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Immune responses to polyethylenimine delivered plasmid DNA encoding a Fasciola gigantica fatty acid binding protein in mice and rabbits

Published online by Cambridge University Press:  01 September 2009

O.K. Raina ,
A. Tripathy ,
D. Sriveny ,
P.K. Gupta ,
S. Samanta ,
S.C. Gupta ,
R. Singh ,
A.K. Tewari ,
P.S. Banerjee  and
S. Kumar
...Show all authors
O.K. Raina*
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
A. Tripathy
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
D. Sriveny
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
P.K. Gupta
Affiliation:
Division of Animal Biotechnology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
S. Samanta
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
S.C. Gupta
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
R. Singh
Affiliation:
Centre for Animal Diseases Research and Diagnosis, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
A.K. Tewari
Affiliation:
Division of Animal Biotechnology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
P.S. Banerjee
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
S. Kumar
Affiliation:
Agricultural Research Information System, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
S.C. Yadav
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, India
*
*E-mail: rainaok@rediffmail.com
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Abstract

Fasciola gigantica fatty acid binding protein (FABP) was evaluated for evoking an effective immune response in mice and rabbits, when delivered as a DNA vaccine in muscle cells. Polyethylenimine (PEI), 25 kDa, branched cationic polymer was used as a delivery vehicle for this DNA in the muscle cells of mice and rabbits. Naked DNA evoked mixed Th1 and Th2 responses in mice. PEI condensed DNA, at amine nitrogen over DNA phosphate (N/P) ratios of 4, 6 and 8 and with various DNA concentrations, failed to evoke a significantly higher antibody response compared to naked DNA in mice. Similarly, the humoral immune response to naked DNA administration in rabbit thigh muscles was poor and no boosting of this antibody response on administration of DNA complexed to PEI was observed. On metacercarial challenge, rabbits failed to show any significant protective immune response in both the naked DNA and PEI–DNA immunized groups. Administration of PEI alone (12.5 μg) in mouse thigh muscles caused significant muscle cytotoxicity but condensation of DNA with PEI had less of a toxic effect on muscle cells, which was inversely related to the N/P ratio. Delivery of plasmid DNA encoding F. gigantica FABP by high molecular weight polyethylenimine (branched, 25 kDa) did not boost the effective immune response in both the animal species, which could either be attributed to cytotoxicity associated with this cationic polymer or muscle cells being unsuitable target cells for PEI condensed DNA delivery.

Type
Research Papers
Information
Journal of Helminthology , Volume 83 , Issue 3 , September 2009 , pp. 275 - 283
Copyright
Copyright © Cambridge University Press 2008

