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; TOXOPLASMA;

MUS; TOXOPLASMA GONDII;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DOWN-REGULATION; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICRORNAS; PARASITE LOAD; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; SEX FACTORS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; TOXOPLASMOSIS, CEREBRAL;

EID: 84911380811     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S003118201400167X     Document Type: Article

References (29)

1. Airan, R. D., Meltzer, L. A., Roy, M., Gong, Y., Chen, H. and Deisseroth, K. (2007). High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 317, 819-823.
2. Benraiss, A., Chmielnicki, E., Lerner, K., Roh, D. and Goldman, S. A. (2001). Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. The Journal of Neuroscience 21, 6718-6731.
3. Berenreiterová, M., Flegr, J., Kuběna, A. A. and Němec, P. (2011). The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: implications for the behavioral manipulation hypothesis. PLoS ONE 6, e28925.
4. Gulinello, M., Acquarone, M., Kim, J. H., Spray, D. C., Barbosa, H. S., Sellers, R., Tanowitz, H. B. and Weiss, L. M. (2010). Acquired infection with Toxoplasma gondii in adult mice results in sensorimotor deficits but normal cognitive behavior despite widespread brain pathology. Microbes and Infection 12, 528-537.
5. Hansen, K. F., Sakamoto, K., Wayman, G. A., Impey, S. and Obrietan, K. (2010). Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS ONE 5, e15497.
6. Hansen, K. F., Karelina, K., Sakamoto, K., Wayman, G. A., Impey, S. and Obrietan, K. (2013). miRNA-132: a dynamic regulator of cognitive capacity. Brain Structure and Function 218, 817-831.
7. Haroon, F., Händel, U., Angenstein, F., Goldschmidt, J., Kreutzmann, P., Lison, H., Fischer, K. D., Scheich, H., Wetzel, W., Schlüter, D. and Budinger, E. (2012). Toxoplasma gondii actively inhibits neuronal function in chronically infected mice. PLoS One 7, e35516.
8. Hermes, G., Ajioka, J.W., Kelly, K. A., Mui, E., Roberts, F., Kasza, K., Mayr, T., Kirisits, M. J., Wollmann, R., Ferguson, D. J., Roberts, C.W., Hwang, J. H., Trendler, T., Kennan, R. P., Suzuki, Y., Reardon, C., Hickey, W. F., Chen, L. and McLeod, R. (2008). Neurological and behavioral abnormalities, ventricular dilatation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. Journal of Neuroinflammation 5, 48.
9. Hourez, R., Servais, L., Orduz, D., Gall, D., Millard, I., de Kerchove d'Exaerde, A., Cheron, G., Orr, H. T., Pandolfo, M. and Schiffmann, S. N. (2011). Aminopyridines correct early dysfunction and delay neurodegeneration in a mouse model of spinocerebellar ataxia type 1. The Journal of Neuroscience 31, 11795-11807.
10. Ingram, W. M., Goodrich, L. M., Robey, E. A., Eisen, M. B. (2013). Mice infected with low-virulence strains of Toxoplasma gondii lose their innate aversion to cat urine, even after extensive parasite clearance. PLoS One 8, e75246.
11. Lambert, T. J., Storm, D. R. and Sullivan, J. M. (2010). MicroRNA132 modulates short-term synaptic plasticity but not basal release probability in hippocampal neurons. PLoS ONE 5, e15182.
12. Lazarov, O., Robinson, J., Tang, Y. P., Hairston, I. S., Korade-Mirnics, Z., Lee, V. M., Hersh, L. B., Sapolsky, R. M., Mirnics, K. and Sisodia, S. S. (2005). Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120, 701-713.
13. Lindová, J., Kubena, A. A., Sturcová, H., Krivohlavá, R., Novotná, M., Rubesová, A., Havlícek, J., Kodym, P. and Flegr, J. (2010). Pattern of money allocation in experimental games supports the stress hypothesis of gender differences in Toxoplasma gondii-induced behavioural changes. Folia Parasitologica (Praha) 57, 136-142.
