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Comparative analysis of two fatty acid binding proteins from Fasciola gigantica

Published online by Cambridge University Press:  16 June 2010

SUPATRA CHUNCHOB ,
RUDI GRAMS ,
VITHOON VIYANANT ,
PETER M. SMOOKER  and
SUKSIRI VICHASRI-GRAMS
SUPATRA CHUNCHOB
Affiliation:
Department of Biology, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok, 10400, Thailand
RUDI GRAMS
Affiliation:
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Phaholyothin Rd., Klongluang, Pathumthani, 12121, Thailand
VITHOON VIYANANT
Affiliation:
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Phaholyothin Rd., Klongluang, Pathumthani, 12121, Thailand
PETER M. SMOOKER
Affiliation:
School of Applied Sciences, RMIT University, BundooraVIC 3032, Australia
SUKSIRI VICHASRI-GRAMS*
Affiliation:
Department of Biology, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok, 10400, Thailand
*
*Corresponding author: Department of Biology, Faculty of Science, Mahidol University, 272 Rama VI Road, Ratchathewi, Bangkok 10400, Thailand. Tel: +662 201 5480. Fax: +662 354 7161. E-mail: grsvc@mahidol.ac.th
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Summary

Fatty acid binding proteins are considered to be promising vaccine candidates against trematodiasis. In order to provide additional information about their function in Fasciola gigantica we performed a comparative analysis of FgFABP1 and FgFABP3, two isoforms with quite different isoelectric points of 4·9 and 9·9 and 67% sequence identity. Both are expressed in the juvenile and adult parasite but differ in their tissue-specific distribution. In addition, the sequence of FABP3 is identical in F. hepatica and F. gigantica indicating the protein's functional importance in this genus. Immune sera produced against soluble recombinant FgFABPs reacted with 14 kDa antigens in crude worm, soluble egg, cirrus sac extracts, and excretion/secretion product. Both FgFABPs were located in the parenchyma of the parasite but in addition, FgFABP1 was abundant in testes and spermatozoa while FgFABP3 was abundant in vitelline cells, eggs, and caecal epithelium. Mass spectrometry identified FgFABP1 and FgFABP3 in the ES product whereas only FgFABP3 was identified in egg extract. Serum samples of an experimentally infected rabbit reacted from week 6 post-infection with FgFABP3 and from week 12 with FgFABP1 while sera of infected sheep were not reactive. The results suggest differences in the biological functions of these 2 isoforms and differences in the host/parasite interaction that should be considered for their potential as vaccines against fascioliasis.

