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

Published online by Cambridge University Press:  02 September 2009

S. Smitha ,
O.K. Raina ,
B.P. Singh ,
S. Samanta ,
R. Velusamy ,
S. Dangoudoubiyam ,
A. Tripathi ,
P.K. Gupta ,
Bhaskar Sharma  and
Meeta Saxena
S. Smitha
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
O.K. Raina*
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
B.P. Singh
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
S. Samanta
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
R. Velusamy
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
S. Dangoudoubiyam
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
A. Tripathi
Affiliation:
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP, India
P.K. Gupta
Affiliation:
Division of Animal Biotechnology, IVRI, Izatnagar, UP, India
Bhaskar Sharma
Affiliation:
Division of Animal Biochemistry, IVRI, Izatnagar, UP, India
Meeta Saxena
Affiliation:
Division of Animal Biochemistry, IVRI, Izatnagar, UP, India
*
*E-mail: [email protected]
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Abstract

Fasciola gigantica fatty acid binding protein (FABP) was evaluated for evoking an immune response in mice, by delivering the gene coding for this protein with mannosylated-polyethylenimine (PEI) to peritoneal cells. Mice were immunized with 50 μg recombinant plasmid DNA (Group I) or DNA-PEI-mannose (a 22 kDa linear cationic polymer with mannose ligand) (Group II) via the intraperitoneal route. Antibody studies showed no significant humoral immune response evoked to this DNA immunization with either PEI-mannose-delivered or naked DNA. However, on protein boosting of these DNA-primed mice there was a significant enhancement of antibody titre. Flow cytometric bead array was used to measure quantitites of interleukin (IL)-2, IL-4, IL-5, interferon-γ (IFN-γ) and tumour necrosis factor (TNF) cytokines. Overexpression of T-helper 1 (Th1) cytokines such as IFN-γ and TNF, with a lower but significant expression of the T-helper 2 (Th2) cytokine IL-5 was detected. Gene delivery using polyethylenimine-mannose ligand showed significant expression of IFN-γ and TNF (P < 0.05), but no significant difference in IL-2, IL-4 and IL-5 (P>0.05) cytokine expression was observed between naked-DNA- and mannosylated PEI-DNA-delivered mice. Naked- or PEI-delivered-DNA immunization produced insignificant levels of IL-2 and IL-4 (P>0.05) cytokines in both groups of mice.

Type
Research Papers
Information
Journal of Helminthology , Volume 84 , Issue 2 , June 2010 , pp. 149 - 155
Copyright
Copyright © Cambridge University Press 2009

