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Vaccination with a cocktail of Ancylostoma ceylanicum recombinant antigens leads to worm burden reduction in hamsters

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Abstract

Hookworms, a group to which Ancylostoma ceylanicum belongs, are gastrointestinal nematodes that infect more than 700 million people around the world. They are a leading cause of anemia in developing countries. In order to effectively prevent hookworm infections research is conducted to develop an effective vaccine using recombinant antigens of the parasite. The aim of this study was to examine the influence of the hosts’ on protection against ancylostomiasis and the shaping of the humoral immune response among Syrian hamsters after immunization with a cocktail of five A. ceylanicum recombinant antigens. Ace-ASP-3, Ace-ASP-4, Ace-APR-1, Ace-MEP-6 and Ace-MEP-7 were obtained in the pET expression system. Immunization with a vaccine cocktail resulted in a 33.5% worm burden reduction. The immunogenicity of the recombinant proteins were determined using ELISA. Statistical analysis showed that vaccinated hamsters developed stronger humoral responses to four of five recombinant antigens (the exception being Ace-ASP-3) compared to hamsters from the control group.

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References

  • Albonico M., Bickle Q., Ramsan M., Montresor A., Savioli L., Taylor M. 2003. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bulletin of the World Health Organization, 81, 343–352

    PubMed  PubMed Central  CAS  Google Scholar 

  • Albonico M., Smith P.G., Ercole E., Hall A., Chwaya H.M., Alawi K.S., Savioli L. 1995. Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or albendazole in a highly endemic area. Transactions of the Royal Society of Tropical Medicine and Hygiene, 89, 538–341

    Article  CAS  Google Scholar 

  • Bąska P., Wiśniewski M., Krzyżowska M., Długosz E., Zygner W., Górski P., Wędrychowicz H. 2013. Molecular cloning and characterization of in vitro immune response against astacinlike metalloprotease Ace-MTP-2 from Ancylostoma ceylanicum. Experimental Parasitology, 133, 472–482. DOI: 10.1016/j.exppara.2013.01.006

    Article  CAS  Google Scholar 

  • Bethony J., Loukas A., Smout M., Brooker S., Mendez S., Plieskatt J., Goud G., Bottazzi M.E., Zhan B., Wang Y., Williamson A., Lustigman S., Correa-Oliveira R., Xiao S., Hotez P.J. 2005. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB Journal, 19, 1743–1745. DOI: 10.1096/fj.05-3936fje

    Article  CAS  Google Scholar 

  • Bungiro R.D., Harrison L.M., Cappello M. 2002. Ancylostoma ceylanicum Excretory/Secretory Protein 1: Purification and molecular cloning of a major secretory protein from adult hookworms. Molecular and Biochemical Parasitology, 119, 147–151. DOI:10.1016/S0166-6851(01)00408-X

    Article  CAS  Google Scholar 

  • Bungiro R.D. Jr, Solis C.V., Harrison L.M., Cappello M. 2004. Purification and molecular cloning of and immunization with Ancylostoma ceylanicum excretory-secretory protein 2, an immunoreactive protein produced by adult hookworms. Infection and Immunity, 72, 2203–2213. DOI: 10.1128/IAI.72.4.2203-2213.2004

    Article  CAS  Google Scholar 

  • Cantacessi C., Campbell B.E., Visser A., Geldhof P., Nolan M., Nisbet A.J., Matthews J.B., Loukas A., Hofmann A., Otranto D., Sternberg P.W., Gasser R.B. 2009. A portrait of the ‘SCP/TAPS’ proteins of eukaryotes–Developing a framework for fundamental research and biotechnological outcomes. Biotechnology Advances, 27, 376–388. DOI: 10.1016/j.biotechadv.2009.02.005

    Article  CAS  Google Scholar 

  • Chu D., Bungiro R.D., Ibanez M., Harrison L.M., Campodonico E., Jones B.F., Mieszczanek J., Kuzmic P., Cappello M. 2004. Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: evidence for a role in hookworm-associated growth delay. Infection and Immunity, 72, 2214–2221. DOI: 10.1128/IAI.72.4.2214-2221.2004

    Article  CAS  Google Scholar 

  • Długosz E., Wiśniewski M., Wójcik L., Wędrychowicz H. 2010. In vitro IL-4, IL-12, and IFN-γ production by splenocytes from Ancylostoma ceylanicum infected hamsters. Bulletin of the Veterinary Institute in Pulawy, 54, 321–325

