Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter March 25, 2015

Antiparasitic DNA vaccines in 21st century

Halina Wedrychowicz
From the journal Acta Parasitologica


Demands for effective vaccines to control parasitic diseases of humans and livestock have been recently exacerbated by the development of resistance of most pathogenic parasites to anti-parasitic drugs. Novel genomic and proteomic technologies have provided opportunities for the discovery and improvement of DNA vaccines which are relatively easy as well as cheap to fabricate and stable at room temperatures. However, their main limitation is rather poor immunogenicity, which makes it necessary to couple the antigens with adjuvant molecules. This paper review recent advances in the development of DNA vaccines to some pathogenic protozoa and helminths. Numerous studies were conducted over the past 14 years of 21st century, employing various administration techniques, adjuvants and new immunogenic antigens to increase efficacy of DNA vaccines. Unfortunately, the results have not been rewarding. Further research is necessary using more extensive combinations of antigens; alternate delivery systems and more efficient adjuvants based on knowledge of the immunomodulatory capacities of parasitic protozoa and helminths.


Ahmad G., Torren W., Zhang W., Wyatt M., Siddiqui A.A. 2009a. Sm-p80-based DNA vaccine formulation induces potent protective immunity against Schistosoma mansoni. Parasite Immunology, 31, 156-161. DOI: 10.1111/j.1365-3024.2008.001091.x Search in Google Scholar

Ahmad G., Zhang W., Torben W., Damian R.T., Chavez-Suarez M., Wolf R.F,. White G.L. 2009b. Protective and antifecundity effects of Sm-p80-based DNA vaccine formulation against Schistosoma mansoni in a nonhuman primate model. Vaccine, 27, 2830-2837. DOI: 10.1016/j.vaccine.2009.02.096Search in Google Scholar

Ahmad G., Zhang W., Torben W., Haskins C., Diggs S., Noor Z., Le L., Siddiqui A.A. 2009c Prime/boost and recombinant protein vaccination strategies using Sm-p80 protects against Schistosoma mansoni infection in the mouse model to levels previously attainable only by the irradiated cercarial vaccine. Parasitology Research, 105, 1767-1777. DOI: 10.1007/s00 436-009-1646-z Search in Google Scholar

Anand S.B., Murugan V., Prabhu P.R., Anandharaman V., Reddy M.V., Kaliraj P. 2008. Comparison of immunogenicity, protective efficacy of single and cocktail DNA vaccine of Brugia malayi abundant larval transcript (ALT-2) and thioredoxin peroxidase (TPX) inmice. Acta Tropica, 107, 106-112Search in Google Scholar

Anand S.B., Kodumudi K.N., Reddy M.V., Kaliraj P. 2011. A combination of two Brugia malayi filarial vaccine candidate antigens (BmALT-2 and BmVAH) enhances immune responses and protection in jirds. Journal of Helminthology, 85, 442-452. DOI: org/10.1017/S0022149X10000799Search in Google Scholar

Bergman P.J., Camps-Palau M.A., McKnight J.A., Leibman N.F., Craft D.M., Leung C., Liao J., Riviere I., Sadelain M., Hohenhaus A.E., Gregor P., Houghton A.N., Perales M.A., Wolchok J.D. 2006. Development of a xenogenetic DNA vaccine program for canine malignantmelanoma at the Animal Medical Center. Vaccine, 24, 4582-4585. DOI: 10.1016/j.vaccine.2005.08.027Search in Google Scholar

Bolhassani A., Gholami E., Zahedifard F., Moradin N., Parsi P., Doustdari F., Seyed N., Papadopoulou B., Rafati S. 2011. Leishmania major: Protective capacity of DNA vaccine using amastin fused to HSV-1 VP22 and EGFP in BALB/c mice model. Experimental Parasitology, 128, 9-17. DOI: 10.1016/ j.exppara.2011.01.012Search in Google Scholar

Cao S., Mousa A.A., Aboge G.O., Kamyingkird K., Zhou M., Moumouni P.F.A., Terkawi M.A., Masatani T., Nishikawa Y., Suzuki H., Fukumoto S., Xuan X. 2013. Prime-boost vaccinationwith plasmid DNA followed by recombinant vaccinia virus expressing BgGARP induced a partial protective immunity to inhibit Babesia gibsoni proliferation in dogs. Acta Parasitologica, 58, 619-623. DOI: 10.2478/s11686-013-0183-1Search in Google Scholar

