Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 16, 2015

Chimeric DNA vaccines encoding Eimeria acervulina macrophage migration inhibitory factor (E.MIF) induce partial protection against experimental Eimeria infection

Xiaokai Song, Ruirui Zhang, Lixin Xu, Ruofeng Yan and Xiangrui Li
From the journal Acta Parasitologica

Abstract

Chimeric DNA vaccines co-expressing Eimeria acervulina macrophage migration inhibitory factor (E.MIF) and chicken IL-2 (IL-2) or interferon-γ (IFN-γ) were constructed and their efficacies against E. acervulina were evaluated. The open reading frame (ORF) of E.MIF was cloned from E. acervulina merozoites and subcloned into the eukaryotic expression vector pVAX1 with chicken cytokine gene IFN-γ or IL-2 to construct the DNA vaccines pVAX-E.MIF-IFN-γ, pVAX-E.MIF-IL-2 and pVAX-E.MIF. The in vivo transfection of the target genes was detected by use of reverse transcription polymerase chain reaction (RT-PCR) and Western blot. Immunizations were carried out by vaccinating chickens twice with a dose rate of 100 μg intramuscularly. Seven days post second immunization, all chickens except the unchallenged control group were challenged orally with 1 × 105 sporulated oocysts of E. acervulina. Seven days later, the duodenum was collected. The results showed that the target genes were expressed effectively in vivo. DNA vaccines and the recombinant E.MIF protein could alleviate body weight loss and duodenal lesions significantly compared to the control groups. Furthermore, pVAX-E.MIF-IL-2 and pVAX-E.MIF-IFN-γ induced anticoccidial indexs (ACIs) of 179.12 and 170, respectively, which were significantly higher than that of pVAX-E.MIF (ACI = 162.31). Our results demonstrated that E.MIF is a potential vaccine candidate against E. acervulina and chicken IFN-γ or IL- 2 may be used as genetic adjuvants to improve the efficacies of DNA vaccines against avian coccidiosis.

References

Alam A., Goyal M., Iqbal M.S., Bindu S., Dey S., Pal C., Maity P., Mascarenhas N.M., Ghoshal N., Bandyopadhyay U. 2011. Cysteine-3 and cysteine-4 are essential for the thioredoxinlike oxidoreductase and antioxidant activities of Plasmodium falciparum macrophage migration inhibitory factor. Free Radical Biology and Medicine, 50, 1659-1668. DOI: 10.1016/ j.freeradbiomed.2011.03.01210.1016/j.freeradbiomed.2011.03.012Search in Google Scholar

Asif M., Jenkins K.A., Hilton L.S., Kimpton W.G., Bean A.G., Lowenthal J.W. 2004. Cytokines as adjuvants for avian vaccines. Immunology and Cell Biology, 82, 638-643. DOI: 10.1111/j.1440-1711.2004.01295.x 10.1111/j.1440-1711.2004.01295.xSearch in Google Scholar

Blake D.P., Tomley F.M. 2014. Securing poultry production from the ever-present Eimeria challenge. Trends in Parasitology, 30, 12-19. DOI: 10.1016/j.pt.2013.10.00310.1016/j.pt.2013.10.003Search in Google Scholar

Chabalgoity J.A., Baz A., Rial A., Grille S. 2007. The relevance of cytokines for development of protective immunity and rational design of vaccines. Cytokine and Growth Factor Reviews, 18, 195-207. DOI: 10.1016/j.cytogfr.2007. 01.016Search in Google Scholar

Chow Y.H., Chiang B.L., Lee Y.L., Chi W.K., Lin W.C., Chen Y.T., Tao M.H. 1998. Development of Th1 and Th2 populations and the nature of immune responses to hepatitis B virus DNA vaccines can be modulated by codelivery of various cytokine genes. The Journal of Immunology, 160, 1320-1329Search in Google Scholar

Cordery D.V., Kishore U., Kyes S., Shafi M.J., Watkins K.R., Williams T.N., Marsh K., Urban B.C. 2007. Characterization of a Plasmodium falciparum macrophage-migration inhibitory factor homologue. The Journal of Infectious Diseases, 195, 905-912. DOI: 10.1086/51130910.1086/511309Search in Google Scholar

Dalloul R.A., Lillehoj H.S. 2006. Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Review of Vaccines, 5, 143-163. DOI: 10.1586/147 60584.5.1.143Search in Google Scholar

Ding X., Lillehoj H.S., Quiroz M.A., Bevensee E., Lillehoj E.P. 2004. Protective immunity against Eimeria acervulina following in ovo immunization with a recombinant subunit vaccine and cytokine genes. Infection and Immunity 72, 6939-6944. DOI: 10.1128/IAI.72.12.6939-6944.200410.1128/IAI.72.12.6939-6944.2004Search 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 for Parasitology, 35, 777-785. DOI: 10.1016/j.ijpara.2005.03.00510.1016/j.ijpara.2005.03.005Search in Google Scholar

Geriletu, Xu L., Xurihua, 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.2010.11.04110.1016/j.vetpar.2010.11.041Search in Google Scholar

