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Immunodiagnostic monoclonal antibody-based sandwich ELISA of fasciolosis by detection of Fasciola gigantica circulating fatty acid binding protein

Published online by Cambridge University Press:  17 June 2016

PANAT ANURACPREEDA*
Affiliation:
Division of Agricultural Science, Mahidol University, Kanchanaburi Campus, Saiyok, Kanchanaburi 71150, Thailand Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok 10400, Thailand
RUNGLAWAN CHAWENGKIRTTIKUL
Affiliation:
Department of Microbiology, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok 10400, Thailand
PRASERT SOBHON
Affiliation:
Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Rd., Bangkok 10400, Thailand
*
*Corresponding author: Division of Agricultural Science, Mahidol University, Kanchanaburi Campus, Saiyok, Kanchanaburi 71150, Thailand. Tel. +66 3458 5060. Fax. +66 3458 5077. E-mail: Panat1@yahoo.com; panat.anu@mahidol.ac.th

Summary

Up to now, parasitological diagnosis of fasciolosis is often unreliable and possesses low sensitivity. Hence, the detection of circulating parasite antigens is thought to be a better alternative for diagnosis of fasciolosis, as it reflects the real parasite burden. In the present study, a monoclonal antibody (MoAb) against recombinant Fasciola gigantica fatty acid binding protein (rFgFABP) has been produced. As well, a reliable sandwich enzyme-linked immunosorbent assay (sandwich ELISA) has been developed for the detection of circulating FABP in the sera of mice experimentally and cattle naturally infected with F. gigantica. MoAb 3A3 and biotinylated rabbit anti-recombinant FABP antibody were selected due to their high reactivities and specificities. The lower detection limit of sandwich ELISA was 5 pg mL−1, and no cross-reaction with other parasite antigens was observed. This assay could detect F. gigantica infection from day 1 post infection. In experimental mice, the sensitivity, specificity and accuracy of this assay were 93·3, 100 and 98·2%, while in natural cattle they were 96·7, 100 and 99·1%. Hence, this sandwich ELISA method showed high efficiencies and precisions for diagnosis of fasciolosis by F. gigantica.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Anuracpreeda, P., Wanichanon, C., Chaithirayanon, K., Preyavichyapugdee, N. and Sobhon, P. (2006). Distribution of 28·5 kDa antigen in tegument of adult Fasciola gigantica . Acta Tropica 100, 3140.Google Scholar
Anuracpreeda, P., Wanichanon, C. and Sobhon, P. (2008). Paramphistomum cervi: antigenic profile of adults as recognized by infected cattle sera. Experimental Parasitology 118, 203207.Google Scholar
Anuracpreeda, P., Wanichanon, C., Chawengkirtikul, R., Chaithirayanon, K. and Sobhon, P. (2009 a). Fasciola gigantica: immunodiagnosis of fasciolosis by detection of circulating 28·5 kDa tegumental antigen. Experimental Parasitology 123, 334340.CrossRefGoogle ScholarPubMed
Anuracpreeda, P., Wanichanon, C. and Sobhon, P. (2009 b). Fasciola gigantica: immunolocalization of 28·5 kDa antigen in the tegument of metacercaria and juvenile fluke. Experimental Parasitology 122, 7583.CrossRefGoogle ScholarPubMed
Anuracpreeda, P., Songkoomkrong, S., Sethadavit, M., Chotwiwatthanakun, C., Tinikul, Y. and Sobhon, P. (2011). Fasciola gigantica: production and characterization of a monoclonal antibody against recombinant cathepsin B3. Experimental Parasitology 127, 340345.Google Scholar
Anuracpreeda, P., Panyarachun, B., Ngamniyom, A., Tinikul, Y., Chotwiwatthanakun, C., Poljaroen, J. and Sobhon, P. (2012). Fischoederius cobboldi: a scanning electronmicroscopy investigation of surface morphology of adult rumen fluke. Experimental Parasitology 130, 400407.CrossRefGoogle Scholar