14. Magill, S. T., Cambronne, X. A., Luikart, B.W., Lioy, D. T., Leighton, B. H., Westbrook, G. L., Mandel, G. and Goodman, R. H. (2010). microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proceedings of the National Academy of Sciences of the USA 107, 20382-20387.
15. McHugh, T. J., Jones, M.W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A. and Tonegawa, S. (2007). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99.
16. Miller, B. H., Zeier, Z., Xi, L., Lanz, T. A., Deng, S., Strathmann, J., Willoughby, D., Kenny, P. J., Elsworth, J. D., Lawrence, M. S., Roth, R. H., Edbauer, D., Kleiman, R. J. and Wahlestedt, C. (2012). MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proceedings of the National Academy of Sciences of the USA 109, 3125-3130.
17. Monje, M. L., Toda, H. and Palmer, T. D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760-1765.
18. Remenyi, J., Hunter, C. J., Cole, C., Ando, H., Impey, S., Monk, C. E., Martin, K. J., Barton, G. J., Hutvagner, G. and Arthur, J. S. (2010). Regulation of the miR-212/132 locus by MSK1 and CREB in response to neurotrophins. The Biochemical Journal 428, 281-291.
19. Roberts, C.W., Cruickshank, S. M. and Alexander, J. (1995). Sex-determined resistance to Toxoplasma gondii is associated with temporal differences in cytokine production. Infection and Immunity 63, 2549-2555.
20. Takahashi, M., Ishikawa, K., Sato, N., Obayashi, M., Niimi, Y., Ishiguro, T., Yamada, M., Toyoshima, Y., Takahashi, H., Kato, T., Takao, M., Murayama, S., Mori, O., Eishi, Y. and Mizusawa, H. (2012). Reduced brain-derived neurotrophic factor (BDNF) mRNA expression and presence of BDNF-immunoreactive granules in the spinocerebellar ataxia type 6 (SCA6) cerebellum. Neuropathology 32, 595-603.
21. Tomita, T., Bzik, D. J., Ma, Y. F., Fox, B. A., Markillie, L. M., Taylor, R. C., Kim, K. and Weiss, L. M. (2013). The Toxoplasma gondii cyst wall protein CST1 is critical for cyst wall integrity and promotes bradyzoite persistence. PLoS Pathogens 9, e1003823.
22. Ueno, A., Dautu, G., Munyaka, B., Carmen, G., Kobayashi, Y. and Igarashi, M. (2009). Toxoplasma gondii: identification and characterization of bradyzoite-specific deoxyribose phosphate aldolase-like gene (TgDPA). Experimental Parasitology 121, 55-63.
23. Vyas, A., Kim, S. K., Giacomini, N., Boothroyd, J. C. and Sapolsky, R. M. (2007). Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proceedings of the National Academy of Sciences of the USA 104, 6442-6447.
24. Wanet, A., Tacheny, A., Arnould, T. and Renard, P. (2012). miR-212/ 132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Research 40, 4742-4753.
25. Wang, R. Y., Phang, R. Z., Hsu, P. H., Wang, W. H., Huang, H. T. and Liu, I. Y. (2013). In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus 23, 625-633.
26. Wibrand, K., Panja, D., Tiron, A., Ofte, M. L., Skaftnesmo, K. O., Lee, C. S., Pena, J. T., Tuschl, T. and Bramham, C. R. (2010). Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo. European Journal of Neuroscience 31, 636-645.
27. Xiao, J., Jones-Brando, L., Talbot, C. C., Jr. and Yolken, R. H. (2011). Differential effects of three canonical Toxoplasma strains on gene expression in human neuroepithelial cells. Infection and Immunity 79, 1363-1373.
28. Xiao, J., Kannan, G., Jones-Brando, L., Brannock, C., Krasnova, I. N., Cadet, J. L., Pletnikov, M. and Yolken, R. H. (2012). Sex-specific changes in gene expression and behavior induced by chronic Toxoplasma infection in mice. Neuroscience 206, 39-48.
29. Xiao, J., Li, Y., Prandovszky, E., Karuppagounder, S. S., Talbot, C. C., Jr., Dawson, V. L., Dawson, T. M. and Yolken, R. H. (2014). MicroRNA-132 dysregulation in Toxoplasma gondii infection has implications for dopamine signaling pathway. Neuroscience 268, 128-138.