    Google Scholar 

  • Fairfax K.C., Vermeire J.J., Harrison L.M., Bungiro R.D., Grant W., Husain S.Z., Cappello M. 2009. Characterisation of a fatty acid and retinol binding protein orthologue from the hookworm Ancylostoma ceylanicum. International Journal for Parasitology, 39, 1561–1571. DOI: 10.1016/j.ijpara.2009.06.005

    Article  CAS  Google Scholar 

  • Goud G.N., Zhan B., Ghosh K., Loukas A., Hawdon J., Dobardzic A., Deumic V., Liu S., Dobardzic R., Zook B.C., Jin Q., Liu Y., Hoffman L., Chung-Debose S., Patel R., Mendez S., Hotez P.J. 2004. Cloning, yeast expression, isolation, and vaccine testing of recombinant Ancylostoma-secreted protein (ASP)-1 and ASP-2 from Ancylostoma ceylanicum. The Journal of Infectious Diseases, 189, 919–929. DOI: 10.1086/381901

    Article  CAS  Google Scholar 

  • Hotez P.J., Ashcom J., Zhan B., Bethony J., Loukas A., Hawdon J., Wang Y., Jin Q., Jones K.C., Dobardzic A., Dobardzic R., Bolden J., Essiet I., Brandt W., Russell P.K., Zook B.C., Howard B., Chacon M. 2003. Effect of vaccination with a recombinant fusion protein encoding an astacinlike metalloprotease (MTP-1) secreted by host-stimulated Ancylostoma caninum third-stage infective larvae. Journal of Parasitology, 89, 853–855. DOI:10.1645/GE-46R

    Article  CAS  Google Scholar 

  • Hotez P.J., Diemert D., Bacon K.M., Beaumier C., Bethony J.M., Bottazzi M.E., Brooker S., Couto A.R., da Silva Freire M., Homma A., Lee B.Y., Loukas A., Loblack M, Morel C.M., Oliveira R.C., Russell P.K. 2013. The human hookworm vaccine. Vaccine, 31, 227–232. DOI: 10.1016/j.vaccine.2012.11.034

    Article  CAS  Google Scholar 

  • Hotez P.J., Fenwick A., Savioli L., Molyneux D.H. 2009. Rescuing the bottom billion through control of neglected tropical diseases. Lancet, 373, 1570–1575. DOI: 10.1016/S0140-6736(09)60233-6

    Article  Google Scholar 

  • Loukas A., Bethony J.M., Mendez S., Fujiwara R.T., Goud G.N., Ranjit N., Zhan B., Jones K., Bottazzi M.E., Hotez P.J. 2005. Vaccination with recombinant aspartic hemoglobinase reduces parasite load and blood loss after hookworm infection in dogs. PLoS Medicine, 2, 1008–1017. DOI: 10.1371/journal.pmed.0020295

    Article  CAS  Google Scholar 

  • Mendez S., Zhan B., Goud G., Ghosh K., Dobardzic A., Wu W., Liu S., Deumic V., Dobardzic R., Liu Y., Bethony J., Hotez P.J. 2005. Effect of combining the larval antigens Ancylostoma secreted protein 2 (ASP-2) and metalloprotease 1 (MTP-1) in protecting hamsters against hookworm infection and disease caused by Ancylostoma ceylanicum. Vaccine, 23, 3123–3130. DOI: 10.1016/j.vaccine.2004.12.022

    Article  CAS  Google Scholar 

  • Palmer D.R., Bradley M., Bundy D.A. 1996. IgG4 responses to antigens of adult Necator americanus: potential for use in largescale epidemiological studies. Bulletin of the World Health Organization, 74, 381–386

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pearson M.S., Bethony J.M., Pickering D.A., de Oliveira L.M., Jariwala A., Santiago H., Miles A.P., Zhan B., Jiang D., Ranjit N., Mulvenna J., Tribolet L., Plieskatt J., Smith T., Bottazzi M.E., Jones K., Keegan B., Hotez P.J., Loukas A. 2009. An enzymatically inactivated hemoglobinase from Necator americanus induces neutralizing antibodies against multiple hookworm species and protects dogs against heterologous hookworm infection. FASEB Journal, 23, 3007–3019. DOI: 10.1096/fj.09-131433

    Article  CAS  Google Scholar 

  • Pearson M.S., Jariwala A.R., Abbenante G., Plieskatt J., Wilson D., Bottazzi M.E., Hotez P.J., Keegan B., Bethony J.M., Loukas A. 2015. New tools for NTD vaccines: A case study of quality control assays for product development of the human hookworm vaccine Na-APR-1M74. Human Vaccines and Immunotherapeutics, 11, 1251–1257. DOI: 10.4161/21645515.2014.980199