Anuracpreeda, P., Chawengkirtikul, R., Tinikul, Y., Poljaroen, J., Chotwiwatthanakun, C. and Sobhon, P. (2013 a). Diagnosis of Fasciola gigantica infection using a monoclonal antibody-based sandwich ELISA for detection of circulating cathepsin B3 protease. Acta Tropica 127, 3845.Google Scholar
Anuracpreeda, P., Poljaroen, J., Chotwiwatthanakun, C., Tinikul, Y. and Sobhon, P. (2013 b). Antigenic components, isolation and partial characterization of excretion-secretion fraction of Paramphistomum cervi . Experimental Parasitology 133, 327333.CrossRefGoogle ScholarPubMed
Anuracpreeda, P., Srirakam, T., Pandonlan, S., Changklungmoa, N., Chotwiwatthanakun, C., Tinikul, Y., Poljaroen, J., Meemon, K. and Sobhon, P. (2014). Production and characterization of a monoclonal antibody against recombinant cathepsin L1 of Fasciola gigantica . Acta Tropica 135, 19.Google Scholar
Anuracpreeda, P., Phutong, S., Ngamniyom, A., Panyarachun, B. and Sobhon, P. (2015). Surface topography and ultrastructural architecture of the tegument of adult Carmyerius spatiosus Brandes, 1898. Acta Tropica 143, 1828.Google Scholar
Anuracpreeda, P., Chawengkirttikul, R. and Sobhon, P. (2016 a). Antigenic profile, isolation and characterization of whole body extract of Paramphistomum gracile . Parasite Immunology (In Press) doi: 10.1111/pim.12330.Google Scholar
Anuracpreeda, P., Chawengkirttikul, R. and Sobhon, P. (2016 b). Immunodiagnosis of Fasciola gigantica infection using monoclonal antibody-based sandwich ELISA and immunochromatographic assay for detection of circulating cathepsin L1 protease. PLoS ONE 11, 122. e0145650.Google Scholar
Anuracpreeda, P., Chawengkirttikul, R. and Sobhon, P. (2016 c). Surface histology, topography, and ultrastructure of the tegument of adult Orthocoelium parvipapillatum (Stiles & Goldberger, 1910). Parasitology Research (In Press) doi: 10.1007/s00436-016-5024-3.Google Scholar
Anuracpreeda, P., Chankaew, K., Puttarak, P., Koedrith, P., Chawengkirttikul, R., Panyarachun, B., Ngamniyom, A., Chanchai, S. and Sobhon, P. (2016 d). The anthelmintic effects of the ethanol extract of Terminalia catappa L. leaves against the ruminant gut parasite, Fischoederius cobboldi . Parasitology 143, 421433.Google Scholar
Arafa, M. S., Abaza, S. M., El-Shewy, K. A., Mohareb, E. W. and El-Moamly, A. A. (1999). Detection of Fasciola-specific excretory/secretory (E/S) protein fraction band (49·5 kDa) and its utilization in diagnosis of early fascioliasis using different diagnostic techniques. Journal of the Egyptian Society of Parasitology 29, 911926.Google Scholar
Ashrafi, K., Valero, M. A., Panova, M., Periago, M. V., Massoud, J. and Mas-Coma, S. (2006 a). Phenotypic analysis of adults of Fasciola hepatica, Fasciola gigantica and intermediate forms from the endemic region of Gilan. Parasitology International 55, 249260.Google Scholar
Ashrafi, K., Valero, M. A., Massoud, J., Sobhani, A., Solaymani-Mohammadi, S., Conde, P., Khoubbane, M., Bargues, M. D. and Mas-Coma, S. (2006 b). Plant-borne human contamination by fascioliasis. American Society of Tropical Medicine and Hygiene 75, 295302.CrossRefGoogle ScholarPubMed
Chicz, R. M. (1994). Submitted to the Protein Sequence Database, August 1994. Accession No. A44638.Google Scholar
Demerdash, Z. A., Diab, T. M., Aly, I. R., Mohamed, S. H., Mahmoud, F. S., Zoheiry, M. K., Mansour, W. A., Attia, M. E. and El-Bassiouny, A. E. (2011). Diagnostic efficacy of monoclonal antibody based sandwich enzyme linked immunosorbent assay (ELISA) for detection of Fasciola gigantica excretory/secretory antigens in both serum and stool. Parasites and Vectors 4, 176.Google Scholar
Espino, A. and Finlay, C. (1994). Sandwich enzyme-liked immunosorbent assay for detection of excretory/secretory antigens in humans with fascioliasis. Journal of Clinical Microbiology 32, 190193.Google Scholar