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References

Anderson, D.G., Peng, W., Akinc, A., Hossain, N., Kohn, A., Padera, R., Langer, R. & Sawicki, J.A. (2004) A polymer library approach to suicide gene therapy for cancer. Proceedings of the National Academy of Sciences, USA 101, 16028–16033.CrossRefGoogle ScholarPubMed
Boussif, O., Lezoualc'h, F., Zanta, M.A., Mergny, M.D., Scherman, D., Demeneix, B. & Behr, J.P. (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proceedings of the National Academy of Sciences, USA 92, 7297–7301.CrossRefGoogle ScholarPubMed
Chang, C.W., Choi, D., Kim, W.J., Yockman, J.W., Christensen, L.V., Kim, Y.H. & Kim, S.W. (2007) Non-ionic amphiphilic biodegradable PEG-PLGA-PEG copolymer enhances gene delivery efficiency in rat skeletal muscle. Journal of Controlled Release 118, 245–253.CrossRefGoogle ScholarPubMed
Chollet, P., Favrot, M.C., Hurbin, A. & Coll, J.L. (2002) Side-effects of a systemic injection of linear polyethylenimine–DNA complexes. Journal of Gene Medicine 4, 84–91.CrossRefGoogle ScholarPubMed
Dai, G., Wang, S., Yu, J., Xu, S., Peng, X., He, Z., Liu, X., Zhou, S. & Liu, F. (2007) Vaccination against Schistosoma japonicum infection by DNA vaccine encoding Sj22.7 antigen. Acta Biochimica Biophysica Sinica 39, 27–36.CrossRefGoogle ScholarPubMed
Dalton, J.P., McGonigle, S., Rolph, T.P. & Andrews, S.J. (1996) Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinases and with hemoglobin. Infection and Immunity 64, 5066–5074.CrossRefGoogle ScholarPubMed
Espino, A.M., Osuna, A., Gil, R. & Hillyer, G. (2005) Fasciola hepatica: humoral and cytokine responses to a member of the saposin-like protein family following delivery as a DNA vaccine in mice. Experimental Parasitology 110, 374–383.CrossRefGoogle ScholarPubMed
Estuningsih, S.E., Smooker, P.M., Wiedosari, E., Widjajanti, S., Vaiano, S., Partoutomo, S. & Spithill, T.W. (1997) Evaluation of antigens of Fasciola gigantica as vaccines against tropical fasciolosis in cattle. International Journal for Parasitology 27, 1419–1428.CrossRefGoogle ScholarPubMed
Garzon, M.R., Berraondo, P., Crettaz, J., Ochoa, L., Vera, M., Lasarte, J.J., Vales, A., Van Rooijen, N., Ruiz, J., Prieto, J., Zulueta, J. & Gonzalez-Aseguinolaza, G. (2005) Induction of gp120-specific protective immune responses by genetic vaccination with linear polyethylenimine-plasmid complex. Vaccine 23, 1384–1392.CrossRefGoogle ScholarPubMed
Kang, S.W., Lim, H.W., Seo, S.W., Jeon, O., Lee, M. & Kim, B.S. (2008) Nanosphere mediated delivery of vascular endothelial growth factor gene for therapeutic angiogenesis in mouse ischemic limbs. Biomaterials 29, 1109–1117.CrossRefGoogle ScholarPubMed
Kennedy, N.J., Spithill, T.W., Tennent, J., Wood, P.R. & Piedrafita, D. (2006) DNA vaccines in sheep: CTLA-4 mediated targeting and CpG motifs enhance immunogenicity in a DNA prime/protein boost strategy. Vaccine 24, 970–979.CrossRefGoogle Scholar
Keyyu, J.D., Kassuku, A.A., Msalilwa, L.P., Monrad, J. & Kyvsgaard, N.C. (2006) Cross-sectional prevalence of helminth infections in cattle on traditional, small-scale and large-scale dairy farms in Iringa district, Tanzania. Veterinary Research Communication 30, 45–55.CrossRefGoogle ScholarPubMed
Kofta, W., Mieszczanek, J., Plucienniczak, G. & Wedrychowicz, H. (2000) Successful DNA immunisation of rats against fasciolosis. Vaccine 18, 2985–2990.CrossRefGoogle ScholarPubMed
Kunath, K., Harpe, A.V., Fischer, D., Petersen, H., Bickel, U., Voigt, K. & Kissel, T. (2003) Low-molecular-weight polyethylenimine as a non-viral vector for DNA delivery: comparison of physicochemical properties, transfection efficiency and in vivo distribution with high-molecular-weight polyethylenimine. Journal of Control Release 89, 113–125.CrossRefGoogle ScholarPubMed
Lee, J.S., Kim, I.S., Sohn, W.M., Lee, J. & Yong, T.S. (2006) A DNA vaccine encoding a fatty acid-binding protein of Clonorchis sinensis induces protective immune response in Sprague–Dawley rats. Scandanavian Journal of Immunology 63, 169–176.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Bargues, M.D. & Valero, M.A. (2005) Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 1255–1278.CrossRefGoogle ScholarPubMed
Meyer, F., Meyer, H. & Bueding, E. (1970) Lipid metabolism in the parasitic and free-living flatworms, Schistosoma mansoni and Dugesia dorotocephala. Biochimica et Biophysica Acta 210, 257–266.CrossRefGoogle ScholarPubMed
Morrison, C.A., Colin, F., Sexton, J.L., Bowen, F., Wicker, J., Friedel, T. & Spithill, T.W. (1996) Protection of cattle against Fasciola hepatica infection by vaccination with glutathione-S-transferase. Vaccine 14, 1603–1612.CrossRefGoogle ScholarPubMed
Nambi, P.A., Yadav, S.C., Raina, O.K., Sriveny, D. & Saini, M. (2005) Vaccination of buffaloes with Fasciola gigantica recombinant fatty acid binding protein. Parasitology Research 97, 129–135.CrossRefGoogle ScholarPubMed