Cannas A., Naguleswaran A., Muller N., Eperon S., Gottstein B., Hemphill A. 2003. Vaccination of mice against experimental Neospora caninum infection using NcSAG1- and NcSRS2- based recombinant antigens and DNA vaccines. Parasitology, 126, 303-312Search in Google Scholar

Chlichlia K., Bahgat M., Ruppel A., Schirrmacher V. 2001. DNA vaccination with asparaginyl endopeptidase (Sm32) from the parasite Schistosoma mansoni: anti-fecundity effect induced in mice. Vaccine, 20, 439-447Search in Google Scholar

Cruz Lança A.S., de Sousa K.P., Atouguia J., Prazeres D.M.F., Monteiro G.A., Silva M.S. 2011. Trypanosoma brucei: Immunisation with plasmid DNA encoding invariant surface glycoprotein gene is able to induce partial protection in experimental African trypanosomiasis. Experimental Parasitology, 127, 18-24. DOI: 10.1016/j.exppara.2010.06.017Search in Google Scholar

Da’dara A.A., Skelly P.J., Fatakawadala M., Visovatti S., Eriksson E., Harn D.A. 2002. Comparative efficacy of the Schistosoma mansoni nucleic acid vaccine, Sm23, following microseeding or gene gun delivery. Parasite Immunology, 24, 179-187Search in Google Scholar

Da’Dara A.A., Li Y.S., Xiong T., Zhou J.,Williams G.M., McManus D.P., Fenge Z., Yu X.L., Gray D.J., Harn D.A. 2008. DNAbased vaccines protect against zoonotic schistosomiasis in water buffalo. Vaccine, 26, 3617-3625. DOI: 10.1016/j.vaccine.2008.04.080Search in Google Scholar

Dalton J.P., Robinson M.W., Mulcahy G., O’Neill S.M., Donnelly S. 2013. Immunomodulatory molecules of Fasciola hepatica. Candidates for both vaccine and immunotherapeutic development. Veterinary Parasitology, 195, 272-285. DOI: org/10.1016/j.vetpar.2013.04.008Search in Google Scholar

Davidson A.H., Traub-Dargatz J.L., Rodeheaver R.M., Ostlund E.N., Pedersen D.D., Moorhead R.G., Stricklin J.B., Dewell R.D., Roach S.D., Long R.E., Albers S.J., Callan R.J., Salman M.D.2005. Immunologic responses to West Nile virus in vaccinated and clinically affected horses. Journal of the American Veterinary Medical Association, 226, 240-245. DOI: 10.2460/ javma.2005.226.240Search in Google Scholar

Dobano C., Rogers W.O.,Gowda K., Doolan D.L. 2007. Targeting antigen to MHC Class I and Class II antigen presentation pathways for malaria DNA vaccines. Immunology Letters, 111, 92-102. DOI: 10.1016/j.imlet.2007.05.007Search in Google Scholar

Du A., Wang S. 2005. Efficacy of a DNA vaccine delivered in attenuated Salmonella typhimurium against Eimeria tenella infection in chickens. International Journal forParasitology, 35, 777-785. DOI: 10.1016/j.ijpara.2005.03.005Search in Google Scholar

Dunachie S.J.,Walther M., Epstein J.E., Keating S., Berthoud T., Andrews, L., Andersen R.F., Bejon P., Goonetilleke N., Poulton I., Webster D.P., Butcher G., Watkins K., Sinden R.E., Levine GL., Richie, T.L., Schneider J., Kaslow D., Gilbert S.C., Carucci D.J., Hill A.V.S. 2006. A DNA Prime-Modified Vaccinia Virus Ankara Boost Vaccine Encoding Thrombospondin- Related Adhesion Protein but Not Circumsporozoite Protein Partially Protects Healthy Malaria- Naive Adults against Plasmodium falciparum Sporozoite Challenge. Infection and Immunity, 74, 5933-5942. DOI: 10.1128/IAI.00590-06Search in Google Scholar

