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Comparative characterization of microRNA profiles of different genotypes of Toxoplasma gondii

Published online by Cambridge University Press:  29 May 2013

M. J. XU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, PR China
D. H. ZHOU
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, PR China
S. Y. HUANG*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, PR China
F. R. ZHAO
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, PR China
A. J. NISBET
Affiliation:
Vaccines and Diagnostics, Moredun Research Institute, Pentlands Science Park, Midlothian EH26 0PZ, Scotland
R. Q. LIN
Affiliation:
College of Veterinary Medicine, South China Agricultural University, Guangzhou, Guangdong Province 510642, PR China
H. Q. SONG
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, PR China
X. Q. ZHU*
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province 730046, PR China College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang Province 163319, PR China
*
*Corresponding authors. State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, People's Republic of China. E-mail: xingquanzhu1@hotmail.com; siyang.huang@hotmail.com
*Corresponding authors. State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, CAAS, Lanzhou 730046, People's Republic of China. E-mail: xingquanzhu1@hotmail.com; siyang.huang@hotmail.com

Summary

The present study compared the miRNA expression profiles of five Toxoplasma gondii strains, namely RH (Type I, ToxoDB10), TgXD (Type I, ToxoDB10), PRU (Type II, ToxoDB1), QHO (Type II, ToxoDB1) and TgC7 (ToxoDB9), by Solexa deep sequencing, bioinformatics analysis and real-time quantitative PCR. A total of 7, 15, 10, 12 and 10 miRNAs were found from RH, TgXD, PRU, QHO and TgC7 strains, respectively. Thirteen miRNAs were shared by three genotypes, with only one miRNA shared by all of the 5 strains and others shared by 2 or more strains. A large number of targets ranging from 1 to 185 were identified for commonly shared miRNAs and strain-specific miRNAs with complete or nearly complete complementarity. Functional prediction showed that these targets were mostly focused on catalytic activity (191 targets) and binding activity (183 targets). Nonetheless, the majority of targets and most of the miRNAs are related to the virulence or invasion proteins of different strains of T. gondii, including ROP and MIC, as well as some other proteins, such as AMA1, GRA and RHO. The present study characterized comparatively the miRNA profiles of 3 different genotypes of T. gondii, identified genotype-shared miRNAs and strain-specific miRNAs.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Ajzenberg, D., Banuls, A. L., Tibayrenc, M. and Darde, M. L. (2002). Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. International Journal for Parasitology 32, 2738.CrossRefGoogle ScholarPubMed
Araujo, F., Slifer, T. and Kim, S. (1997). Chronic infection with Toxoplasma gondii does not prevent acute disease or colonization of the brain with tissue cysts following reinfection with different strains of the parasite. Journal of Parasitology 83, 521522.CrossRefGoogle ScholarPubMed
Boothroyd, J. C. and Dubremetz, J. F. (2008). Kiss and spit: the dual roles of Toxoplasma rhoptries. Nature Reviews. Microbiology 6, 7988.CrossRefGoogle ScholarPubMed
Braun, L., Cannella, D., Ortet, P., Barakat, M., Sautel, C. F., Kieffer, S., Garin, J., Bastien, O., Voinnet, O. and Hakimi, M. A. (2010). A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathogens 6, e1000920.CrossRefGoogle ScholarPubMed
Chen, C., Ridzon, D. A., Broomer, A. J., Zhou, Z., Lee, D. H., Nguyen, J. T., Barbisin, M., Xu, N. L., Mahuvakar, V. R., Andersen, M. R., Lao, K. Q., Livak, K. J. and Guegler, K. J. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research 33, e179.CrossRefGoogle ScholarPubMed
Dao, A., Fortier, B., Soete, M., Plenat, F. and Dubremetz, J. F. (2001). Successful reinfection of chronically infected mice by a different Toxoplasma gondii genotype. International Journal for Parasitology 31, 6365.CrossRefGoogle ScholarPubMed
de Roever-Bonnet, H. (1969). Congenital toxoplasma infections in mice and hamsters infected with avirulent and virulent strains. Tropical and Geographical Medicine 21, 443450.Google Scholar
Dowse, T. J. and Soldati, D. (2005). Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature. Trends in Parasitology 21, 254258.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2010). Toxoplasmosis of Animals and Humans, 2nd Edn, p. 313. CRC Press, Boca Raton, Florida.Google Scholar
Dubey, J. P., Lago, E. G., Gennari, S. M., Su, C. and Jones, J. L. (2012). Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 139, 13751424.CrossRefGoogle ScholarPubMed
Howe, D. K. and Sibley, L. D. (1995). Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. Journal of Infectious Diseases 172, 15611566.CrossRefGoogle ScholarPubMed
Huynh, M. H., Harper, J. M. and Carruthers, V. B. (2006). Preparing for an invasion: charting the pathway of adhesion proteins to Toxoplasma micronemes. Parasitology Research 98, 389395.CrossRefGoogle ScholarPubMed