Keywords

Fasciola giganticafatty acid binding proteintissue-specificity2DE proteomics
Type
Research Article
Information
Parasitology , Volume 137 , Issue 12 , October 2010 , pp. 1805 - 1817
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410. doi: 10.1006/jmbi.1990.9999.Google Scholar
Angelucci, F., Johnson, K. A., Baiocco, P., Miele, A. E., Brunori, M., Valle, C., Vigorosi, F., Troiani, A. R., Liberti, P., Cioli, D., Klinkert, M. Q. and Bellelli, A. (2004). Schistosoma mansoni fatty acid binding protein: specificity and functional control as revealed by crystallographic structure. Biochemistry 43, 13000–13011. doi: 10.1021/bi048505f.CrossRefGoogle ScholarPubMed
Brito, C. F., Oliveira, G. C., Oliveira, S. C., Street, M., Riengrojpitak, S., Wilson, R. A., Simpson, A. J. and Correa-Oliveira, R. (2002). Sm14 gene expression in different stages of the Schistosoma mansoni life cycle and immunolocalization of the Sm14 protein within the adult worm. Brazilian Journal of Medical and Biological Research 35, 377–381. doi: 10.1590/S0100-879X2002000300014.Google Scholar
Chmurzynska, A. (2006). The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. Journal of Applied Genetics 47, 39–48.Google Scholar
Espino, A. M. and Hillyer, G. V. (2001). Identification of fatty acid molecules in a Fasciola hepatica immunoprophylactic fatty acid-binding protein. Journal of Parasitology 87, 426–428. doi: 10.1645/0022-3395(2001)087[0426:IOFAMI]2.0.CO;2.CrossRefGoogle Scholar
Espino, A. M., Rodriguez Medina, J. R. and Hillyer, G. V. (2001). Isolation and immunological characterization of fatty acid binding protein isoforms from Fasciola hepatica. Journal of Parasitology 87, 1028–1033. doi: 10.2307/3285227.Google Scholar
Esteves, A., Dallagiovanna, B. and Ehrlich, R. (1993). A developmentally regulated gene of Echinococcus granulosus codes for a 15·5-kilodalton polypeptide related to fatty acid binding proteins. Molecular and Biochemical Parasitology 58, 215–222. doi: 10.1016/0166-6851(93)90043-W.CrossRefGoogle ScholarPubMed
Esteves, A. and Ehrlich, R. (2006). Invertebrate intracellular fatty acid binding proteins. Comparative Biochemistry and Physiology. Toxicology & Pharmacology 142, 262–274. doi: 10.1016/j.cbpc.2005.11.006.CrossRefGoogle ScholarPubMed
Esteves, A., Joseph, L., Paulino, M. and Ehrlich, R. (1997). Remarks on the phylogeny and structure of fatty acid binding proteins from parasitic platyhelminths. International Journal for Parasitology 27, 1013–1023. doi: 10.1016/S0020-7519(97)00071-4.Google Scholar
Esteves, A., Portillo, V. and Ehrlich, R. (2003). Genomic structure and expression of a gene coding for a new fatty acid binding protein from Echinococcus granulosus. Biochimica et Biophysica Acta 1631, 26–34.CrossRefGoogle ScholarPubMed
Gobert, G. N., Stenzel, D. J., Jones, M. K. and McManus, D. P. (1997). Immunolocalization of the fatty acid-binding protein Sj-FABPc within adult Schistosoma japonicum. Parasitology 115, 33–39. doi: 10.1017/S0031182097008925.CrossRefGoogle ScholarPubMed
Grams, R., Adisakwattana, P., Ritthisunthorn, N., Eursitthichai, V., Vichasri-Grams, S. and Viyanant, V. (2006). The saposin-like proteins 1, 2, and 3 of Fasciola gigantica. Molecular and Biochemical Parasitology 148, 133–143. doi: 10.1016/j.molbiopara.2006.03.007.Google Scholar
Grams, R., Vichasri-Grams, S., Sobhon, P., Upatham, S. and Viyanant, V. (2000). Molecular cloning and characterization of antigen encoding genes from Fasciola gigantica. In Proceedings of the 2nd Congress of the Federation of Immunological Societies of Asia-Oceania (ed. Sirisinha, , Chaiyaroj, S., Tapchaisri, S. C., , P.), pp. 39–43. Monduzzi Editore, Bologna, Italy.Google Scholar
Haunerland, N. H. and Spener, F. (2004). Fatty acid-binding proteins – insights from genetic manipulations. Progress in Lipid Research 43, 328–349. doi: 10.1016/j.plipres.2004.05.001.Google Scholar
Hillyer, G. V. (1985). Induction of immunity in mice to Fasciola hepatica with a Fasciola/Schistosoma cross-reactive defined immunity antigen. American Journal of Tropical Medicine and Hygiene 34, 1127–1131.CrossRefGoogle ScholarPubMed
Hillyer, G. V. (1995). Comparison of purified 12 kDa and recombinant 15 kDa Fasciola hepatica antigens related to a Schistosoma mansoni fatty acid binding protein. Memorias do Instituto Oswaldo Cruz 90, 249–253.Google Scholar
Hillyer, G. V. and Soler de Galanes, M. (1988). Identification of a 17-kilodalton Fasciola hepatica immunodiagnostic antigen by the enzyme-linked immunoelectrotransfer blot technique. Journal of Clinical Microbiology 26, 2048–2053.CrossRefGoogle ScholarPubMed
Klebe, R. J., Harriss, J. V., Sharp, Z. D. and Douglas, M. G. (1983). A general method for polyethylene-glycol-induced genetic transformation of bacteria and yeast. Gene 25, 333–341. doi: 10.1016/0378-1119(83)90238-X.Google Scholar
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948. doi: 10.1093/bioinformatics/btm404.Google Scholar
Law, R. H., Smooker, P. M., Irving, J. A., Piedrafita, D., Ponting, R., Kennedy, N. J., Whisstock, J. C., Pike, R. N. and Spithill, T. W. (2003). Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection. Infection and Immunity 71, 6921–6932. doi: 10.1128/IAI.71.12.6921-6932.2003.Google Scholar
Lee, J. S. and Yong, T. S. (2004). Expression and cross-species reactivity of fatty acid-binding protein of Clonorchis sinensis. Parasitology Research 93, 339–343. doi: 10.1007/s00436-004-1139-z.CrossRefGoogle ScholarPubMed