Espino A.M., Morales A., Delgado B., Rivera F.M., Figueroa O., Suárez E. 2010. Partial immunity to Fasciola hepatica in mice after vaccination with FhSAP2 delivered as recombinant protein or DNA construct. Ethnicity & Disease, 20, S1-17-23Search in Google Scholar

Fukumoto F., Tamaki Y., Igarashi I., Suzuki H., Xuan X. 2009. Immunogenicity and growth inhibitory efficacy of the prime- boost immunization regime with DNA followed by recombinant vaccinia virus carrying the P29 gene of Babesia gibsoni in dogs. Experimental Parasitology, 123, 296-301. DOI: 10. 1016/j.exppara.2009.08.012Search in Google Scholar

Garver K.A., LaPatra S.E., Kurath G. 2005. Efficacy of an infectious hematopoietic necrosis (IHN) virus DNA vaccine in Chinook Oncorhynchus tshawytscha and sockeye O. nerka salmon. Diseases of Aquatic Organisms, 64, 13-22. DOI: 10.3354/ dao064013Search in Google Scholar

Geriletu Xu L., Xurihu Li X. 2011. Vaccination of chickens with DNA vaccine expressing Eimeria tenella MZ5-7 against coccidiosis. Veterinary Parasitology, 177, 6-12. DOI: 10.1016/ j.vetpar.2010.11.041Search in Google Scholar

Han K., Xu L., Yan R., Song X., Li X. 2012. Vaccination of goats with glyceraldehyde-3- phosphate dehydrogenase DNA vaccine induced partial protection against Haemonchus contortus. Veterinary Immunology and Immunopathology, 149, 177-185. DOI :10.1016/j.vetimm.2012.06.016. Epub 2012 Jun 19Search in Google Scholar

He S., Yang L., Lv Z., Hu W., Cao J., Wei J., Sun X., Zheng H., Wu Z. 2010. Molecular and functional characterization of a mortalin-like protein from Schistosoma japonicum (SjMLP/ hsp70) as a member of the HSP70 family. Parasitology Research, 107, 955-966. DOI: 10.1007/s00436-010-1960-5Search in Google Scholar

Hezarjaribi H.Z., Ghaffarifar F., Dalimi F., Sharifi Z., Jorjani O. 2013. Effect of IL-22 on DNA vaccine encoding LACK gene of Leishmania major in BALB/c mice. Experimental Parasitology, 134, 341-348. DOI: org/10.1016/j.exppara.2013.03.012Search in Google Scholar

Hiszczynska-Sawicka E., Olędzka G., Holec-Gąsior L., Li H., Xua, J.B. Sedcole R., Kur J., Bickerstaffe R., Stankiewicz M. 2011a. Evaluation of immune responses in sheep inducedby DNA immunization with genes encoding GRA1, GRA4, GRA6 and GRA7 antigens ofToxoplasma gondii. Veterinary Parasitology, 177, 281-289. DOI: 10.1016/j.vetpar.2010. 11.047 Search in Google Scholar

Hiszczynska-Sawicka E., Li H., Xua J.B., Holec-Gąsior L., Kur J., Sedcole R., Bickerstaffe R., Stankiewicz M. 2011b. Modulation of immune response to Toxoplasma gondii in sheep by immunization with a DNA vaccine encoding ROP1 antigen as a fusion protein with ovine CD154. Veterinary Parasitology, 183, 72-78. DOI: 10.1016/j.vetpar.2011.06.010Search in Google Scholar

Januszkiewicz K. 2010. Optimalization of vaccination against Fasciola hepatica infections using cDNA encoding for selected fluke antigens and specific for the host species CTLA-4 molecule. PhD Thesis. Witold Stefański Institute of Parasitology Polish Academy of Sciences, Warsaw, Poland Search in Google Scholar

Jaros S., Jaros D., Wesolowska A., Zygner W., Wedrychowicz H. 2010. Blocking Fasciola hepatica‘s energy metabolism - a pilot study of vaccine potential of a novel gene - phosphoglycerate kinase. Veterinary Parasitology, 172, 229-237. DOI: 10.1016/j.vetpar.2010.05.008Search in Google Scholar

Jayaraj R., Piedrafita D., Spithill T., Smooker P. 2012. Evaluation of the immune responses induced by four targeted DNA vaccines encoding the juvenile liver fluke antigen, cathepsin B in a mouse model. Genetic Vaccines and Therapy 2012, 10, 2-7, in Google Scholar