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References

Akinc, A., Thomas, M., Klibanov, A.M. & Langer, R. (2005) Exploring poly-ethylenimine mediated DNA transfection and the proton sponge hypothesis. Journal of Gene Medicine 7, 657–663.CrossRefGoogle Scholar
Bonnet, M.E., Erbacher, P. & Bolcato-Bellemin, A.L. (2008) Systemic delivery of DNA or siRNA mediated by linear polyethylenimine (L-PEI) does not induce an inflammatory response. Pharmacology Research 25, 2972–2982.CrossRefGoogle Scholar
Boussif, O., Lezoualch, 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
Brady, M.T., O'Neill, S.M., Dalton, J.P. & Mills, K.H.G. (1999) Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infection and Immunity 67, 5372–5378.CrossRefGoogle ScholarPubMed
Clery, D.G., Torgerson, P. & Mulcahy, G. (1996) Immune responses of chronically infected adult cattle to Fasciola hepatica. Veterinary Parasitology 62, 71–82.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 Sj 22.7 antigen. Acta Biochimica et Biophysica Sinica (Shanghai) 39, 27–36.CrossRefGoogle Scholar
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
Else, K.J., Finkelman, F.D. & Grencis, R.K. (1994) Cytokine-mediated regulation of chronic intestinal helminth infection. Journal of Experimental Medicine 179, 347–351.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
Hattori, Y., Kawakami, S., Nakamura, K., Yamashita, F. & Hashida, M. (2006) Efficient gene transfer into macrophages and dendritic cells by in vivo gene delivery with mannosylated lipoplex via the intraperitoneal route. Journal of Pharmacology and Experimental Therapy 318, 828–834.CrossRefGoogle ScholarPubMed
Kawakami, S., Ito, Y., Charoensit, P., Yamashita, F. & Hashida, M. (2006) Evaluation of proinflammatory cytokine production induced by linear and branched polyethylenimine/plasmid DNA complexes in mice. Journal of Pharmacology and Experimental Therapy 317, 1382–1390.CrossRefGoogle ScholarPubMed
Kawakami, S., Higuchi, Y. & Hashida, M. (2008) Nonviral approaches for targeted delivery of plasmid DNA and oligonucleotide. Journal of Pharmacological Science 97, 726–745.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
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
Lisziewicz, J., Trocio, J., Whitman, L., Varga, G., Xu, J., Bakare, N., Erbacher, P., Fox, C., Woodward, R., Markham, P., Arya, S., Behr, J.P. & Lori, F. (2005) Derma vir: a novel topical vaccine for HIV/AIDS. Journal of Investigative Dermatology 124, 160–169.CrossRefGoogle Scholar
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
Moghadami, M. & Mardani, M. (2008) Fasciola hepatica: a cause of obstructive jaundice in an elderly man from Iran. Saudi Journal of Gastroenterology 14, 208–210.CrossRefGoogle Scholar
Molina, E.C. (2005) Serum interferon gamma and interleukins-6 and -8 during infection with Fasciola gigantica in cattle and buffaloes. Journal of Veterinary Science 6, 135–139.CrossRefGoogle ScholarPubMed
Moreau, E., Chauvin, A. & Boulard, C. (1998) IFN γ and IL 10 production by hepatic lymph node and peripheral blood lymphocytes in Fasciola hepatica infected sheep. Parasite 5, 307–315.CrossRefGoogle ScholarPubMed
Morrison, C.A., Colin, T., 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 2, 2837–2843.CrossRefGoogle Scholar
O'Neill, S.M., Brady, M.T., Callanan, J.J., Mulcahy, G., Joyce, P., Mills, K.H.G. & Dalton, J.P. (2000) Fasciola hepatica infection down regulates Th1 response in mice. Parasite Immunology 22, 147–155.CrossRefGoogle ScholarPubMed
Pankao, V., Sirisriro, A., Grams, R., Vichasri-Grams, S., Meepool, A., Kangwanrangsan, N., Wanichanon, C., Ardseungneon, P., Viyanant, V., Upatham, E.S. & Sobhon, P. (2006) Classification of the parenchymal cells in Fasciola gigantica based on ultra structure and their expression of fatty acid binding proteins (FABPs). Veterinary Parasitology 142, 281–292.CrossRefGoogle Scholar
Raina, O.K., Tripathy, A., Sriveny, D., Gupta, P.K., Samanta, S., Gupta, S.C., Singh, R., Tewari, A.K., Banerjee, P.S., Sanjay Kumar, & Yadav, S.C. (2009) Immune responses to polyethylenimine delivered plasmid DNA encoding a Fasciola gigantica fatty acid binding protein in mice and rabbits. Journal of Helminthology 83, 275–283.CrossRefGoogle Scholar
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. (2002) Laboratory and field evaluation of Schistosoma japonicum DNA vaccines in sheep and water buffalo in China. Vaccine 20, 462–467.CrossRefGoogle Scholar
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
Spithill, T.W., Smooker, P.M. & Copeman, D.B. (1999) Fasciola gigantica: epidemiology, control, immunology and molecular biology. Wallingford, UK, 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
Waine, G.J., Yang, W., Scott, J.C., McManus, D.P. & Kalinna, B.H. (1997) DNA-based vaccination using Schistosoma japonicum (Asian blood fluke) genes. Vaccine 15, 846–848.CrossRefGoogle ScholarPubMed
Waldvogel, A.S., Lepage, M.F., Zakher, A., Reichel, M.P., Eicher, R. & Heussler, V.T. (2004) Expression of interleukin-4, interleukin-4 splice variants and interferon-gamma mRNA in calves experimentally infected with Fasciola hepatica. Veterinary Immunology and Immunopathology 97, 53–63.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 behaviour 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
Wiseman, J.W., Goddard, C.A., McLelland, D. & Colledge, W.H. (2003) A comparison of linear and branched polyethylenimine (PEI) with DCChol/DOPE liposomes for gene delivery to epithelial cells in vitro and in vivo. Gene Therapy 10, 1654–1662.CrossRefGoogle ScholarPubMed
Zhang, Y., Taylor, M.G., Johansen, M.V. & Bickle, Q.D. (2002) Vaccination of mice with a cocktail DNA vaccine induces a Th1-type immune response and partial protection against Schistosoma japonicum infection. Vaccine 20, 724–730.CrossRefGoogle Scholar
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