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Molecular and immunological characterization of encoding gene and 14-3-3 protein 1 in Fasciola gigantica

Published online by Cambridge University Press:  29 August 2006

K. CHAITHIRAYANON ,
R. GRAMS ,
S. VICHASRI-GRAMS ,
A. HOFMANN ,
G. KORGE ,
V. VIYANANT ,
E. S. UPATHAM  and
P. SOBHON
K. CHAITHIRAYANON
Affiliation:
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok, 10400, Thailand
R. GRAMS
Affiliation:
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Phahonyothin Rd., Klongluang, Pathumthani, 12120, Thailand
S. VICHASRI-GRAMS
Affiliation:
Department of Biology, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok, 10400, Thailand
A. HOFMANN
Affiliation:
Institut für Biologie-Genetik, Freie Universität Berlin, Arnimallee 7, Berlin 14195, Germany
G. KORGE
Affiliation:
Institut für Biologie-Genetik, Freie Universität Berlin, Arnimallee 7, Berlin 14195, Germany
V. VIYANANT
Affiliation:
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Phahonyothin Rd., Klongluang, Pathumthani, 12120, Thailand
E. S. UPATHAM
Affiliation:
Department of Biology, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok, 10400, Thailand
P. SOBHON
Affiliation:
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok, 10400, Thailand
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Abstract

A cDNA encoding Fg14-3-3 protein 1 was cloned by immunoscreening of an adult-stage Fasciola gigantica cDNA library using a rabbit antiserum against tegumental antigens of the parasite. The protein has a deduced amino acid sequence of 252 residues and a calculated molecular weight of 28·7 kDa. It shows sequence identity values between 57·6 and 58·1% to the human 14-3-3 beta, zeta, theta, and eta proteins and is in a phylogenetic cluster with the 14-3-3 protein 1 of Schistosoma spp. Nucleic acid analyses indicate that the Fg14-3-3 protein 1 is encoded by a single copy gene and that this gene is expressed as a transcript of 1250 nucleotides. In adult and 4-week-old parasites the gene's transcriptional and translational products were localized in the gut epithelium, parenchyma, tegument cells, and in the reproductive organs. An antiserum against recombinant Fg14-3-3 protein 1 detected a slightly smaller 14-3-3 protein in the parasite's excretion/secretion material and showed cross-reactivity with 14-3-3 proteins in extracts of other trematodes and mouse. Antibodies against Fg14-3-3 protein were detected in the sera of rabbits as early as 2 weeks after infection with metacercariae of F. gigantica and the antibody titre increased continuously over a 10-week observation period.

Keywords

Fasciola gigantica14-3-3 proteintegumental antigensexpressionlocalization
Type
Research Article
Information
Parasitology , Volume 133 , Issue 6 , December 2006 , pp. 763 - 775
Copyright
2006 Cambridge University Press