Han C., Lin Y., Shan G., Zhang Z., Sun X., Wang Z., Wei C., Deng Y., Zhang L., Bu L., Shao D., Wang H. 2010. Plasma concentration of malaria parasite-derived macrophage migration inhibitory factor in uncomplicated malaria patients correlates with parasitemia and disease severity. Clinical and Vaccine Immunology, 17, 1524-1532. DOI: 10.1128/CVI.00149-1010.1128/CVI.00149-10Search in Google Scholar

Hoan T.D., Thao D.T., Gadahi J.A., Song X., Xu L., Yan R., Li X. 2014. Analysis of humoral immune response and cytokines in chickens vaccinated with Eimeria brunetti apical membrane antigen-1 (EbAMA1) DNA vaccine. Experimental Parasitology, 144, 65-72. DOI: 10.1016/j.exppara.2014.04.01510.1016/j.exppara.2014.04.015Search in Google Scholar

Hong Y.H, Lillehoj H.S, Lee S.H., Dalloul R.A., Lillehoj E.P. 2006. Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Veterinary Immunology and Immunopathology, 114, 209-223. DOI: 10.1016/j.vetimm.2006.07.00710.1016/j.vetimm.2006.07.007Search in Google Scholar

Ivory C., Chadee K. 2004. DNA vaccines: designing strategies against parasitic infections. Genet Genetic Vaccines and Therapy, 2, 17. DOI: 10.1186/1479-0556-2-1710.1186/1479-0556-2-17Search in Google Scholar

Jang S.I., Lillehoj H.S., Lee S.H., Kim D.K., Pages M., Hong Y.H., Min W., Lillehoj E.P. 2011. Distinct immunoregulatory properties of macrophage migration inhibitory factors encoded by Eimeria parasites and their chicken host. Vaccine, 29, 8998-9004. DOI: 10.1016/j.vaccine.2011.09.03810.1016/j.vaccine.2011.09.038Search in Google Scholar

Jenkins M.C., Dame J.B. 1987. Identification of immunodominant surface antigens of Eimeria acervulina sporozoites and merozoites. Molecular and Biochemical Parasitology, 25, 155-164. DOI: 10.1016/0166-6851(87)90004-110.1016/0166-6851(87)90004-1Search in Google Scholar

Johnson J., Reid W.H. 1970. Anticoccidial drug: lesion scoring techniques in battery and floor-pen experiment. Experimental Parasitology, 29, 30-36. DOI: 10.1016/0014-4894(70)90063-910.1016/0014-4894(70)90063-9Search in Google Scholar

Kamir D., Zierow S., Leng L., Cho Y., Diaz Y., Griffith J., McDonald C., Merk M., Mitchell R.A., Trent J., Chen Y., Kwong Y.K., Xiong H., Vermeire J., Cappello M., McMahon-Pratt D., Walker J., Bernhagen J., Lolis E., Bucala R. 2008. A Leishmania ortholog of macrophage migration inhibitory factor modulates host macrophage responses. The Journal of Immunology, 180, 8250-8261. DOI: 10.4049/jimmunol.180.12.825010.4049/jimmunol.180.12.8250Search in Google Scholar

Kleemann R., Hausser A., Geiger G., Mischke R., Burger-Kentischer A., Flieger O., Johannes F.J., Roger T., Calandra T., Kapurniotu A., Grell M., Finkelmeier D., Brunner H., Bernhagen J. 2000. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature, 408, 211-216. DOI: 10.1038/35041591 10.1038/35041591Search in Google Scholar

Kopko S.H., Martin D.S., Barta J.R. 2000. Responses of chickens to a recombinant refractile body antigen of Eimeria tenella administered using various immunizing strategies. Poultry Science, 79, 336-342. DOI: 10.1093/ps/79.3.33610.1093/ps/79.3.336Search in Google Scholar

Lillehoj H.S., Choi K.D., Jenkins M.C., Vakharia V.N., Song K.D., Han J.Y., Lillehoj E.P. 2000. A recombinant Eimeria protein inducing interferon-gamma production: comparison of different gene expression systems and immunization strategies for vaccination against coccidiosis. Avian Diseases, 44, 379-38910.2307/1592553Search in Google Scholar

Lillehoj H.S., Ding X., Quiroz M.A., Bevensee E., Lillehoj E.P. 2005. Resistance to intestinal coccidiosis following DNA immunization with the cloned 3-1E Eimeria gene plus IL-2, IL-15, and IFN-gamma. Avian Diseases, 49, 112-117. DOI: 10. 1637/7249-073004R 10.1637/7249-073004RSearch in Google Scholar

Martin A., Awadalla S., Lillehoj H.S. 1995. Characterization of cellmediated responses to Eimeria acervulina antigens. Avian Diseases, 39, 538-547. DOI: 10.2307/159180710.2307/1591807Search in Google Scholar