Jenkins M., Parker C., Tuo W.,Vinyard B., Dubey J.P. 2004. Inclusion of CpG adjuvant with plasmid DNA coding for NcGRA7 improves protection against congenital neosporosis. Infection and Immunity, 72, 1817-1819, DOI: 10.1128/IAI.72.3.1817-1819.2004Search in Google Scholar

Kalyanasundaram R., Balumuri P. 2011. Multivalent vaccine formulation with BmVAL-1 and BmALT-2 confer significant protection against challenge infections with Brugia malayi in mice and jirds. Research and Reports in Tropical Medicine 2011, 45-56. DOI: 10.2147/RRTMS13679Search in Google Scholar

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. DOI: 10.1016/ j.vaccine.2005.08.076Search in Google Scholar

Kimani D., Jagne Y.J., Cox M., Kimani E., Bliss C.M., Gitau, E., Ogwang C., Afolabi M.O., Bowyer G., Collins K.A. et al. 2014. Translating the immunogenicity of prime-boost immunization with ChAd63 and MVA ME-TRAP from malaria naive to malaria-endemic populations. Molecular Therapy, 22, 1992-2003. DOI: 10.1038/mt.2014.109.Search in Google Scholar

Klinman D.M., Yamshchikov G., Ishigatsubo Y. Contribution of CpG motifs to the immunogenicity of DNA vaccines. Journal of Immunology, 158, 3635-3642Search in Google Scholar

Kofta W., Wędrychowicz H. 2001. c-DNA vaccination against parasitic infections: advantages and disadvantages. Veterinary Parasitology 94; 243-247, DOI: 10.1016/SO304-4017(01) 00478-2Search in Google Scholar

Kurup S.P., Tewari A.K. 2012. Induction of protective immune response in mice by a DNA vaccine encoding Trypanosoma evansi beta tubulin gene. Veterinary Parasitology, 187, 9-16. DOI: 10.1016/j.vetpar.2012.01.009Search in Google Scholar

Lee J.S., Kim I.S., Sohn W.M., Lee J., Yong T.S. 2006a. A DNA vaccine encoding a fatty acid binding protein of Clonorchis sinensis induces protective immune response in Sprague-Dawley rats. Scandinavian Journal of Immunology, 63, 169-176 DOI: 10.1111/j.1365-3083.2006.01721.x Search in Google Scholar

Lee J., Kim I.S., Sohn W., Lee J., Yong T. 2006.b Vaccination with DNA encoding cysteine proteinase confers protective immune response to rats infected with Clonorchis sinensis.Vaccine, 24, 2358-2366Search in Google Scholar

Levine M.M. and Sztein M.B. 2004. Vaccine development strategies for improving immunization: The role of modern immunology. Nature Immunology, 5, 460-464. DOI: 10.1038/ni0504-460Search in Google Scholar

Li M., Lei J., WangT., Lu S., Guan F., Liu W., Li Y. 2011. Cimetidine enhances the protective effect of GST DNA vaccine against Schistosoma japonicum. Experimental Parasitology 128, 427-432. DOI: 10.1016/j.exppara.2011.05.012Search in Google Scholar

Liddell S., Parker C., Vinyard B., Jenkins M., Dubey J.P. 2003. Immunization of mice with plasmid DNA coding for NcGRA7 or NcsHSP33 confers partial protection against vertical transmission of Neospora caninum. Journal of Parasitology, 89, 496-500. DOI: org/10.1645/GE-2969Search in Google Scholar

Liu, M.A. 2010. DNA vaccines: An historical perspective and view to the future. Immunological Reviews, 239, 62-84. DOI: org/10.1111/j.1600-065X.2010.00980.x Liu Q., Shang L., Jin H., WeiF., Zhu Q., Gao H. 2010. The protective effect of a Toxoplasma gondii SAG1 plasmid DNA vaccine in mice is enhanced with IL-18. Research in Veterinary Science, 89, 93-97. DOI: 10.1016/j.rvsc.2010.01.007Search in Google Scholar

Mancini-Bourgine M., Fontaine H., Brechot C., Pol S., Michel M.L. 2006. Immunogenicity of a hepatitis B DNA vaccine administered to chronic HBV carriers. Vaccine, 24, 4482-4489. DOI: 10.1016/j.vaccine.2005.08.013Search in Google Scholar