Fagbemi, B. O. and Obarisiagbon, I. O. (1990). Comparative evaluation of the enzyme-linked immunosorbent assay (ELISA) in the diagnosis of natural Fasciola gigantica infection in cattle. Veterinary Quarterly 12, 3538.Google Scholar
Fagbemi, B. O., Obarisiagbon, I. O. and Mbuh, J. V. (1995). Detection of circulating antigen in sera of Fasciola gigantica-infected cattle with antibodies reactive with a Fasciola-specific 88-kDa antigen. Veterinary Parasitology 58, 235246.Google Scholar
Fagbemi, B. O., Aderibigbe, O. A. and Guobadia, E. E. (1997). The use of monoclonal antibody for the immunodiagnosis of Fasciola gigantica infection in cattle. Veterinary Parasitology 69, 231240.CrossRefGoogle ScholarPubMed
Galen, R. S. (1980). Predictive value and efficiency of laboratory testing. Pediatric Clinics of North America 27, 861869.CrossRefGoogle ScholarPubMed
Ghosh, S., Rawat, P., Velusamy, R., Joseph, D., Gupta, S. C. and Singh, B. P. (2005). 27 kDa Fasciola gigantica glycoprotein for the diagnosis of prepatent fasciolosis in cattle. Veterinary Research Communications 29, 123135.Google Scholar
Grams, R., Vichasri-Grams, S., Sobhon, P., Upatham, E. S. and Viyanant, V. (2000). Molecular cloning and characterization of antigen encoding genes from Fasciola gigantica . In International Proceedings of the Second Congress of the Federation of Immunological Societies of Asia-Oceania (ed. Sirisinha, S., Chaiyaroj, S. C. and Tapchaisri, P.), pp. 3943. Monduzzi Editore, Bangkok, Thailand, January 23–27. Bologna, Italy.Google Scholar
Guobadia, E. E., and Fagbemi, B. O. (1995). Immunodiagnosis of fasciolosis in ruminants using a 28-kDa cysteine protease of Fasciola gigantica adult worms. Veterinary Parasitology 57, 309318.Google Scholar
Hammond, J. A. and Sewell, M. M. H. (1972). Flotation on the Sellotape (demonstration). Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 547.Google Scholar
Hillyer, G. V. (1999). Immunodiagnosis of human and animal fasciolosis. In Fasciolosis (ed. Dalton, J. P.), pp. 435447. CABI Publishing, Oxon, UK.Google Scholar
Hillyer, G. V., del Llano de Diaz, A. and Reyes, C. N. (1977). Schistosoma mansoni: acquired immunity in mice and hamsters using antigens of Fasciola hepatica . Experimental Parasitology 42, 348355.Google Scholar
Kumar, N., Ghosh, S. and Gupta, S. C. (2008). Early detection of Fasciola gigantica infection in buffaloes by enzyme-linked immunosorbent assay and dot enzyme-linked immunosorbent assay. Parasitology Research 103, 141150.Google Scholar
Langley, R. J. and Hillyer, G. V. (1989). Detection of circulating parasite antigen in murine fascioliasis by two-site enzyme-linked immunosorbent assays. American Journal of Tropical Medicine and Hygiene 41, 472478.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685.Google Scholar
Le, T. H., De, N. V., Agatsuma, T., Blair, D., Vercruysse, J., Dorny, P., Nguyen, T. G. and McManus, D. P. (2007). Molecular confirmation that Fasciola gigantica can undertake aberrant migrations in human hosts. Journal of Clinical Microbiology 45, 648650.Google Scholar
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randal, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Chemical Biology 193, 265275.Google Scholar
Mas-Coma, S., Bargues, M. D. and Valero, M. A. (2005). Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 12551278.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2009). Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41146.Google Scholar
Mbuh, J. V. and Fagbemi, B. O. (1996). Antibody and circulating antigen profiles before and after chemotherapy in goats infected with Fasciola gigantica . Veterinary Parasitology 66, 171179.Google Scholar
Meyer, F., Myer, H., and Bueding, E. (1970). Lipid metabolism in the parasitic and free-living flatworms, Schistosoma mansoni and Dugesia dorotocephala . Biochimica et Biophysica Acta. 210, 257266.CrossRefGoogle ScholarPubMed