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References

REFERENCES

Aitken, A. ( 1995). 14-3-3 proteins on the MAP. Trends in Biochemical Sciences 20, 95–97. doi: 10.1016/S0968-0004(00)88971-9.CrossRefGoogle Scholar
Aitken, A. ( 1996). 14-3-3 and its possible role in co-ordinating multiple signalling pathways. Trends in Cell Biology 6, 341–347. doi: 10.1016/0962-8924(96)10029-5.CrossRefGoogle Scholar
Aitken, A. ( 2002). Functional specificity in 14-3-3 isoform interactions through dimer formation and phosphorylation. Chromosome location of mammalian isoforms and variants. Plant Molecular Biology 50, 993–1010. doi: 10.1023/A:1021261931561.CrossRefGoogle Scholar
Aitken, A., Collinge, D. B., van Heusden, B. P., Isobe, T., Roseboom, P. H., Rosenfeld, G. and Soll, J. ( 1992). 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins. Trends in Biochemical Sciences 17, 498–501.CrossRefGoogle Scholar
Aitken, A., Jones, D., Soneji, Y. and Howell, S. ( 1995). 14-3-3 proteins: biological function and domain structure. Biochemical Society Transactions 23, 605–611.CrossRefGoogle Scholar
Andrade, M. A., Siles-Lucas, M., Espinoza, E., Perez Arellano, J. L., Gottstein, B. and Muro, A. ( 2004). Echinococcus multilocularis laminated-layer components and the E14t 14-3-3 recombinant protein decrease NO production by activated rat macrophages in vitro. Nitric Oxide 10, 150–155. doi: 10.1016/j.niox.2004.03.002.CrossRefGoogle Scholar
Bairoch, A. and Bucher, P. ( 1994). PROSITE: recent developments. Nucleic Acids Research 22, 3583–3589.Google Scholar
Broadie, K., Rushton, E., Skoulakis, E. M. and Davis, R. L. ( 1997). Leonardo, a Drosophila 14-3-3 protein involved in learning, regulates presynaptic function. Neuron 19, 391–402. doi: 10.1016/S0896-6273(00)80948-4.CrossRefGoogle Scholar
Carreno, F. R., Goni, C. N., Castro, L. M. and Ferro, E. S. ( 2005). 14-3-3 epsilon modulates the stimulated secretion of endopeptidase 24.15. Journal of Neurochemistry 93, 10–25. doi: 10.1111/j.1471-4159.2004.02967.x.CrossRefGoogle Scholar
Cervi, L., Rossi, G., Cejas, H. and Masih, D. T. ( 1998). Fasciola hepatica-induced immune suppression of spleen mononuclear cell proliferation: role of nitric oxide. Clinical Immunology and Immunopathology 87, 145–154. doi:10.1006/clin.1997.4499.CrossRefGoogle Scholar
Chaithirayanon, K., Wanichanon, C., Vichasri-Grams, S., Ardseungneon, P., Grams, R., Viyanant, V., Upatham, E. S. and Sobhon, P. ( 2002). Production and characterization of a monoclonal antibody against 28·5 kDa tegument antigen of Fasciola gigantica. Acta Tropica 84, 1–8. doi: 10.1016/S0001-706(02)00138-9.CrossRefGoogle Scholar
Chamberlain, L. H., Roth, D., Morgan, A. and Burgoyne, R. D. ( 1995). Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis. Journal of Cell Biology 130, 1063–1070.CrossRefGoogle Scholar
Dougherty, M. K. and Morrison, D. K. ( 2004). Unlocking the code of 14-3-3. Journal of Cell Science 117, 1875–1884. doi: 10.1242/10.1242/jcs.01171.CrossRefGoogle Scholar
Edgar, R. C. ( 2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle Scholar
Grams, R., Vichasri-Grams, S., Sobhon, P., Upatham, E. S. and Viyanant, V. ( 2001). Molecular cloning and characterization of cathepsin L encoding genes from Fasciola gigantica. Parasitology International 50, 105–114. doi: 10.1016/S1383-5769(01)00068-X.CrossRefGoogle Scholar
Grens, A., Gee, L., Fisher, D. A. and Bode, H. R. ( 1996). CnNK-2 an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra. Developmental Biology 180, 473–488. doi: 10.1006/dbio.1996.0321.CrossRefGoogle Scholar
Hanna, R. E. ( 1980). Fasciola hepatica: glycocalyx replacement in the juvenile as a possible mechanism for protection against host immunity. Experimental Parasitology 50, 103–114.CrossRefGoogle Scholar
Ichimura, T., Uchiyama, J., Kunihiro, O., Ito, M., Horigome, T., Omata, S., Shinkai, F., Kaji, H. and Isobe, T. ( 1995). Identification of the site of interaction of the 14-3-3 protein with phosphorylated tryptophan hydroxylase. Journal of Biological Chemistry 270, 28515–28518.CrossRefGoogle Scholar
Liu, D., Bienkowska, J., Petosa, C., Collier, R. J., Fu, H. and Liddington, R. ( 1995). Crystal structure of the zeta isoform of the 14-3-3 protein. Nature, London 376, 191–194. doi: 10.1038/376191a0.CrossRefGoogle Scholar
Mas-Coma, S., Bargues, M. D. and Esteban, E. G. ( 1999). Human fasciolosis. In Fasciolosis ( ed. Dalton, J. P.), pp. 411–434. CABI Publishing, Wallingford.
Meemon, K., Grams, R., Vichasri-Grams, S., Hofmann, A., Korge, G., Viyanant, V., Upatham, E. S., Habe, S. and Sobhon, P. ( 2004). Molecular cloning and analysis of stage and tissue-specific expression of cathepsin B encoding genes from Fasciola gigantica. Molecular and Biochemical Parasitology 136, 1–10. doi: 10.1016/j.molbiopara.2004.02.010.CrossRefGoogle Scholar