Masih S., Arora S.K., Vasishta R.K. 2011. Efficacy of Leishmania donovani ribosomal P1 gene asDNA vaccine in experimental visceral leishmaniasis. Experimental Parasitology, 129, 55-64. DOI: 10.1016/j.exppara.2011.05.014Search in Google Scholar

Martin J.E., Louder M.K., Holman L.A., Gordon I.J., Enama M.E, Larkin B.D. et al. 2008 A SARS DNA vaccine induces neutralizing antibody and cellular immune responses in healthy adults in a Phase I clinical trial. Vaccine, 26, 6338-6343. DOI: 10.1016/j.vaccine.2008.09.026Search in Google Scholar

McCullers J.A. 2007. Evolution, benefits, and shortcomings of vaccine management. Journal of Managed Care Pharmacy, 13, S2-S6Search in Google Scholar

Mc Neilly T.N., Nisbet A.J. 2014. Immune modulation by helminth parasites of ruminants: implications for vaccine development and host immune competence. Parasite, 21, 51-62. DOI: 10.1051/parasite/2014051Search in Google Scholar

Molloy M., Bouladoux N., Belkaid Y. 2012. Intestinal microbiota: shaping local and systemic immune responses. Seminar in Immunology, 24, 51-55. DOI: 10.1016/j.smim.2011Search in Google Scholar

Nielsen H.V., Di Cristina M., Beghetto E., Spadoni A., Petersen E., Gargano N. 2006. Toxoplasma gondii: DNA vaccination with bradyzoite antigens induces protective immunity in mice against oral infection with parasite cysts. Experimental Parasitology, 112, 274-279. DOI: 10.1016/j.exppara.2005.11.009Search in Google Scholar

Payette P.J., Weeratna R.D., McCluskie M.J., Davis H.L. 2001. Immune- mediated destruction of transfected myocytes following DNA vaccination occurs via multiple mechanisms. Gene Therapy, 8, 1395-1400. DOI: org/10.1038/ in Google Scholar

Person R., Bodles-Brakhop A.M., Pope M.A., Brown P.A., Khan A.S., Draghia-Akli R. 2008. Growth hormone-releasing hormone plasmid treatment by electroporation decreases offspring mortality over three pregnancies. Molecular Therapy, 16, 1891-1897. DOI: 10.1038/mt.2008.178Search in Google Scholar

Qu D., Han J., Du A. 2013. Evaluation of protective effect of multiantigenic DNA vaccine encoding MIC3 and ROP18 antigen segments of Toxoplasma gondii in mice Parasitology Research, 112, 2593-2599. DOI 10.1007/s00436-013-3425-0Search in Google Scholar

Rafati S., Zahedifard F., Azari M.K.,Taslimi Y., Taheri T. 2008. Leishmania infantum: Prime boost vaccination with C-terminal extension of cysteine proteinase type I displays both type 1 and 2 immune signatures in BALB/c mice. Experimental Parasitology, 118, 393-401. DOI: 10.1016/j.exppara.2007.10.004Search in Google Scholar

Rainczuk A., Scorza T., Spithill T.W., Smooker P.M. 2004. A bicistronic DNA vaccine containing Apical Membrane Antigen 1 and Merozoite Surface Protein 4/5 can prime humoral and cellular immune responses and partially protect mice against virulent Plasmodium chabaudi adami DS malaria.. Infection and Immunity, 72, 5565-5573. DOI: 10.1128/IAI.72.10. 5565-5573.2004Search in Google Scholar

Rathaur S., Yadav M., Gupta S., Anandharaman V., Reddy M.V. 2008. Filarial glutathione-S- transferase: a potential vaccine candidate against lymphatic filariasis. Vaccine, 26, 4094-4100. DOI: 10.1016/j.vaccine.2008.03.099Search in Google Scholar

Robinson M.W., Dalton J.P., O’Brien B.A., Donnelly S. 2013. Fasciola hepatica: The therapeutic potential of a worm secretome. International Journal for Parasitology, 43, 283-291. ttp:// in Google Scholar

Saade F., Petrovsky N. 2012. Technologies for enhanced efficacy of DNA vaccines. Expert Review of Vaccines, 11, 189-209. DOI: 10.1586/erv.11.188Search in Google Scholar