Miller J.L., Harupa A., Kappe S.H., Mikolajczak S.A. 2012. Plasmodium yoelii macrophage migration inhibitory factor is necessary for efficient liver-stage development. Infection and Immunity, 80, 1399-1407. DOI: 10.1128/IAI.05861-1110.1128/IAI.05861-11Search in Google Scholar

Min W., Lillehoj H.S., Burnside J., Weining K.C., Staeheli P., Zhu J.J. 2001. Adjuvant effects of IL-1β, IL-2, IL-8, IL-15, IFN- α, IFN-γ TGF-β4 and lymphotactin on DNA vaccination against Eimeria acervulina. Vaccine, 20, 267-274. DOI: 10.1016/S0264-410X(01)00270-510.1016/S0264-410X(01)00270-5Search in Google Scholar

Miska K.B., Fetterer R.H., Lillehoj H.S., Jenkins M.C., Allen P.C., Harper S.B. 2007. Characterisation of macrophage migration inhibitory factor from Eimeria species infectious to chickens. Molecular and Biochemical Parasitology, 151, 173-183. DOI: 10.1016/j.molbiopara.2006.10.02010.1016/j.molbiopara.2006.10.020Search in Google Scholar

Qu G., Fetterer R., Jenkins M., Leng L., Shen Z., Murphy C., Han W., Bucala R., Tuo W. 2013. Characterization of Neospora Caninum macrophage migration inhibitory factor. Experimental Parasitology, 135, 246-256. DOI: 10.1016/j.exppara.2013. 07.001Search in Google Scholar

Reid A.J., Blake D.P., Ansari H.R., Billington K., Browne H.P., Bryant J., Dunn M., Hung S.S., Kawahara F., Miranda-Saavedra D., Malas T.B., Mourier T., Naghra H., Nair M., Otto T.D., Rawlings N.D., Rivailler P., Sanchez-Flores A., Sanders M., Subramaniam C., Tay Y.L., Woo Y., Wu X., Barrell B., Dear P.H., Doerig C., Gruber A., Ivens A.C., Parkinson J., Rajandream M.A., Shirley M.W., Wan K.L., Berriman M., Tomley F.M., Pain A. 2014. Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Research, 24, 1676-1685. DOI: 10.1101/gr.168955.113 10.1101/gr.168955.113Search in Google Scholar

Rosado J.de D., Rodriguez-Sosa M. 2011. Macrophage migration inhibitory factor (MIF): a key player in protozoan infections. International Journal of Biological Sciences, 7, 1239-1256. DOI: 10.7150/ijbs.7.123910.7150/ijbs.7.1239Search in Google Scholar

Shah M.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-γ and their efficacy against poultry coccidiosis. Research in Veterinary Science, 90, 72-77. DOI: 10.1016/j.rvsc.2010.05.00310.1016/j.rvsc.2010.05.003Search in Google Scholar

Sin J.I., Kim J.J., Boyer J.D., Ciccarelli R.B., Higgins T.J., Weiner D.B. 1999. In vivo modulation of vaccine-induced immune responses toward a Th1 phenotype increases potency and vaccine effectiveness in a herpes simplex virus type 2 mouse model. Journal of Virology, 73, 501-50910.1128/JVI.73.1.501-509.1999Search 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: 10.1016/j.rvsc.2012.11.00610.1016/j.rvsc.2012.11.006Search in Google Scholar

Song H., Yan R., Xu L., Song X., Shah M.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 X., Xu L., Yan R., Huang X., Shah M.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.2008.10.01510.1016/j.vetpar.2008.10.015Search in Google Scholar

Vermeire J.J., Cho Y., Lolis E., Bucala R., Cappello M. 2008. Orthologs of macrophage migration inhibitory factor from parasitic nematodes. Trends in Parasitology, 24, 355-363. DOI: 10.1016/j.pt.2008.04.00710.1016/j.pt.2008.04.007Search in Google Scholar

Wedrychowicz H. 2015. Antiparasitic DNA vaccines in 21st century. Acta Parasitologica, 60, 179-189. DOI: 10.1515/ap-2015-002610.1515/ap-2015-0026Search in Google Scholar

William RB. 1999. A compartmentalised model for estimation of the cost of coccidiosis to the world’s chicken production industry. International Journal for Parasitology, 29, 1209-1229. DOI: 10.1016/S0020-7519(99)00086-710.1016/S0020-7519(99)00086-7Search in Google Scholar

Witcombe D.M., Smith N.C. 2014. Strategies for anti-coccidial prophylaxis. Parasitology, 141, 1379-1389. DOI: 10.1017/ S003118201400019510.1017/S0031182014000195Search in Google Scholar

Xu Q., Song X., Xu L., Yan R., Shah M.A., 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.2008.05.02510.1016/j.vetpar.2008.05.025Search 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: 10.1016/j.exppara.2012.11.02610.1016/j.exppara.2012.11.026Search in Google Scholar

Received: 2015-1-5
Revised: 2015-2-10
Accepted: 2015-3-25
Published Online: 2015-6-16
Published in Print: 2015-9-1

© W. Stefański Institute of Parasitology, PAS