    Article  Google Scholar 

  • de Silva N.R. 2003. Impact of mass chemotherapy on the morbidity due to soil-transmitted nematodes. Acta Tropica, 86, 197–214. DOI: 10.1016/S0001-706X(03)00035-4

    Article  Google Scholar 

  • Siwińska A.M., Bąska P., Daniłowicz-Luebert E., Januszkiewicz K., Długosz E., Wędrychowicz H., Cappello M., Wiśniewski M. 2013. Cloning and molecular characterization of cDNAs encoding three Ancylostoma ceylanicum secreted proteins. Acta Parasitologica, 58, 112–118. DOI: 10.2478/s11686-013-0116-z

    Article  CAS  Google Scholar 

  • Stoltzfus R.J., Dreyfuss M.L., Chwaya H.M., Albonico M. 1997. Hookworm control as a strategy to prevent iron deficiency. Nutrition Reviews, 55, 223–232. DOI: 10.1111/j.1753-4887.1997.tb01609.x

    Article  CAS  Google Scholar 

  • Xiao S., Zhan B., Xue J., Goud G.N., Loukas A., Liu Y., Williamson A., Liu S., Deumic V., Hotez P. 2008. The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm, Necator americanus. Experimental Parasitology, 118, 32–40. DOI: 10.1016/j.exppara.2007.05.010

    Article  CAS  Google Scholar 

  • Wasyl K., Zawistowska-Deniziak A., Bąska P., Wędrychowicz H., Wiśniewski M. 2013. Molecular cloning and expression of the cDNA sequence encoding a novel aspartic protease from Uncinaria stenocephala. Experimental Parasitology, 134, 220–227. DOI: 10.1016/j.exppara.2013.03.013.

    Article  CAS  Google Scholar 

  • Wędrychowicz H. 2015. Antiparasitic DNA vaccines in 21st century. 2015. Acta Parasitologica, 60, 179–189. DOI: 10.1515/ap-2015-0026

    Article  CAS  Google Scholar 

  • Wiśniewski M., Jaros S., Bąska P., Cappello M., Długosz E., Wędrychowicz H. 2016. Molecular cloning and analysis of Ace-mep- 7 cDNA vaccine efficiency on the laboratory model Ancylostoma ceylanicum–Syrian hamster. Experimental Parasitology, 163, 1–7. DOI: 10.1016/j.exppara.2016.01.006

    Article  CAS  Google Scholar 

  • Wiśniewski M., Jaros S., Bąska P., Cappello M., Wędrychowicz H. 2013. Ancylostoma ceylanicum metalloproteases 6 DNA vaccination induces partial protection against hookworm challenge infection. Acta Parasitologica, 58, 367–383. DOI: 10.2478/s11686-013-0151-9

    Article  CAS  Google Scholar 

  • Wiśniewski M., Lapiński M., Zdziarska A.M., Długosz E., Bąska P. 2014. Molecular cloning and analysis of Ancylostoma ceylanicum glutamate-cysteine ligase. Molecular and Biochemical Parasitology, 196, 12–20. DOI: 10.1016/j.molbiopara.2014.07.003

    Article  CAS  Google Scholar 

  • Zhan B., Liu Y., Badamchian M., Williamson A., Feng J., Loukas A., Hawdon J.M., Hotez P.J. 2003. Molecular characterisation of the Ancylostoma-secreted protein family from the adult stage of Ancylostoma caninum. International Journal for Parasitology, 33, 897–907. DOI: 10.1016/S0020-7519(03)00111-5

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Division of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, Warsaw University of Life Sciences, Ciszewskiego 8, 02-786, Warsaw, Poland

    Marcin Wiśniewski, Maciej Łapiński, Emilia Daniłowicz-Luebert, Sławomir Jaros, Ewa Długosz & Halina Wędrychowicz

  2. Department of Molecular Biology, Laboratory of Molecular Parasitology, W. Stefański Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda St., 00-818, Warsaw, Poland

    Halina Wędrychowicz

Authors
  1. Marcin Wiśniewski
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  2. Maciej Łapiński
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  3. Emilia Daniłowicz-Luebert
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  4. Sławomir Jaros
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  5. Ewa Długosz
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  6. Halina Wędrychowicz
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Correspondence to Marcin Wiśniewski.

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Wiśniewski, M., Łapiński, M., Daniłowicz-Luebert, E. et al. Vaccination with a cocktail of Ancylostoma ceylanicum recombinant antigens leads to worm burden reduction in hamsters. Acta Parasit. 61, 556–561 (2016). https://doi.org/10.1515/ap-2016-0074

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  • DOI: https://doi.org/10.1515/ap-2016-0074

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