Sato Y, Roman M., Tighe H., Lee D., Corr M., Nguyen M., Silverman G.J., Lotz M., Carson D.A., Raz E. 1996. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science, 273, 352-354Search in Google Scholar

Shah M.A.A.,Yan R., Xu L., Song X., Li X. 2010. A recombinant DNA vaccine encoding Eimeria acervulina cSZ-2 induces immunity against experimental E. tenella infection. Veterinary Parasitology, 169, 185-189. DOI: 10.1016/j.vetpar.2009.12.035Search in Google Scholar

Shah M.A.A., Song X., Xu L.,Yan R., Li X. 2011. Construction of DNA vaccines encoding Eimeria acervulina cSZ-2 with chicken IL-2 and IFN-c and their efficacy against poultry coccidiosis. Research in Veterinary Science, 90, 72-77. DOI: 10.1016/j.rvsc.2010.05.003Search in Google Scholar

ShiW., Liu Q., Zhang J., Sun J., Jiang X., Geng J., Wang F., Xiao Y., Li H., Zhao X. 2014. Co-expression of EtMic2 protein and chicken interleukin-18 for DNA vaccine against chicken coccidiosis. Research in Veterinary Science, 97, 64-70. DOI: org/10.1016/j.rvsc.2014.05.001Search in Google Scholar

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, DOI: 10.1006/expr.2001.4601Search in Google Scholar

Song X., Xu L., Yan R., Huang X., Shah M.A.A., Li X. 2009. The optimal immunization procedure of DNA vaccine pcDNA- TA4-IL-2 of Eimeria tenella and its cross-immunity to Eimeria necatrix and Eimeria acervulina. Veterinary Parasitology 159, 30-36. DOI: 10.1016/j.vetpar.2008.10.015Search in Google Scholar

Song H., Yan R., Xu L., Song X., Shah M.A.A., Zhu H., Li X., 2010. Efficacy of DNA vaccines carrying Eimeria acervulina lactate dehydrogenase antigen gene against coccidiosis. Experimental Parasitology, 126, 224-231. DOI: 10.1016/j.exppara. 2010.05.015Search in Google Scholar

Song H., Qiu B.,Yan R Xu L., Song X., Li X. 2013. The protective efficacy of chimeric SO7/IL-2 DNA vaccine against coccidiosis in chickens Research in Veterinary Science, 94, 562-567. DOI: org/10.1016/j.rvsc.2012.11.006Search in Google Scholar

Schneider J., Langermans J.A., Gilbert S.C., Blanchard T.J., Twigg S., Naitza S., Hannan C.M., Aidoo M., Crisanti A., Robson K.J. et al. A prime-boost immunisation regimen using DNA followed by recombinant modified vaccinia virus Ankara induces strong cellular immune responses against the Plasmodium falciparum TRAP antigen in chimpanzees. Vaccine 2001, 19, 4595-4602Search in Google Scholar

Sun W., Song X., Yan R., Xu L., Li X. 2011.Vaccination of goats with a glutathione peroxidase DNA vaccine induced partial protection against Haemonchus contortus infection. Veterinary Parasitology 182, 239-247. DOI: 10.1016/j.vetpar.2011.05.024Search in Google Scholar

Thirugnanam S., Pandiaraja P., Ramaswamy K., Murugan V., Gnanasekar M., Nanadakumar K., Reddy M.V., Kaliraj P. 2007. Brugia malayi: comparison of protective immune responses induced by Bm-alt-2 DNA, recombinant Bm-ALT-2 protein and prime-boost vaccine regimens in a jird model. Experimental Parasitology, 116, 483-491. DOI: 10.1016/ j.exppara.2007.02.017Search in Google Scholar

Van Riet E., Hartgers F.C.,Yazdanbakhsh M. 2007. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology, 212, 6, 475-490. DOI: 10.1016/ j.imbio.2007.03.009Search in Google Scholar

Vaughan E.E., Dean D.A. 2006. Intracellular trafficking of plasmids during transfection is mediated by microtubules. Molecular Therapy, 13, 422-428. DOI: org/10.1016/j.ymthe.2005.10.004Search in Google Scholar