Mezo, M., Gonzalez-Warleta, M. and Ubeira, F. M. (2004). An ultrasensitive capture ELISA for detection of Fasciola hepatica coproantigens in sheep and cattle using a new monoclonal antibody (MM3). Journal of Parasitology 90, 845852.Google Scholar
Panyarachun, B., Sobhon, P., Yotsawan, T., Chotwiwatthanakun, C., Anupunpisit, V. and Anuracpreeda, P. (2010). Paramphistomum cervi: surface topography of the tegument of adult fluke. Experimental Parasitology 125, 9599.Google Scholar
Panyarachun, B., Ngamniyom, A., Sobhon, P. and Anuracpreeda, P. (2013). Morphologyand histology of the adult Paramphistomum gracile Fischoeder, 1901. Journal of Veterinary Science 14, 425432.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, 400407.Google Scholar
Sirisriro, A., Grams, R., Vichasri-Grams, S., Ardseungneon, P., Pankao, V., Meepool, A., Chaithirayanon, K., Viyanant, V., Tan-Ariya, P., Upatham, E. S. and Sobhon, P. (2002). Production and characterization of a monoclonal antibody against recombinant fatty acid binding protein of Fasciola gigantica . Veterinary Parasitology 105, 119129.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, 8991.Google Scholar
Sobhon, P., Anantavara, S., Dangprasert, T., Viyanant, V., Krailas, D., Upatham, E. S., Wanichanon, C., Kusamran, T. (1998). Fasciola gigantica: studies of the tegument as a basis for the developments of immunodiagnosis and vaccine. Southeast Asian Journal of Tropical Medicine and Public Health 29, 387400.Google Scholar
Soulsby, E. J. L. (1965). Textbook of Veterinary Clinical Parasitology. I. Helminths. Blackwell Scientific Publications, Oxford, p. 1120.Google Scholar
Spithill, T. W., Smooker, P. M. and Copeman, D. B. (1999). Fasciola gigantica: epidemiology, control, immunology and molecular biology. In Fasciolosis (ed. Dalton, J. P.), pp. 465525. CABI Publishing, Oxon.Google Scholar
Sriveny, D., Raina, O. K., Yadav, S. C., Chandra, D., Jayraw, A. K., Singh, M., Velusamy, R., and Singh, B. P. (2006). Cathepsin L cysteine proteinase in the diagnosis of bovine Fasciola gigantica infection. Veterinary Parasitology 135, 2531.Google Scholar
Swarup, D., Pachauri, S. P., Sharma, B., and Bandhopadhyay, S. K. (1987). Serodiagnosis of Fasciola gigantica infection in buffaloes. Veterinary Parasitology 24, 6774.Google Scholar
Torgerson, P. and Claxton, J. (1999). Epidemiology and control. In In Fasciolosis (ed. Dalton, J. P.), pp. 113149. CABI Publishing, Oxon.Google Scholar
Towbin, H., Staehelin, T. and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheet: procedure and some applications. Proceedings of the National Academy of Sciences of the United States of America 76, 43504354.Google Scholar
Velusamy, R., Singh, B. P., Sharma, R. L. and Chanda, D. (2004). Detection of circulating 54 kDa antigen in sera of bovine calves experimentally infected with F. gigantica . Veterinary Parasitology 119, 187195.Google Scholar
Viyanant, V., Krailas, D., Sobhon, P., Upatham, E. S., Kusamran, T., Chompoochan, T., Thammasart, S. and Prasittirat, P. (1997). Diagnosis of cattle fasciolosis by the detection of a circulating antigen using a monoclonal antibody. Asian Pacific Journal of Allergy and Immunology 15, 153159.Google Scholar
Wongwairot, S., Kueakhai, P., Changklungmoa, N., Jaikua, W., Sansri, V., Meemon, K., Songkoomkrong, S., Riengrojpitak, S. and Sobhon, P. (2015). Monoclonal antibody against recombinant Fasciola gigantica cathepsin L1H could detect juvenile and adult cathepsin Ls of Fasciola gigantica . Parasitology Research 114, 133140.Google Scholar
Zimmerman, G. L., Nelson, M. J. and Clark, C. R. (1985). Diagnosis of ovine fascioliasis by a dot enzyme-linked immunosorbent assay: a rapid microdiagnostic technique. American Journal of Veterinary Research 46, 15131515.Google Scholar
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