Meyer, F., Meyer, H. and Bueding, E. (1970). Lipid metabolism in the parasitic and free-living flatworms, Schistosoma mansoni and Dugesia dorotocephala. Biochimica et Biophysica Acta 210, 257–266. doi: 10.1016/0005-2760(70)90170-0.Google Scholar
Morphew, R. M., Wright, H. A., Lacourse, E. J., Woods, D. J. and Brophy, P. M. (2007). Comparative proteomics of excretory-secretory proteins released by the liver fluke Fasciola hepatica in sheep host bile and during in vitro culture ex host. Molecular & Cellular Proteomics:MCP 6, 963–972. doi: 10·1074/mcp.M600375-MCP200.CrossRefGoogle ScholarPubMed
Moser, D., Tendler, M., Griffiths, G. and Klinkert, M. Q. (1991). A 14-kDa Schistosoma mansoni polypeptide is homologous to a gene family of fatty acid binding proteins. Journal of Biological Chemistry 266, 8447–8454.Google Scholar
Muro, A., Ramajo, V., Lopez, J., Simon, F. and Hillyer, G. V. (1997). Fasciola hepatica: vaccination of rabbits with native and recombinant antigens related to fatty acid binding proteins. Veterinary Parasitology 69, 219–229. doi: 10.1016/S0304-4017(96)01131-4.CrossRefGoogle ScholarPubMed
Pankao, V. (2006). The expression of fatty acid binding proteins (FABPs) in tissues of Fasciola gigantica, their significance and potential applications in immunodiagnosis and vaccine development. Ph. D. thesis, Mahidol University, Bangkok, Thailand.Google Scholar
Pankao, V., Sirisriro, A., Grams, R., Vichasri-Grams, S., Meepool, A., Kangwanrangsan, N., Wanichanon, C., Ardseungneon, P., Viyanant, V., Upatham, E. S. and Sobhon, P. (2006). Classification of the parenchymal cells in Fasciola gigantica based on ultrastructure and their expression of fatty acid binding proteins (FABPs). Veterinary Parasitology 142, 281–292. doi: 10.1016/j.vetpar.2006.07.009.Google Scholar
Raina, O. K., Sriveny, D. and Yadav, S. C. (2004). Humoral immune response against Fasciola gigantica fatty acid binding protein. Veterinary Parasitology 124, 65–72. doi: 10.1016/j.vetpar.2004.04.013.Google Scholar
Ramos, C. R., Figueredo, R. C., Pertinhez, T. A., Vilar, M. M., do Nascimento, A. L., Tendler, M., Raw, I., Spisni, A. and Ho, P. L. (2003). Gene structure and M20 T polymorphism of the Schistosoma mansoni Sm14 fatty acid-binding protein. Molecular, functional, and immunoprotection analysis. Journal of Biological Chemistry 278, 12745–12751.Google Scholar
Rice, P., Longden, I. and Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics 16, 276–277. doi: 10.1016/S0168-9525(00)02024-2.CrossRefGoogle ScholarPubMed
Richieri, G. V., Ogata, R. T., Zimmerman, A. W., Veerkamp, J. H. and Kleinfeld, A. M. (2000). Fatty acid binding proteins from different tissues show distinct patterns of fatty acid interactions. Biochemistry 39, 7197–7204. doi: 10.1021/bi000314z.Google Scholar
Rodriguez-Perez, J., Rodriguez-Medina, J. R., Garcia-Blanco, M. A. and Hillyer, G. V. (1992). Fasciola hepatica: molecular cloning, nucleotide sequence, and expression of a gene encoding a polypeptide homologous to a Schistosoma mansoni fatty acid-binding protein. Experimental Parasitology 74, 400–407. doi: 10.1016/0014-4894(92)90202-L.Google Scholar
Scott, J. C., Kennedy, M. W. and McManus, D. P. (2000). Molecular and immunological characterisation of a polymorphic cytosolic fatty acid binding protein from the human blood fluke of humans, Schistosoma japonicum. Biochimica et Biophysica Acta 1517, 53–62.Google Scholar
Shields, H. M., Bates, M. L., Bass, N. M., Best, C. J., Alpers, D. H. and Ockner, R. K. (1986). Light microscopic immunocytochemical localization of hepatic and intestinal types of fatty acid-binding proteins in rat small intestine. Journal of Lipid Research 27, 549–557.Google Scholar
Smooker, P. M., Hickford, D. E., Vaiano, S. A. and Spithill, T. W. (1997). Isolation, cloning, and expression of fatty-acid binding proteins from Fasciola gigantica. Experimental Parasitology 85, 86–91. doi: 10.1006/expr.1996.4098.Google Scholar
Storch, J. and Corsico, B. (2008). The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annual Review of Nutrition 28, 73–95. doi: 10.1146/annurev.nutr.27.061406.093710.Google Scholar
Storch, J. and McDermott, L. (2009). Structural and functional analysis of fatty acid-binding proteins. Journal of Lipid Research 50 (Suppl.), S126–31. doi: 10.1194/jlr.R800084-JLR200.Google Scholar
Tendler, M., Brito, C. A., Vilar, M. M., Serra-Freire, N., Diogo, C. M., Almeida, M. S., Delbem, A. C., Da Silva, J. F., Savino, W., Garratt, R. C., Katz, N. and Simpson, A. S. (1996). A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proceedings of the National Academy of Sciences, USA 93, 269–273. doi: 10.1073/pnas.93.1.269.CrossRefGoogle ScholarPubMed
Tendler, M. and Simpson, A. J. (2008). The biotechnology-value chain: development of Sm14 as a schistosomiasis vaccine. Acta Tropica 108, 263–266. doi: 10.1016/j.actatropica.2008.09.002.CrossRefGoogle ScholarPubMed
Tendler, M., Vilar, M. M., Brito, C. A., Freire, N. M., Katz, N. and Simpson, A. (1995). Vaccination against schistosomiasis and fascioliasis with the new recombinant antigen Sm14: potential basis of a multi-valent anti-helminth vaccine? Memorias do Instituto Oswaldo Cruz 90, 255–256. doi: 10.1590/S0074-02761995000200022.Google Scholar
Zimmerman, A. W. and Veerkamp, J. H. (2002). New insights into the structure and function of fatty acid-binding proteins. Cellular and Molecular Life Sciences 59, 1096–1116.CrossRefGoogle ScholarPubMed