Waine G.J., Alarcon J.B., McManus D.P. 2002. Genetic immunization of mice with DNA encoding the 23 kDa transmembrane surface protein of Schistosoma japonicum (Sj23) induces antigen- specific immunoglobulin G antibodies. Parasite Immunology, 1999, 21, 377-381Search in Google Scholar

Wang H., He S., Yao Y., Cong H., Zha H., Li T., Zhu X. 2009. Toxoplasma gondii: Protective effect of an intranasal SAG1 and MIC4 DNA vaccine in mice. Experimental Parasitology, 122, 226-232. DOI: 10.1016/j.exppara.2009.04.002Search in Google Scholar

Wahren W., Liu M.A. 2014. DNA vaccines: recent developments and the future. Vaccines, 2, 785-796. DOI: 10.3390/vaccines 2040785Search in Google Scholar

WesołowskaA., NorburyL., Januszkiewicz K., Jedlina L., Jaros S., Zawistowska- Deniziak A., ZygnerW., Wędrychowicz H. 2013. Evaluation of the immune response of male and female rats vaccinated with cDNA encoding a cysteine proteinase of Fasciola hepatica (FhPcW1). Acta Parasitologica, 58, 198-206. DOI :10.2478/s11686-013-0120-3Search in Google Scholar

Wedrychowicz H., Szymanski P., Panasiuk L.J., Bienkowska-Szewczyk K. 2002. Humoral immune response of rats vaccinated with cDNA or protein form of glutathione-S-transferase of Fasciola hepatica to infection with metacercariae of the fluke. Helminthologia, 39, 127-133Search in Google Scholar

Wędrychowicz H., Lamparska M., Kęsik M., Kotomski G., Mieszczanek J., Jedlina-Panasiuk L., Płucienniczak A. 2003. The immune response of rats to vaccination with cDNA or protein forms of the cysteine proteinase of Fasciola hepatica. Veterinary Immunology and Immunopathology, 94, 83-93. DOI: 10.1016/S0165-2427(03)00085-0Search in Google Scholar

Williams J.A. 2013. Vector Design for Improved DNA Vaccine Efficacy, Safety and Production. Vaccines, 1, 225-249. DOI: 10.3390/vaccines1030225Search in Google Scholar

Wiśniewski M., Jaros S., Bąska P., Capello M., Wędrychowicz H. 2013. Ancylostoma ceylanicum metalloprotease 6 DNA vaccination induces partial protection against hookworm challenge infection. Acta Parasitologica 58, 376-383. DOI: 10.2478/s11686-013-0151-9Search in Google Scholar

Wolff J.A., Malone R.W., Williams P., Chong W., Acsadi G., Jani A., Felgner P.L. 1990. Direct gene transfer into mouse muscle in vivo. Science, 247, 1465-1468. DOI: org/10.1126/science. 1690918Search in Google Scholar

Xiang W., Qiong Z., Li-peng L., Kui T., Jian-wu G., Heng-ping S. 2009. The location of invasion- related protein MIC3 of Toxoplasma gondii and protective effect of its DNA vaccine in mice. Veterinary Parasitology, 166, 1-7. DOI: 10.1016/j.vetpar. 2009.08.014Search in Google Scholar

Xu Q., Song X., Xu L., Yan R., Shah M., Li X., 2008. Vaccination of chickens with a chimeric DNA vaccine encoding Eimeria tenella TA4 and chicken IL-2 induces protective immunity against coccidiosis. Veterinary Parasitology, 156, 319-323. DOI: 10.1016/j.vetpar.2008.05.025Search in Google Scholar

Xue M., He S., Zhang J., Cui Y., Yao Y.,Wang H. 2008a. Comparison of cholera toxin A2/B and murine interleukin-12 as adjuvants of Toxoplasma multi-antigenic SAG1-ROP2 DNA vaccine. Experimental Parasitology, 119, 352-357, DOI: 10.1016/ j.exppara.2008.03.005Search in Google Scholar

Xue M., He S., Zhang J., Cui Y., Yao Y.,Wang H. 2008b. Evaluation of the immune response elicited by multi-antigenic DNA vaccine expressing SAG1, ROP2 and GRA2 against Toxoplasma gondii. Parasitology International 57,424-429. DOI: 10.1016/ j.parint.2008.05.001Search in Google Scholar