Ockner, R.K. (1990) Historic overview of the studies on fatty acid binding proteins. Molecular and Cellular Biochemistry 98, 3–9.CrossRefGoogle ScholarPubMed
Oh, Y.K., Kim, J.P., Yoon, H., Kim, J.M., Yang, J.S. & Kim, C.K. (2001) Prolonged organ retention and safety of plasmid DNA administered in polyethylenimine complexes. Gene Therapy 8, 1587–1592.CrossRefGoogle ScholarPubMed
Oh, Y.K., Park, J.S., Kang, M.J., Ko, J.J., Kim, J.M. & Kim, C.K. (2003) Enhanced adjuvanticity of interleukin-2 plasmid DNA administered in polyethylenimine complexes. Vaccine 21, 2837–2843.CrossRefGoogle ScholarPubMed
Ramajo, V., Oleaga, A., Casanueva, P., Hillyer, G.V. & Muro, A. (2001) Vaccination of sheep against Fasciola hepatica with homologous fatty acid binding proteins. Veterinary Parasitology 97, 35–46.CrossRefGoogle ScholarPubMed
Sanyal, P.K. (2001) Control of tropical fasciolosis in cattle and buffaloes in India at the backdrop of its integrated management. Journal of Veterinary Parasitology 15, 13–16.Google Scholar
Sharma, R.L., Dhar, D.N. & Raina, O.K. (1989) Studies on the prevalence and laboratory transmission of fascioliasis in animals in the Kashmir Valley. British Veterinary Journal 145, 57–61.CrossRefGoogle ScholarPubMed
Shi, F., Zhang, Y., Ye, P., Lin, J., Cai, Y., Shen, W., Bickle, Q.D. & Taylor, M.G. (2001) Laboratory and field evaluation of Schistosoma japonicum DNA vaccines in sheep and water buffalo in China. Vaccine 20, 462–467.CrossRefGoogle ScholarPubMed
Smooker, P.M., Steeper, K.R., Drew, D.R., Strugnell, R.A. & Spithill, T.W. (1999) Humoral responses in mice following vaccination with DNA encoding glutathione S-transferase of Fasciola hepatica: effects of mode of vaccination and the cellular compartment of antigen expression. Parasite Immunology 21, 357–364.CrossRefGoogle ScholarPubMed
Smooker, P.M., Kennedy, N.J., Steeper, K.R., Christopoulos, H. & Spithill, T.W. (2001) Fasciola: kinetics and quality of humoral responses to fatty acid binding protein and cathepsin L following delivery as DNA vaccines in mice. Experimental Parasitology 97, 154–160.CrossRefGoogle ScholarPubMed
Smooker, P.M., Rainczuk, A., Kennedy, N. & Spithill, T.W. (2004) DNA vaccines and their application against parasites – promise, limitations and potential solutions. Biotechnological Annual Reviews 10, 189–236.CrossRefGoogle ScholarPubMed
Spithill, T.W., Smooker, P.M. & Copeman, D.B. (1999) Fasciola gigantica: epidemiology, control, immunology and molecular biology. Wallingford, CAB International.Google Scholar
Tang, L., Zhou, Z., Chen, Y., Luo, Y., Wang, L., Chen, L., Huang, F., Zeng, X. & Yi, X. (2007) Vaccination of goats with 31 kDa and 32 kDa Schistosoma japonicum antigens by DNA priming and protein boosting. Cell and Molecular Immunology 4, 153–156.Google ScholarPubMed
Tendler, M., Brito, C.A., Vilar, M., Serra-Freire, N., Diogo, C.M., Almeida, M.S., Delbem, A.C., Silva, J.F.D., Savino, W., Garratt, R.C., Katz, N. & 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.CrossRefGoogle ScholarPubMed
Wang, J., Zhang, P.C., Mao, H.-Q. & Leong, K.W. (2002) Enhanced gene expression in mouse muscle by sustained release of plasmid DNA using PPE-EA as a carrier. Gene Therapy 9, 1254–1261.CrossRefGoogle ScholarPubMed
Wedrychowicz, H., Lamparska, M., Kesik, M., Kotomski, G., Mieszczanek, J., Jedlina-Panasiuk, L. & 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.CrossRefGoogle ScholarPubMed
Wightman, L., Kircheis, R., Rossler, V., Carotta, S., Ruzicka, R., Kursa, M. & Wagner, E. (2001) Different behavior of branched and linear polyethylenimine for gene delivery in vitro and in vivo. Journal of Gene Medicine 3, 362–372.CrossRefGoogle ScholarPubMed
Wijffels, G.L., Salvatore, L., Dosen, M., Waddington, J., Wilson, L., Thompson, C., Campbell, N., Sexton, J., Wicker, J., Bowen, F., Friedel, T. & Spithill, T.W. (1994) Vaccination of sheep with purified cysteine proteinases of Fasciola hepatica decreases worm fecundity. Experimental Parasitology 78, 132–148.CrossRefGoogle ScholarPubMed
Zhou, X., Liu, B., Yu, X., Zha, X., Zhang, X., Chen, Y., Wang, X., Jin, Y., Wu, Y., Chen, Y., Shan, Y., Chen, Y., Liu, J., Kong, W. & Shen, J. (2007) Controlled release of PEI/DNA complexes from mannose bearing chitosan microspheres as a potent delivery system to enhance immune response to HBV DNA vaccine. Journal of Controlled Release 121, 200–207.CrossRefGoogle ScholarPubMed
Zhu, Y., Ren, J., Da'dara, A., Harn, D., Xu, M., Si, J., Yu, C., Liang, Y., Ye, P., Yin, X., He, W., Xu, Y., Cao, G. & Hua, W. (2004) The protective effect of a Schistosoma japonicum Chinese strain 23 kDa plasmid DNA vaccine in pigs is enhanced with IL-12. Vaccine 23, 78–83.CrossRefGoogle ScholarPubMed