Jerome, M. E., Radke, J. R., Bohne, W., Roos, D. S. and White, M. W. (1998). Toxoplasma gondii bradyzoites form spontaneously during sporozoite-initiated development. Infection and Immunity 66, 48384844.CrossRefGoogle ScholarPubMed
Khan, A., Taylor, S., Ajioka, J. W., Rosenthal, B. M. and Sibley, L. D. (2009). Selection at a single locus leads to widespread expansion of Toxoplasma gondii lineages that are virulent in mice. PLoS Genetics 5, e1000404.CrossRefGoogle Scholar
Kruger, J. and Rehmsmeier, M. (2006). RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Research 34, W451W454.CrossRefGoogle ScholarPubMed
Lau, N. C., Lim, L. P., Weinstein, E. G. and Bartel, D. P. (2001). An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858862.CrossRefGoogle ScholarPubMed
Lehmann, T., Marcet, P. L., Graham, D. H., Dahl, E. R. and Dubey, J. P. (2006). Globalization and the population structure of Toxoplasma gondii. Proceedings of the National Academy of Sciences USA 103, 1142311428.CrossRefGoogle ScholarPubMed
Lewis, B. P., Burge, C. B. and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 1520.CrossRefGoogle ScholarPubMed
Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., Bartel, D. P., Linsley, P. S. and Johnson, J. M. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769773.CrossRefGoogle ScholarPubMed
Mirovsky, P. and Valkoun, A. (1981). Preparation of purified Toxoplasma gondii suspensions. Folia Parasitologica (Praha) 28, 2327.Google ScholarPubMed
Nam, H. W. (2009). GRA proteins of Toxoplasma gondii: maintenance of host–parasite interactions across the parasitophorous vacuolar membrane. Korean Journal of Parasitology 47(Suppl), S29S37.CrossRefGoogle ScholarPubMed
Olguin-Lamas, A., Madec, E., Hovasse, A., Werkmeister, E., Callebaut, I., Slomianny, C., Delhaye, S., Mouveaux, T., Schaeffer-Reiss, C., Van Dorsselaer, A. and Tomavo, S. (2011). A novel Toxoplasma gondii nuclear factor TgNF3 is a dynamic chromatin-associated component, modulator of nucleolar architecture and parasite virulence. PLoS Pathogens 7, e1001328.CrossRefGoogle ScholarPubMed
Reikvam, A. and Lorentzen-Styr, A. M. (1976). Virulence of different strains of Toxoplasma gondii and host response in mice. Nature 261, 508509.CrossRefGoogle ScholarPubMed
Robert-Gangneux, F. and Darde, M. L. (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clinical Microbiology Reviews 25, 264296.CrossRefGoogle ScholarPubMed
Rodriguez, J. B. and Szajnman, S. H. (2012). New antibacterials for the treatment of toxoplasmosis; a patent review. Expert Opinion on Therapeutic Patents 22, 311333.CrossRefGoogle ScholarPubMed
Sibley, L. D. and Boothroyd, J. C. (1992). Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 359, 8285.CrossRefGoogle ScholarPubMed
Tyler, J. S., Treeck, M. and Boothroyd, J. C. (2011). Focus on the ringleader: the role of AMA1 in apicomplexan invasion and replication. Trends in Parasitology 27, 410420.CrossRefGoogle ScholarPubMed
Wang, J., Liu, X., Jia, B., Lu, H., Peng, S., Piao, X., Hou, N., Cai, P., Yin, J., Jiang, N. and Chen, Q. (2012). A comparative study of small RNAs in Toxoplasma gondii of distinct genotypes. Parasites and Vectors 5, 186.CrossRefGoogle ScholarPubMed
Wu, L., Fan, J. and Belasco, J. G. (2006). MicroRNAs direct rapid deadenylation of mRNA. Proceedings of the National Academy of Sciences USA 103, 40344039.CrossRefGoogle ScholarPubMed
Xu, M. J., Liu, Q., Nisbet, A. J., Cai, X. Q., Yan, C., Lin, R. Q., Yuan, Z. G., Song, H. Q., He, X. H. and Zhu, X. Q. (2010). Identification and characterization of microRNAs in Clonorchis sinensis of human health significance. BMC Genomics 11, 521.CrossRefGoogle ScholarPubMed
Xu, M. J., Liu, Q. Y., Fu, J. H., Nisbet, A. J., Shi, D. S., He, X. H., Pan, Y., Zhou, D. H., Song, H. Q. and Zhu, X. Q. (2012). Seroprevalence of Toxoplasma gondii and Neospora caninum infection in dairy cows in subtropical southern China. Parasitology 139, 14251428.CrossRefGoogle ScholarPubMed
Yildiz, K., Kul, O., Babur, C., Kilic, S., Gazyagci, A. N., Celebi, B. and Gurcan, I. S. (2009). Seroprevalence of Neospora caninum in dairy cattle ranches with high abortion rate: special emphasis to serologic co-existence with Toxoplasma gondii, Brucella abortus and Listeria monocytogenes. Veterinary Parasitology 164, 306310.CrossRefGoogle ScholarPubMed
Yu, J., Xia, Z., Liu, Q., Liu, J., Ding, J. and Zhang, W. (2007). Seroepidemiology of Neospora caninum and Toxoplasma gondii in cattle and water buffaloes (Bubalus bubalis) in the People's Republic of China. Veterinary Parasitology 143, 7985.CrossRefGoogle ScholarPubMed
Zhang, B., Wang, Q. and Pan, X. (2007). MicroRNAs and their regulatory roles in animals and plants. Journal of Cellular Physiology 210, 279289.CrossRefGoogle ScholarPubMed
Zhou, P., Zhang, H., Lin, R. Q., Zhang, D. L., Song, H. Q., Su, C. and Zhu, X. Q. (2009). Genetic characterization of Toxoplasma gondii isolates from China. Parasitology International 58, 193195.CrossRefGoogle ScholarPubMed
Zhou, P., Sun, X. T., Yin, C. C., Yang, J. F., Yan, H. K., Yuan, Z. G., Zhu, X. Q. and Zou, F. C. (2011). Genetic characterization of Toxoplasma gondii isolates from pigs in southwestern China. Journal of Parasitology 97, 11931195.CrossRefGoogle ScholarPubMed
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