Yamakami K., Akao S., Sato M., Nitta Y., Miyazaki J., Tadakuma T. 2001. A single intradermal administration of soluble leishmanial antigen and plasmid expressing interleukin-12 protects BALB c mice from Leishmania major infection.. Parasitology International, 50, 81-91Search in Google Scholar

Yan H.,Yuan Z., Petersen E., Zhang X., Zhou D., Liu Q., He Y., Lin R., Xu M., Chen X., Zhong X., Zhu X. 2011.Toxoplasma gondii: Protective immunity against experimental toxoplasmosis induced by a DNA vaccine encoding the perforin-like protein 1. Experimental Parasitology, 128, 38-43. DOI: 10.1016/j.exppara.2011.02.005Search in Google Scholar

Yan R., Sun W., Song X., Li X. 2013. Vaccination of goats with DNA vaccine encoding Dim-1 induced partial protection against Haemonchus contortus: A preliminary experimental study Research in Veterinary Science, 95, 189-199. DOI: org/10.1016/j.rvsc.2013.02.020Search in Google Scholar

You Z., Huang X., Hester J., Toh H.C., Chen S.Y. 2001. Targeting dendritic cells to enhance DNA vaccine potency. Cancer Research, 61, 3704-3711Search in Google Scholar

Yu Q., Li J., Zhang X., Gong P., Zhang P., Li S., Wang H. 2010. Induction of immune responses in mice by a DNA vaccine encoding Cryptosporidium parvum Cp12 and Cp21 and its effect against homologous oocyst challenge. Veterinary Parasitology. 172, 1-7. DOI: 10.1016/j.vetpar.2010.04.036Search in Google Scholar

Yu L., Yamagishi J., Zhang S., Jin Ch., Aboge O.G., Zhang H., Zhang G., Tanaka T., Fujisaki K., Nishikawa Y., Xuan X. 2012. Protective effect of a prime-boost strategy with plasmid DNA followed by recombinant adenovirus expressing TgAMA1 as vaccines against Toxoplasma gondii infection in mice. Parasitology International, 61, 481-486. DOI: 10.1016/j.parint. 2012.04.001Search in Google Scholar

Yuan H.,You-en S., Long-jiang Y., Xiao-hua Z., Liu-zhe L.,Cash M., Lu Z., Zhi L., Deng-xin S. 2006. Studies on the protective immunity of Schistosoma japonicum bivalent DNA vaccine encoding Sj23 and Sj14. Experimental Parasitology, 115, 379-386. DOI: 10.1016/j.exppara.2006.09.022Search in Google Scholar

Zhao Y., Bao Y., Zhang L., Chang L., Jiang L., Liu Y., Zhang L., Qin J. 2013. Biosafety of the plasmid pcDNA3-1E of Eimeria acervulina in chicken. Experimental Parasitology, 133, 231-236, DOI: org/10.1016/j.exppara.2012.11.026Search in Google Scholar

Zhao G., Yan R., Muleke C.I., Sun Y., Xu L., Li X. 2012. Vaccination of goats with DNA vaccines encoding H11 and IL-2 induces partial protection against Haemonchus contortus infection. Veterinary Journal, 191, 94-100. DOI: 10.1016/j.tvjl.2010.12.023. Epub 2011 Feb 16.Search in Google Scholar

Zhu Y., Lu F., Dai Y., Wang X., Tang J., Zhao S., Zhang Ch., Zhang H., Lu S., Wang S. 2010. Synergistic enhancement of immunogenicity and protection in mice against Schistosoma japonicum with codon optimization and electroporation delivery of SjTPI DNA vaccines. Vaccine, 28, 5347-5355. DOI: 10.1016/j.vaccine.2010.05.017Search in Google Scholar

Zhu L., Liu H., Lu M., Long Q., Shi Y., Yu L. 2011.Construction, purification, and evaluation of multivalent DNA vaccine against Schistosoma japonicum Parasitology Research, 108, 115- 121. DOI: 10.1007/s00436-010-2040-6 Search in Google Scholar

Received: 2014-12-14
Revised: 2014-12-15
Accepted: 2014-12-17
Published Online: 2015-3-25
Published in Print: 2015-6-1

© 2015 W. Stefański Institute of Parasitology, PAS