Mulcahy, G. and Dalton, J. P. ( 2001). Cathepsin L proteinases as vaccines against infection with Fasciola hepatica (liver fluke) in ruminants. Research in Veterinary Science 70, 83–86. doi: 10.1053/rvsc.2000.0425.CrossRefGoogle Scholar
Pfukenyi, D. M. and Mukaratirwa, S. ( 2004). A retrospective study of the prevalence and seasonal variation of Fasciola gigantica in cattle slaughtered in the major abattoirs of Zimbabwe between 1990 and 1999. Onderstepoort Journal of Veterinary Research 71, 181–187.CrossRefGoogle Scholar
Roth, D. and Burgoyne, R. D. ( 1995). Stimulation of catecholamine secretion from adrenal chromaffin cells by 14-3-3 proteins is due to reorganisation of the cortical actin network. FEBS Letters 374, 77–81. doi: 10.1016/0014-5793(95)01080-X.CrossRefGoogle Scholar
Roth, D., Morgan, A. and Burgoyne, R. D. ( 1993). Identification of a key domain in annexin and 14-3-3 proteins that stimulate calcium-dependent exocytosis in permeabilized adrenal chromaffin cells. FEBS Letters 320, 207–210. doi: 10.1016/0014-5793(93)80587-K.CrossRefGoogle Scholar
Roth, D., Morgan, A., Martin, H., Jones, D., Martens, G. J., Aitken, A. and Burgoyne, R. D. ( 1994). Characterization of 14-3-3 proteins in adrenal chromaffin cells and demonstration of isoform-specific phospholipid binding. The Biochemical Journal 301, 305–310.CrossRefGoogle Scholar
Saitou, N. and Nei, M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Sambrook, J. and Russell, D. ( 2001). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Schechtman, D., Tarrab-Hazdai, R. and Arnon, R. ( 2001 a). The 14-3-3 protein as a vaccine candidate against schistosomiasis. Parasite Immunology 23, 213–217. doi: 10.1046/j.1365-3024.2001.00378.x.CrossRefGoogle Scholar
Schechtman, D., Winnen, R., Tarrab-Hazdai, R., Ram, D., Shinder, V., Grevelding, C. G., Kunz, W. and Arnon, R. ( 2001 b). Expression and immunolocalization of the 14-3-3 protein of Schistosoma mansoni. Parasitology 123, 573–582.Google Scholar
Siles-Lucas, M., Felleisen, R. S., Hemphill, A., Wilson, W. and Gottstein, B. ( 1998). Stage-specific expression of the 14-3-3 gene in Echinococcus multilocularis. Molecular and Biochemical Parasitology 91, 281–293. doi: 10.1016/S0166-6851(97)00208-9.CrossRefGoogle Scholar
Siles-Lucas, M. and Gottstein, B. ( 2003). The 14-3-3 protein: a key molecule in parasites as in other organisms. Trends in Parasitology 19, 575–581. doi: 10.1016/j.pt.2003.10.003.CrossRefGoogle Scholar
Siles-Lucas, M., Merli, M., Mackenstedt, U. and Gottstein, B. ( 2003). The Echinococcus multilocularis 14-3-3 protein protects mice against primary but not secondary alveolar echinococcosis. Vaccine 21, 431–439. doi: 10.1016/S0264-410(02)00517-0.CrossRefGoogle Scholar
Siles-Lucas, M., Nunes, C. P., Zaha, A. and Breijo, M. ( 2000). The 14-3-3 protein is secreted by the adult worm of Echinococcus granulosus. Parasite Immunology 22, 521–528. doi: 10.1046/j.1365-3024.2000.00334.x.CrossRefGoogle Scholar
Sobhon, P., Dangprasert, T., Chuanchaiyakul, S., Meepool, A., Khawsuk, W., Wanichanon, C., Viyanant, V. and Upatham, E. S. ( 2000). Fasciola gigantica: Ultrastructure of the adult tegument. Science Asia 26, 137–148.CrossRefGoogle Scholar
Spithill, T. W., Piedrafita, D. and Smooker, P. M. ( 1997). Immunological approaches for the control of fasciolosis. International Journal for Parasitology 27, 1221–1235. doi:10.1016/S0020-7519(97)00120-3.CrossRefGoogle Scholar
Sun, L., Bittner, M. A. and Holz, R. W. ( 2003). Rim, a component of the presynaptic active zone and modulator of exocytosis, binds 14-3-3 through its N terminus. Journal of Biological Chemistry 278, 38301–38309.CrossRefGoogle Scholar
Wedrychowicz, H., Lamparska, M., Kesik, M., Kotomski, G., Mieszczanek, J., Jedlina-Panasiuk, L. and Plucienniczak, A. ( 2003). The immune response of rats to vaccination with the cDNA or protein forms of the cysteine proteinase of Fasciola hepatica. Veterinary Immunology and Immunopathology 94, 83–93. doi: 10.1016/S0165-24277(03)00085-0.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION. ( 1995). Control of Foodborne Trematode Infections. WHO Technical Series No. 849. WHO, Geneva.
Xiao, B., Smerdon, S. J., Jones, D. H., Dodson, G. G., Soneji, Y., Aitken, A. and Gamblin, S. J. ( 1995). Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature, London 376, 188–191. doi: 10.1038/376188a0.CrossRefGoogle Scholar
Zhang, Y., Taylor, M. G., McCrossan, M. V. and Bickle, Q. D. ( 1999). Molecular cloning and characterization of a novel Schistosoma japonicum “irradiated vaccine-specific” antigen, Sj14-3-3. Molecular and Biochemical Parasitology 103, 25–34. doi: 10.1016/S0166-6851(99)00083-3.CrossRefGoogle Scholar